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by: Percy Wintheiser


Percy Wintheiser
GPA 3.77

Christopher Kenaley

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Christopher Kenaley
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This 173 page Class Notes was uploaded by Percy Wintheiser on Wednesday September 9, 2015. The Class Notes belongs to FISH 311 at University of Washington taught by Christopher Kenaley in Fall. Since its upload, it has received 36 views. For similar materials see /class/192261/fish-311-university-of-washington in Aquatic And Fishery Sciences at University of Washington.

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Date Created: 09/09/15
BIOLOGY OF FISHES FISH 311 BIODIVERSITY IV TELEOST EVOLUTION CONTINUED PRIMITIVE EUTELEOSTS AND THE RISE OF ACANTHOMORPH FISHES General topics 1 lONUIbUJN Euteleosts the true teleosts Ostariophysi Salmoniformes salmon trout and their allies Stomiiformes and scopelomorphs Where are we Paracanthopterygii cod shes and their allies Acanthopterygii the true spinyrayed shes Atherinomorpha ying shes and their allies 1 EUTELEOSTEI THE TRUE TELEOSTS Now we come to the great Euteleostei containing all the remaining actinopterygian shes something like 33 orders 414 families 4010 genera and 25350 species It is nearly as large as all other vertebrates put together but very poorly characterized eg there is no known unique character present in all contained species there is no hard evidence that all members of this group are closely related ie that all share a common ancestor Much more work remains to be done before a sound classi cation of euteleosteans can be made The Euteleostei is far too large for us to give coverage to all major groups so I39ve chosen to say something about groups that are exceptionally large and therefore warrant discussion andor groups that are commercially important to sheries or to the aquarium trade RELATIONSHIPS OF THE MAJOR GROUPS OF LIVING TELEOSTS TETRAODONTIFORMES l PLEURONECTIFORMES j l 39 1 PERCIFORMES SYNBRANCHIFORMES to GASTEROSTEIFORMES SCORPAENIFORMES ZEIFORMES O GOBIESOCIFORMES LAMPRIFORMES LOPHIIFORMES to BATFiACHOlDIFORMES OPHIDIIFORMES and GADIFORMES as PERCOPSIFORMES SCOPELOMORPHA STOMHFORMES SALMONlFORME CLUPEIFORMES ELOPOMORPHA l I r PHOLIDOPHORIFORMES 2 OSTARIOPHYSI Ostariophysans are the dominate shes in continental freshwaters of the world including ve orders 68 families 1075 genera and about 7931 species roughly three out of every four species that occur in freshwater belong to this group it is represented on every major land mass except Greenland and Antarctica all members of the group are con ned to freshwater except the gonorhynchiform genera Gonorhynchus and Chanos and members of three cat sh families the Ariidae Plotosidae and Aspredinidae Order Gonorhynchiformes the milkfish etc most species without common names 37 species in seven genera and four families restricted to freshwater habitats except for six species and all con ned to tropical Africa except for Chanos chanos the milkfish and members of the genus Gonorhynchus which are found in marine and brackish Gonorynchidae waters of the Indian and tropical Paci c oceans The milk sh is of great importance as a food sh in Southeast Asia in the Philippines Indonesia and Taiwan there is an extensive pond culture Females are highly fecund producing eggs in the millions Order Cypriniformes minnows carps suckers and loaches six families including Cyprinidae the largest fish family with some 2420 species 321 genera and about 3268 species con ned to North America Africa and Eurasia Members of this group have lost their jaw teeth but the lips and toothed upper pharyngeal bones have undergone tremendous specialization and exhibit great morphological diversity Cyprinidae Order Characiformes characins tetras piranhas pacus silver dollars curimatas etc the basis for the freshwater tropical sh trade extremely diverse including 18 families about 270 genera and at least 1674 species con ned to Central and South America Mexico and Africa Adaptive radiation within the characiforms has emphasized innovations in feeding structures especially jaw teeth some have a kind of tooth replacement reminiscent of that of sharks Order Siluriformes catfishes including 35 families about 446 genera and about 2867 species found on all major land masses except Greenland and Antarctica All members have barbels whiskers associated with the mouth Icialuridue Order Gymnotiformes the knifefishes with ve families 30 genera and about 134 species with at least 38 new species waiting to be described and no doubt many more yet to be Q discovered restricted to Central and South America All the gymnotids are specialized in having elaborate electrogenic and GW39WW quot electrosensory structures OK so we have almost 8000 species distributed among the ve primary groups described above What is the evidence that they are phylogenetically related There are a number of characters we could cite but I39ll mention onlytwo 1 Weberian apparatus 2 Alarm substance Schreckstoff The Weberian apparatus discovered in 1820 by Ernst Heinrich Weber professor of comparative anatomy at Leipzig is a complex and unique modi cation of the anteriormost four or ve vertebrae consisting of moveable bony parts called ossicles that connect the swimbladder to the inner ear to allow for sound transmission neural arch pedlcle of lhird verlebra WIlh transverse process neural arch and f spine of fourl rt iquot vertebra 4 neural Complex neural splne clauslrum scaphium inlercalarium parapophysis of slxlh verlebra laleral process Mu cen rum 2 pleural rib centrum lrl us cenlrum 2 p 05 suspensorium pleural rib fossa for parapophysis WW 4 of mm verlebra All but the most primitive ostariophysans have this structure and those few that don39t the 27 species of the Order Gonorhynchiformes possess modi cations of the rst three vertebrae that are thought to represent the beginnings of a Weberian Apparatus So here we have nearly 8000 species sharing a highly complex morphological character complex strong evidence that they all evolved together from the same ancestor Ostariophysans also possess what is called a fright reaction that is elicited by an alarm substance This was rst documented in 1938 by the famous German behaviorist Karl von Frisch who coined the term Schreckstoff to describe the substance and later described in detail by Wolfgang Pfeiffer in papers published in 1963 Alarm substances Experientia 19113 123 and 1977 The distribution of fright reaction and alarm substance cells in shes Copez39a 1977653 665 The alarm substance is a chemical communicant pheromone that is chemically similar in all ostariophysans and is produced by cells of the epidermis Injuries to the skin release the alarm substance which is then detected by the sense of smell causing a fright reaction in members of the same species or sometimes in closely related species This is additional strong evidence that ostariophysans are derived from a common ancestor 3 SALMONIFORMES SALMON TROUTS AND THEIR ALLIES This order contains four suborders 15 families 90 genera and about 320 species Most systematists divide these species into four primary groups Esocoidei pikes pickerals and mudminnows freshwater Northern Hemisphere two families 4 genera 10 species Esociduc Umbridac Argentinoidei argentines herrings smelts deepsea smelts and slickheads marine coastal to deepsea in all oceans six families 57 genera about 202 species JEO Argenfinidao Ban qugidu39 Alepoccphulidac Lepidogalaxioidei the salamander fish con ned to freshwater and found only in Western Australia a single species Lepidogalaxias salamandroides Salmonoidei freshwater smelts the ayu ice shes or noodlefishes New Zealand smelts galaxiids inconnu whitefishes ciscos graylings charrs trouts and salmon 7 families 32 genera about 153 species Osmcriduc phcoglouida Golaxiidut Rdropinnidue Aplochi anidut Salmonidae All members of the Salmoniformes are characterized by having their ns in the primitive state the dorsal and anal ns are short and inserted far back on the body the pectoral ns are low on the body and inserted horizontally the pelvic are abdominal in position Spines are absent scales are cycloid Most are characterized by having a relatively short premaxilla with the maxilla well toothed and forming part of the gape of the mouth Finally many but certainly not all have a adipose n 4 STOMIIFORMES AND SCOPELOMORPHS Now if we look once again at our branching diagram of teleost relationships we nd a couple of small groups called the Stomiiformes and Scopelomorpha We won39t say much about these TETRAODONTIFORMES I L PLEURONECTIFORMES J l PERCIFORMES SYNBRANCHIFORMES to GASTEROSTEIFORMES SCORPAENIFORMES THERINIFORMES 39 GOBIESOCIFORMES ZEIFORMESto LAMPRIFORMES LOPHIIFORMES to BATRACHOIDIFORMES OPHIDIIFORMES and GADIFORMES 58 PERCOPSIFORMES SCOPELOMORPHA STOMIIFORMES C SALMONIFORME CLUPEIFORMES ELOPOMORPHA I 39 T PHOLIDOPHORIFORMES i Stomiiformes deepsea shes found in all oceans of the world characterized by having elaborate bioluminescent organs photo phores 9 families 53 genera and about 391 species All are characterized by having the teleost trends in the primitive state many have an adipose n Scopelomorpha marine shes they are highly variable in habitat occupying inshore coastal areas to oceanic and deep sea found in all oceans of the world 17 families 79 genera and about 482 species Many have bioluminescent structures as well as an adipose n Scopelomorphs are dif cult to distinguish from stomiiforms but a toothless maxilla excluded from the gape of the mouth by the premaxilla is a dead giveaway every time u A n a Omoaudidac Aulapididuc D Alepisuuridan Gonoslomaiida l Synodonlidac Chlorophlhalmiduc M1 Anoioplcriduc Evormannclliduc Melanoslomiuiidac Sccpclurchidul Scopelaanuridac E lpnopidac O 39 mt Paralcpididao Mycthhidac 5 WHERE ARE WE So far in our summary of teleost shes we39ve talked only about the more primitive groups Osteoglossomorpha Elopomorpha Clupeomorpha and the less derived members of the Euteleostei the huge Ostariophysi and the Salmoniformes Stomiiformes and Scopelomorphs We want to now turn to the remaining members of the Euteleostei an assemblage of some 20 orders 311 families 2705 genera and 16168 species Altogether these taxa are collectively referred to as the Acanthomorpha or Spinyrayed teleosts We39ve reached a level of specialization within teleosts at which true spines are present in the ns and at which the other teleost trends that we described earlier are nearly always found in the derived state Within all this great diversity we can identify two major groups 1 Paracanthopterygii 2 Acanthopterygii These two groups are comparable to each other in the sense that both have reached a similar level of specialization TETRAODONTIFORMES I PLEURONECTIFORMES I 1 l PERCIFORMES SYNBRANCHIFORMES m GASTEROSTEIFOHMES SCORPAENIFORMES H mNIFonMEs GOBIESOClFORMES ZEIFORMESm LAMPRIFORMES LOPHIIFORMES to BATRACHOIbIFORMES OPHIDIIFORMES and GADIFORMES l PEHCOPSIFORMES SCOPELOMORPHA STOMIIFORMES SALMONIFORMES CLUPEIFORMES ELOPOMORPHA I t PHOLIDOPHORIFORMES 6 PARACANTHOPTERYGII THE CODFISHES AND THEIR ALLIES Branching off just beyond the scopelomorpha is a group of six orders that appear to be closely related to the exclusion of all other remaining teleosts This is a superorder called the Paracanthopterygii which contains ve orders 36 families 270 genera and about 1340 species Order Percopsiformes troutperches pirate perch and cavefishes con ned to freshwater habitats of northern North America 3 families 7 genera and 9 species Order Gadiformes cods codlets hakes burbot rocklings and grenadiers or rattails marine very rarely freshwater shallowwater to deepsea pelagic and benthic in all oceans of the world 3 suborders 9 families 75 genera and about 555 species Order Ophidiiformes cusk eels pearlfishes and brotulas marine very rarely in brackish or freshwater associated with the bottom in shallow water to deep sea in all oceans of the world 5 families 100 genera and about 385 species numerous undescribed species are known Order Batrachoidiformes toadfishes marine primarily coastal and benthic rarely entering brackish water a few species con ned to freshwater found in all oceans of the world a single family 22 genera and about 78 species Order Lophiiformes angler shes marine shallow to deepsea pelagic and benthic in all oceans of the world 5 suborders 18 families 66 genera and about 320 species Gadidau Batrachoididac Lophiidac The Paracanthopterygii is relatively new having been rst recognized in 1966 the concept supported with additional evidence in 1969 and recon rmed in 1989 Over the years the group has been plagued with problems and confusion the major dif culty being the lack of unique characters shared by all members of the group The prevailing thought is that the caudal skeleton of paracanthopterygians has evolved in a unique way a sequence of evolutionary change that helps to de ne the Paracanthopterygii as a group and to separate it from the more derived Acanthopterygii Note in the following diagram that Myctophiformes is equivalent to Scopelomorpha EVOLUTION OF THE CAUDAL SKELETON IN ADVANCED TELEOSTS Evolution of the caudal skeleton in the advanced neoteleosts The arrows connecting the different types indicate possible structural changes not phyletic lineages The epurals are stippled the second preural neural spine crest is black The primitive configuration of the caudal skeleton is exhibited in the Myctophiformes in the Paracan thopterygii the most anterior epural fuses with the second preural neural spine crest Further specializations involve the fusions of the hypurals into platelike elements In the Acanthopterygii fusions occur of two preural vertebrae of which one has a complete neural spine and the other a reduced or no neural spine crest The result of this vertebral fusion is a caudal skeleton configuration which is convergent to that of the Paracanthopterygii Among more specialized Acan thopterygii fusions occur of the hypurals to form hypural plates 7 ACANTHOPTERYGII THE TRUE SPINYRAYED FISHES Let39s turn now to the Acanthopterygii a huge assemblage of some 13 orders 267 families 2422 genera and about 14797 species Great problems of de nition exist with this group as well in fact the diversity is so great and so poorly understood that most ideas about evolutionary relationship are not well supported There is one character however that appears to tie at least the primitive members of the group together the retractor dorsalis muscle I D b D 9139 t 039 w 394 RETRACTOR DORSALIS MUSCLE P83 P82 P81 39 E3 E3TPF I Dorsal gill arch elements and the retractor dorsalis RAB muscle in the acanthopterygian Epinepheus ventral vIew Muscle Is Inserted on the upper toothplate UPSF fused to the third pharyngobranchial P83 The retractor dorsalis muscle is a large paired muscle that originates along the ventral margin of the anteriormost three or four vertebral centra and inserts on the dorsalmost parts of the gill arches The muscle mctions to retract or pull back on the upper pharyngeal teeth as part of a chewing mechanism that prepares food for swallowing In acanthopterygians insertion of the retractor dorsalis muscle is con ned to the dorsalmost aspect of the third gill arch only ie on the third pharyngobranchial In addition in acanthopterygians the second and third epibranchials are enlarged to form the principal structural support for the upper pharyngeal jaws The Acanthopterygii consists of two primary groups 1 Atherinomorpha ying fishes and their allies 2 Percomorpha perches and perch derivatives 11 8 ATHERINOMORPHA THE FLYINGFISHES AND THEIR ALLIES Atherinomorphs have a nearly worldwide distribution in both tropical and temperate regions about 25 of the species are marine 75 live in fresh or brackish water most are surface feeding shes 2 orders 18 families 168 genera and about 1080 species Order Cyprinodontiformes flyingfishes halfbeaks needlefishes sauries rice fishes rivulines killi shes goodeids foureyed fishes topminnows and live bearers 0r guppies found around the world in tropical and temperate marine and Order Atheriniformes silversides rain bowfishes and phallostethids primarily marine but some in freshwater found around the world in tropical and temperate regions six families 48 genera and about 312 species freshwater habitats 15 families 145 genera and about 1240 species s Exocodidac Horuichihyiduc Mclum ucniida o o a Cyprinodonlidao Exoeodidac Aibcrinidac Bolanidan Scombcruacidq lsonidqc U J Anoblcpidac Poceiliidan Ncoahlhiduc Phallodcihiduc Adriu nichihyidcc There is considerable evidence that atherinomorphs form a natural assemblage ie that all members of the group share common ancestry All members share a specialized feeding mechanism that allows for upper jaw protrusion but the protrusion differs from that of other acanthopterygians in lacking a ball and socket joint between the palatine and maxilla There are also peculiarities of the crossed ligaments that extend between the palatine bones and maxillae These modi cations prevent the premaxillae from being locked in the protruded position but seems to allow the left and right premaxillae to undergo independent movement during upper jaw protrusion BIOLOGY OF FISHES FISH 311 FORM AND FUNCTION FEEDING MODES AND MECHANISMS PART II HOW FISHES GET THEIR MOUTHS OPEN AND CLOSED FEEDING IN A LIE ANDWAIT PREDATOR General topics 1 Gape and suck feeding 2 The hyoid coupling of primitive actinopterygian shes 3 The opercular coupling of derived actinopterygians 4 Closing the mouth 5 How do we know how shes open and close their mouths 6 Evidence for ultrafast feeding in a lie andwait predator 1 GAPE AND SUCK FEEDING Generally speaking the vast majority of living shes are gape and suck feeders They feed by opening the mouth while simultaneously lowering the oor of the mouth and expanding the sides of the mouth cavity This great and sudden increase in volume creates negative pressure Le a vacuum which in turn results in a sudden rush of water into the mouth When directed adequately by the predator it39s this sudden rush of water that carries or pulls prey into the mouth to be swallowed Neurocranium m Levator hyomandibulae m Levator operculi 0 ercular a aratus Suspensorlum D W lnterhyal Lower jaw Hyoid apparatus m Protractor hyoideus Clelthrum m Sternohyoideus When the jaws are closed the water and whatever it contains stays in the expanded oral cavity water and hopefully prey do not pass out through the mouth A pair of membranous valves just inside the upper and lower jaws present in most shes helps prevent water from escaping anteriorly These are called oral valves Once the jaws are closed the oor of the throat is raised and the cheeks or sides of the mouth are contracted forcing the trapped water out through the gills Any food item contained in the water is strained out by the gills particularly the gill rakers and passed back into the opening of the esophagus to be swallowed All of these various movements of the jaws and the mouth cavity are made possible by a complex series of interlocking bones and tendons and muscles attached to them The complexity is increased by the fact that there is often more than one way to accomplish essentially the same movement So let39s look in some detail at how shes open their mouths 2 THE HYOID COUPLING OF PRIMITIVE ACTINOPTERYGIAN FISHES In primitive actinopterygians ie living sturgeons paddle shes and even in gars the lowering of the mandible or opening the mouth seems to be entirely dependent on lowering the oor of the throat These primitive forms have only one means by which they can open the mouth a biomechanical coupling called the hyoid coupling In levator operculi EDaXIaIIHUSC 39 lnterhyal Cleithrunt Hypaxiallnusc nL Sternohyoideus Lower jaw depression is initiated by contractions of body musculature the epaxial musculature above and the hypaxial musculature below Contraction of the epaxial musculature which inserts on the rear of the cranium causes the head to rotate upward relative to the body axis Contraction of the hypaxial musculature a large part of which inserts on the cleithrum causes a backward and downward rotation of the pectoral girdle Anteriorly the cleithra one on each side are attached to the hyoid apparatus by a strong muscle called the sternohyoideus this muscle contracts as well so that the backward and downward movement is transmitted to the hyoid Finally because the hyoid lies between and is attached to the elements of the lower jaw by skin and ligaments the downward and backward pull on the hyoid apparatus is transmitted to the lower jaw This mechanism is then an indirect way of opening the mouth Any opening of the mouth is preceded by a downward and backward movement of the oor of the mouth This results in an expansion of the oral cavity which in turn creates suction water is drawn into the mouth as the lower jaw is depressed 39 Opercular apparatus This is simply a primitive gape and suck feeding mechanism found today in living sturgeons paddle shes and gars And as you know most shes rely on this creation of negative pressure inside the mouth cavity to pull prey and the water that surrounds it into the mouth The effectiveness of the suction in capturing prey depends on two things 1 The degree to which the mouth cavity can be expanded 2 The suddenness with which the mouth cavity can be expanded 3 THE OPERCULAR COUPLING OF DERIVED ACTINOPTERYGIANS OK we39ve described the biomechanical coupling responsible for opening the mouth in primitive actinopterygians What about derived actinopterygians In turns out that the bow n genus Amia and teleosts have developed a second moreor less independent system for opening the mouth that supplements the coupling just described for primitive actinopterygians called the opercular coupling m levator operculi EDBXIal muse Upper jaw Opercular apparatus Lower jaw lnterhyal m Protractor hyoid39eus cregthrum Hyoid apparatus Hypaxial musc m Sternohyoideus Opening of the mouth with the opercular coupling is initiated by contraction of the levator operculi a muscle that originates on the cranium and inserts along the dorsal margin of the opercle This causes the opercle to swing up and backward Since the subopercle and interopercle are attached to the opercle this movement is transmitted ventrally throughout all the elements of the opercular apparatus In turn the interopercle pulls back on the lower jaw by means of a strong ligament that has developed between these two bones b So in addition to the indirect hyoid coupling inherited from primitive actinopterygians the bow n and teleosts have evolved a second moreorless independent and direct mechanism for opening the mouth one that does not involve the creation of suction What good is it Because this new opercular coupling does not involve the creation of negative pressure ie suction its development was a necessary preadaptation for those kinds of shes that browse along nipping at rocks and coral picking up small prey from soft bottoms forms that bite off and crush chunks of coral shes like surgeon shes parrot shes wrasses trigger shes and a whole host of other perciform taxa m levator operculi Opercular apparatus 39 Interhyal Cleithrum Hypaxial musc m Sternohyoideus So what we have here is a whole new way for shes to feed that does not involve the old gape and suck approach but if they need to gape and suck they have that ability as well 4 CLOSING THE MOUTH Getting the mouth closed is relatively simple It is accomplished by contraction of a large complex muscle called the adductor mandibulae cheek muscles which is usually divided into three or four separate sections It originates on the bones of the suspensorium and has a complex insertion primarily along the length of a long ligament that stretches between the head of the maxilla and the inner surface of the lower jaw This ligament is called the primordial ligament Levator operculi Adductor EanIal musc mandibulae Primordial Ligament Protractor hyoideus Hypaxial musc Sternohyoideus The adductor mandibulae is a very important muscle because all movement related to feeding whether it be full gape and suck or simple nipping grasping or crushing as well as respiration depends on it The size and shape of the adductor mandibulae varies greatly among teleosts and it is a widely used character complex in systematic studies especially in comparing higher taxonomic categories A B 5 HOW DO WE KNOW HOW FISHES OPEN AND CLOSE THEIR MOUTHS Early studies in functional morphology relied on simple dissection and manipulation of dead organisms Function was routinely extrapolated from form and structure For example if you opened up a sh and found a big muscle properly connected to perform the function in question you simply declared that that is the function of the muscle Somewhat later experimentalists began cutting ligaments and tendons of living aquariumheld shes to see how the decoupling of various elements altered function This is how the two biomechanical couplings described above were rst discovered by Ballintijn and Hughes in 1965 See J Exp Biol 432349362 This rather crude approach was replaced in the late 19605 and early 19705 by technical advances in electromyography and xray cinematography and now of course we have highspeed video which has greatly enhanced our ability to see and describe the sequence of events that take place when a sh feeds or for that matter performs almost any function E9 E lt23 T I l MAXILLA UPPER ZElt m m SUSPENSORIUM r Pd ivR39USION GIRDL E m mac I E L quot p IrlMLj D PECTORAL Ll k L HYOID GIRDLE l E7 9 MOUTH Structural network in the head of a primitive E 4 NEUROCRAN39UM a OPEN39NG actinopterygian A a primitive halecostome B and a percomorph C to show the biomechanical path r ways governing mouth opening suction feeding and jaw protrusion functions Homologous biomechanical OPERCELUM MAND39BLE pathways are similarly numbered Note the increase in Complexity of the structural network in actinop L MEJ terygian evolution Only the function of jaw protru NTEROPERCULUM NM sion is shown in C the primitive functions of mouth HYOID opening and suction feeding are omitted for clarity i G FEEDING MECHANISMS IN RAYFINNED FISHES M V k GP J39l4H 3 Prey capture in Amia calva as seen in lateral A and ventral B views This gure is traced from frames of highspeed lms of two separate prey cap ture events Modi ed from gures 13 and 14 of Lau der l980a Note the delay in opercular and bran chiostegal expansion until the mouth is nearly completely open and the anteroposterior sequence of peak excursion in mouth opening hyoid depres sion and opercular dilation Abbrevations GP gular plate MX maxilla OPERCULAR DILATION cm ob oo I f T 39T 1 l I l I I l I OPERCULAR LEVAT ION cm club F I Fquot39T 40 20E HYOID ANGLE degree I 0 I l 20 LOWER JAW ANGLE degrees 10 I I O I l 40 ANGLE OF MAXILLA degrees 20 I l I MOUTH OPENING cm 15 17 19 21 23 1 3 5 7 911 13 FRAME NUMBER TIME Ll 10 ms Pattern of jaw bone movement in Salvelinus fontmalis to illustrate the primitive halecostome ki nematic pro le The relative sequence of bone move ment at the strike is very similar in all predaceous halecostomes that have been studied experimentally see text 0n left lateral and ventral aspects of the ce phalic musculature of Serranochromu rabuslus 13 de plcted In the center representative myog rams taken dur mg the capture of a slow moving goldfish Surrounding the myograms are tracings of frames of a high speed mo tlon picture Frame numbers l16l accompanying the trac lngs correspond with the numbers Indtcated at the top of the myog rams The three phases are the preparatory pl expansive tel and compresswe lcl Major movements of the cephalic components between successn e frames are Indicated by arrows During the preparatory phase Jaws are tlghtly closed and the orophary nx compressed whtle the expansive phase is charactertzed by an explosive unfoldlng and law opemng mutated by the levator oper Cull ILOl muscle and Immedlately followed by the epaxml tEM sternohyondeus lSHl hyanIal MW and levator arcus palatim LAP and dllatator operculi DO muscles During the compressn e phnse the Jaws are closed at htgh veloctty by the adductor mandibulae complex lAMl3I and the oropherynx compressed by the sdductor arcus palatlm lAAPl and gemohyoxdeus anterior CHM and postenor IGHPl muscles At frame 6 the elements have returned to than resnng condition ESOX CH DEGLUTITION I PCi Ell LE1 mgr U I l p I l 39l m A05 pee l 1 1 SH l 50ms 1535 D AMBLOPLITES MANIPULATION DEGLUTITION GH lL megL l 4 U LE4 L J Fquot1 pH J L 50 ms 100 ms Diagrammatic view of the pharyngeal jaws and their relation to the skull in A Esox niger and B Ambloplites rupesms Heavy lines indicate pharyn gealjaw muscles and their approximate line of action Thin lines represent the branchial basket Black bars represent electromyographic activity in selected bran chial muscles during manipulation and deglutition white bars indicate occasional activity The short ver tical line anterior to levator externus one connects the gill basket with the neurocranium and represents pharyngobranchial one Note the two salient special izations which distinguish advanced euteleosteans such as Ambloplites from more primitive forms Esox l the shift in origin of the pharyngohyoideus muscle PH t0 the urohyal and 2 the occurrence of a re tractor dorsalis muscle RD Abbreviations AD5 fth branchial adductor GH geniohyoideus LEI 4 levator externi muscles PCi e pharyngocleithralis internus and externus muscles PH pharyngohyoi deus RD retractor dorsalis SH sternohyoideus SCIENTIFIC AN June 1990 Volume 262 Number 6 SCIENCE IN PICTURES Frog shes Theodore W Piemuh and David B Grabecker Beautifully camouflaged as rock coral or some other feature of the aquatic landscape these sedentary superpredators display a modified fin that acts as a lure When the prey is within range they engulf the meal in milliseconds SCIENCE IN PICTURES Frog shes Masters of aggressive mimicry these voracious carnivores can gulp prey faster than any other vertebrate predator by Theodore W Pietsch and David B Grobecker n the morning of December 29 1696 a Dutch captain and his crew were searching for the survivors of a ship that had gone down not far off the coast of Western Aus tralia Although no sunavors were ever found what the crew did find washed up on the shore of a nearby island amid rats as big as house catsiwas a most remarkable fish The Fish unlike any the sailors had ever seen was de scribed as being about two feet long with a round head and a sort of arms and legs an even something like handsquot There is no doubt in our minds although its specific identity will never own t this strange sh sketch ily described so long ago was a og sh Aptly named these unusual fishes do bear a surprising resemblance to frogs their bodies which range in length from one to 16 inches are glo hose and equipped with welldeveloped leglike fins that enable them to clam TlLEODORE W l lETSCl l and DAVID E GROBECKJZR have collaborated on a number of research projects Pietsch is professor of fisheries al the University of Washington where he has been a member of the faculty since 1978 in recognition of his work on the systemab ics behavior and ecology of marine flSh39 es he has been made a lellow of the Lin nean Society of London and also of the California Academy of Sciences Pietsch has a 85 from the University of Michiv gan and a PhD from the University of Southern California Grobecker is now scienti c director of the Pacific Ocean Research Foundation in Kailua Kona Hawaii before that he was a graduate student working with l ietsch in Seattle Grobecker has a HS from California State University Long Beach and a PhD from the University of Washington 516 SCIENTLI39IC AMIIRJCAN june 1990 butquot across rocks sand and coral reefs much as a tetrapod might move about such as a piece of coral m39thin a mat ter of days in some species m ihin a matter of seconds As a result a frog fish that moves from one type of sub strate to another can change its color and s blend in with its surrounds ings For that reason most frogt39ishes are virtually impossible to distinguish from their backgrounds and so many are overlooked not only by their pred ators but by experienced divers and ichthyologists as well Commerson39s frogfish Antennarius commersoni which is widespread in the Indian and Pacific oceans is repre sentative of the group in many ways Males and females occur in a wide range of colors including red yellow brown creamy white black and vari ous hues in between their skin more over is accentuated by a regular pat tern of small brown spots and pink blotches In shallow water where streaks of sunlight mottle the ocean floor the fish bears a remarkable almost un cannyiresemblance to an algaeen crusted rock And there it sits the clas sic example of a hour ail predator ready to strike at any fish or crus tacean that passes by Should a suit able animal swim too close the large cavernous mouth of the lquotroglquotish opens engulfing its hapless victim in a matter of milliseconds Masten ng the art of mimicry has thus imbued frogfishes with an impor tant evolutionary advantage By ap pearing to be inanimate frogi39ishes are not only overlooked by those that prey on them but they are also overlooked by their own prey in addition they are PAINTED FROGI ISH Anteunarius pic tus lives in the warm ihalIow waters surrounding the Hawaiian islands Like surprisingly effective at enticing prey within striking distanccin large part because they possess a small append age called a lure that projects forward from just above the animal s lip and can bc viggled when prev come into view As long ago as 344 B Aristotle re marked on the role of the lure quotThe fishmgfrog has a set of filaments that project in front of its eyes they me long and thin like hairsand are used as baitsquot Those observations were re confirmed in l875 by the Reverend S l Whitmee of Samoa who described angling in a frogl39ish It angledf0r all frog75h species it attracts prey by wiggling a lure which is a modified elongated dorsal n spine The ere extending diagonally upward between the sh39s eyes termi some of the small sh in the aquarium t hoped to see it catch one but they were too waryquot Whitmee39s observations which were later substantiated by others represent a concept in behavioral biology that is known today as aggressive mimicry ltnlike pa mimicry whereby can39t ouflage or resemblance to one39s back ground provides a certain degree ot protection from one s predators ire gressive mimicr t uires that an an imal imitate a spt 39 object both physically and behaviorally in order to gain some advantage from II in other r lure seen h words by mimicking not only an llt u li39 mate object but also the behauor and appearance of a particular food item a 39rogfish can lure another animal into its strike zone Studies we have carried out no indicate that the irogt ish with its wide array of specialized adap rations is one at nature s best tmost ltiullh exolwtll examples of aetires mimic ies belong to the family n which in turn belongs to a t 01 bony t39ishcs the s the name tmplte an 39gely sedent39 y lietn E y r m I I 3 c Hales in a structure called the gym or bait Animals that are tracth to the lure mouth 0quot the l ragish are engulfed in a matter of39 milliseconds and came too close to the cavernous wait predators that attract prey with the aicl ol a lure in the case of t39rogt39islr es the lure a highly conspicuous exr tension of the rst spine of the dorsal Fin sways forward from the face uni tilting the jigging action of a fisher rnan39s rod In some species the entire apparatus cam lie l39oltlecl back into a nar rcm groove on top of the head and thus the lure is protected when not in use Lures which van trotn spec species cot 39I ot two major parts the spine itself and a conspicuous tleshv structure at the tip calletl the 391 or bait Depending on the spectes the Stumtttt Mutual tune Ith 397 FROGFISHES belong to a large and diverse family the An h a 39ngs w it than 100 years ugoiindicate From left to right at the tap tennariidae as t e have drawn esca may range in size and shape from a simple ball of tissue perhaps 116 of an inch in diameter to a highly ornate and lamentous structure an inch or more in length in some species the esca mimics a small fish in others it seems to mimic a crustacean or a worm Although widely distributed in tropi cal and subtropical waters around the world including the Gulf of California and the Red Sea the vast majority of frogfishcs are confined to the coastal areas of Indonesia the Philippines and various other island groups of the South Pacific One species Histria his lrio lives ami eating sargassum weed the remainder spend their lives either on the ocean bottom in areas where the water is shallow to moder ately deep or on rock or coral reefs Most taxonomists now agree that c taxonomic confu sion can be blamed in part on the amount of variation in both color and pattern that occurs within a single species Individuals have the ability to switch Tl 39 or two Such back and forth between two color 98 SCILN39ITI39IC AMLRK39AN Iunu 1090 the species shown are Commerson39s frag sh Antennarius L were made more I the phases a light phase usually yellow or tan and a dark phase often green dark red or black Although the light phase seems to predominate in most habitats for reasons that are not well understood it is not uncommon to nd an area where the entire color range for the species is represented The striated frogfish Antennarius sm ams for example maintains at least four distinct color phases a green phase during which it looks very much like an algaecovered rock an orange phase during which it has the appear ance of an orange sponge a white phase during which it seems to mimic a white sponge and a black phase when it is reminiscent of a black sponge We surmised that such marked change in color must occur when the fishes move to a slightly different habi tat say a region of the coral reef where orange sponges rather than white ones predominate In order to test the response of frog fishes to background visual cues we devised an experiment involvtng two species the tuberculated frogl ish Art terminus tuberosus and Commerson s l rogfish A cummersani We placed in striated f f suiatus the tasseled frogfiSh Rhycherus filamentosus and the painted dividuals in separate observation tanks and after a period of habituation changed the color of the gravel sub strate from white to black and also added rocks and coral in various color combinations to the tank Although the tuberculated frogfish changed from dark gray to light cream and Commer son s frogfish changed from lemon yel ow to brick red we were unable to de termine the precise stimuli responsible for the color transformation Clearly er stu 39es under natural field con ditions are necessary VARIATION IN PIGMENTA39HON can be quite marked within a single species of spat frogfish Lophiocharon trisignatus the New Guinean frog sh Amenn arius dorehensis the warty fragfish Antennarius maculatus and the striated frogfish We do know that the t39rogfish is a ma racious and highly successful predator Not only is it virtually indiscriminanl in its dietary preferences but it will at tempt to swallow anything within strilc ing distance including animals slightly bigger than itself By studying the Feed in behavior of l39rogfishes we have de termined for example that a l39rogl39ish can enlarge its mouth by a factor oi 13 moreover it can do so in about si milliseconds less time than it lakes or a normal striated muscle to con traet We have also analyzed locomo tion in these fishes which ranges from across the substrate to jet Our studies which have been carried out both in the laboratory and at field sites off the coast of Oahu Hawaii and in Sydney Harbor Australia during the past 15 years have enabled us to amass varying amounts of behavioral and ecological data for eight different species Commerson s l rogl ish the striated l rogfish the tuberculated frog fish the hispid frogfish A IiispidLIS the rvarty trogt39ish A mneulutus the scarlet l39rogi39ish L tl caccineus the bloody t39rogt39ish A snnguineusl and the threespot frog sh Lophiocharon Irisiymitust Ve began our research by analyzing luring behavior in particular we want ed to knon whether luring directly intlu enCes the kinds of prey that a rogfish captures ci 39 quot that is does each species 01 frogfish have a morphologically unique lure And is there a correlation between the appearance of the lure and diet that is does the lure resemble the preferred food items of the species attracted to it The shape and size of the lure it seems are Lulique to most specie 39 in fact a species can often be identitied on the basis of its lure alone The esea of the striated t rogt ish looks some thing like a polychaete worm whereas the esca ol39 the hispid l39rogfish resemv bles a tube worm In contrast the we ty i rogi39ish has an esca that looks like a small fish Commerson s l roet39ish has a shrimplike one The effecu39veness of the lure is based on more than just appearance how ever A frogfish must wiggle and ma nipulate the lure in ways that simulate the natural swimming movements of the animal being mimicked The fisl t like lure of the warty frogfish for ex ample ripples as it is pulled through the water and so mimics the lateral un dulations of a swimming l39ish lsee lllllS trntion on next mtg e We hypothesized that such morpho logically distinct litres might reflect a highly specialized diet After all it seemed reasonable to suppose that a striated frogfish with its wormlike esca might teed primarily on species that normally prey on and are there fore most attracted to polyehaetes or other marine worms To test our hy pothesis we decided to analyze th stomach contents of four species i pictus A commersont39 and llntemmtns hiberasusi Somewhat to OLLt surprise our study revealed that frogfishcs are not specialized l39eeclers I39rogfish It is thought that inclivitluuls Change color to mimic particular objects in their environment such as melts wont es or pieces o wml Only four of many color and pattern phases of the painted frogfish At pictus are shown here 539ltttlll lt tllRlCN lime 11190 till APPEARING T0 MIMIC its background in his case an algaeencrusted ruck top the warty frogfisli A maculatus sits for hours waiting for potential prey to swim by The in ol ihe lure called the esca varies 39om species to species but here it re sembles a small fish middle If another animal comes into View the frogfish wig gles its lure bottom in a way that mimics the movements of a small sh 00 SCIIZN l39ll IL AMERJLZAN June 199 but eat a highly varied overlapping as sortment of prey Our findings were unexpected Why we wondered should evolution favor such complex and apparently species specific lures when the average frog fish is successful at attracting a wide variety of prey One possible explana tion is that food acquisition in the ma rine environment is both unpredictable and complex Many individuals will randomly enter a frogfish39s strike zone wilhout being specifically attracted to e lure others are attracted to the area not by the wriggling lure but by the frogfish itself which may be misi taken for an appropriate site such as a piece of coral on which to lay eggs graze or seek shelter Another possibility is that the lure may elicit a defensive or territorial re sponse from nearby fishes In a labora tory experiment involving the damsel fish Dascyllus aruamis we observed that individual damsell ish placed in the same tank as a frogfish would re peatedly direct aggressive displays to ward the lure On several occasions in what seemed to be an overly aggressive attack a damsett39ish entered the strike zone of the l rogl ish and was eaten Capture under those drcuinstances is instantaneous indeed almost an fish that swims within the strike zone an area w ose ra ins is rou hl 39 tw thirds the length of the frogfish has little chance of survival To our knowl edge a frog sh can extend its mouth and engulf its victim at a speed greater than that of any other vertebrate pred ator In fact such rapid prey capture is perhaps the most remarkable of all the frogfish39s attributes With the aid of such modern tech niques as highspeed cinematography we have spent a considerable amount of time analyzing the biomechanics of Feeding in three species A striarus A hispidus and A maculat39us By integrat ing franiebyl rame analyses of high speed film from 800 to 1000 frames per second with anatomical analyses of the bones muscles and ligaments in the fish39s head we have come to real ize that prey capture in the frogfish in volves a highly choreographed se quence of behaiiors Threc functionally distinct phases can be identified Phase one consists of prestrike behavior phase two is the strike itself and phase three is prey ma nipulation which involves swallowing During the preSlI ikC phase prey are followed visually until they come with in a certain distance about seven body lengths of the frogfish At that pointx the i39rogfish begins wiggling its lure If IOGRAPH shows that the longlure frog75h A multiDCel latus has swallowed u scorpion fish Pontinus 10 which is the prey responds by approaching the lure the Progfish then enters the strike phase If the prey does not respond the l rogfish mat start moving toward it quotrapidly at fits but then much more slowly During the slow phase the frog l39t39sh flattens its body into what loolts like a crouchi g position doing so pre sumably renders it less conspicuous to its victim When the targeted prey is about one body length away the frog l39ish now in the strike phase orients it selt39by twisting or rocking its both into the proper position for attaelt 39l39he trogi39ish watts or the prey to en ter its strike zone and then lifts its head and opens its mouth hy depress ing the lOWel39JHW at the same Lune that it expands the upper jaw In that con figuration the mouth forms an extend ed tube which sucks a Victim inward in much the same way that a vacuum cleaner pulls dttst from a carpet Once the prey is taken into the mouth the l roel ish enters the preyvmanipttlation phase As the prey i s allowed a large quantity of water is also ingested which facilitates the passage of large prey into the l39rogl39islt s gullet When swallowing is complete excess water is ejected through the gills artd a sphincA ter muscle at the base at the esophav pus closes which prevents the prey from escaping This method of prey capture which is practiced by most 01 the world39s E longer than itself A frog sh can swallow such large prey be cause its mouth expands in Size by a factor 012 or more fishes is known as gapeandsuclt feed ing The underlying principle is a sun ple one negative pressure suction is created by the rapid expansion of the gill cavity and mouth which creates an inward flow of water and so increases the speed with which prey are en gttlfed Unlike l astswiimnlng preda tors that incorporate body speed to en gull39 prey the lieirtwait predator de pends on the rapid expansion ot its oral cavity in order to surprise and can tune its prey The gaperandsuck preda tor can also feed on pre without adA ertising its presence to other potential prey tsh in close proximity to one an other for example are often apparent ly unaware of the sudden loss of one of SctttNttt39tt AMI39RICAN June 15M 10 FROGFISH39S MOUTH remains closed left comes within Striking distance The 39 their neighbors and so remain vulnera ble to repeated strikes by a liein wait carnivore The difference between frog shes and other shes is the degree to which the mouth expands as well as its rate of expansion We have determined by t is gt3 Awe5 39 m 39Lh FROGFISHES MOVE across the substrate with the help of leg like ns They do so either by quotcrutchingquot top or by walk ing bottom When crunching the sh moves forward by resting its weight on the pectoral ns 8 the pelvic ns b 102 705 the muscles of its upper and lower body and throat which causes the head to li and the mouth to open right these SCIENTTFIC AMlZRlL39AN June 1990 until suitable prey ish then contracts injecting liquid paraf n into both the closed and fully expanded mouths of preserved fishes that frogfishes can expand their mouths to a much greater extent than other gapeandsuck feed ers The European perch Perm uvia n lis for example expands its mouth same muscle contractions cause the upper jaw to push out ward and the lowerjaw to descend As the mouth expands it extends forward a process that takes about six milliseconds which enables the frog sh to sack in its victim by only a factor of six when feeding Moreover the frogfish39s mouth ex pands with incredible rapidity Analy ses of highspeed lms indicate that the hispid frogfish opens its mouth and engulfs its prey in less than six milliseconds Similar times were meas hear the animal39s weight only while the pectoral ns are be ing repositioned When walking the frog sh alternates its pectoral ns pushing forward rst with one then the other much as humans move their legs when walking tired for the striated and varty frog l39ishes By comparison the stonel ish Synanceia vet39rucoxtt which is thought to be the next fastest gapeandsuck feeder requires 15 milliseconds and the European perch needs a fill 40 milliseconds We wondered about the mechanism that makes such speed possible Do frogl39ishes have specially modified jaws A unique set of muscles What accounts for their remarkable prey capturing ability To answer those questions we dissected the heads of several species and carefully examined the muscles responsible for optming the jaw Our results were unexpected there are no significant structural dil l39et ences between the jaw muscles of frogi39ishes and those of other verte brates Moreover we found no signii ir cant differences in bone structure Although we have yet to determine the means by which lrogl39ishes open their mouths so quickly we suspect that a Currently unknown mechanism maybe responsible Perhaps frogfishes ess a biomechanical feeding mech anism similar to the mechanism in l39leas that enables them to store elas tic energy in the thorax and so jump to incredible heights see The Flying Leap of the Fleaquot by Miriam Rothschild et 211 ScrEN39nrtc AMIZR ber 19731 is it not posstble that frog t39ishes have a catapault mechanism in the jaw that enables them to store elas tic energy and then quickly release it 1 We think such a modification may ex ist although further studies are needed to confirm our hypothesis The family Antennariiclae enjovs many other highly complex and i39asct nating adaptations including novel forms of locomotion To move across the substrate either in pursuit of prey or in search of a new resting site l39rog fishes rely on one of two tetrapodlike gaits One is reminiscent of a person 0 ehes the pectoral fins like crutches bear the weight of the fish39s body as it moves forward only at the end of the stroke weight transferred briefly to the pelvic l39ins The other gait superficially resembles the walk of ter restrial vertebrates which ambulate by mon ng alternate limbs The pectoral fins provide power For walking while the pelvic fins serve only to stabilize the Fish Frogl ishes also swim doing so by undulating their body as diey move Ln addition they often jet propel thenr selves through the water a feat the fishes accomplish by ingesting large amounts 0139 water antl then forcing it backward through gill openings llltral39ast l39eeding mechanisms jet t GEOGRAPHICAL DISTRIBUTION or froglshes i orem abun 39 tropical waters They ost pines and other island groups of the South l uctftc Few we or south of the region indicated in color a 1 I the map most prefer areas where the average annual waterSurface temperature is greater than 20 degrees Celsius m OSTEOGLOSSO v MORPHS TARPONS AND EELS Wig HERRINCS AND ANCHOVIB r SALMON AND TROUTS 4 PERCHES ANGLERFlSHES AND FROCFISHES CODFlSHB E AND HAKES 0 39 quot MINNOWS 7 CHARACINS 39 AND cmnsnes DIAGRAM of the evolutionary relationships among hony shes the 21905 sh es indicates that anglerlines are most closely related to codishes and hakes propulsion and aggressive mimetic de vices by themselves are not unique to t39rogfishes each adaptation can be 39ound in a wide variety of other fish species Yet in no other group are so many highly evolved and complev adaptations integrated into a single or ganism it is not just the ability to lure prey or to change color or to clamber across the substrate that makes frog fishes so interesting More important perhaps is that natural selection has I39avorecl the evolution of so many spe cializaLions within a single Iquot 39 of fishes Understanding the specialized morphological and behavioral adapta tions of Lhese aggressive mimics is7 without questionia challenge that will continue to occupy investigators for many years to come quota FUR l HER ltFDlNG Mttt names or H 39 ll Vt oils TL iost antler in journal of Part ages lt Ct ltN39L t39ott til i ANILNNARHU ltNillltllll t irohecker an Theodore W l ietsch in Science Vol 203 No ttl 1 pages 1 til tlt5215eptenther 11 970 int quotlllquotlNV ITquot FllllNLi Moor or A L39itvrttt39 quot 39 SlN1N FRRII cost 1 It Grobetker ll enml Biology u Fishex Vol 8 No 34 pages l l2i 39l 8 3t FRUGI39ISIII S HT HI URL 5 Q39l39llMAT l 39 t 39 Likl ll Nl ill ll 39lRrl e l it39tsch and Da rnbecker Stanlot39d University Press tlt7 39llN ll39l MllltlEAN tlIlL I ll 03 BIOLOGY OF FISHES FISH 311 BIODIVERSITY METHODS AND GOALS OF SYSTEMATICS PHENETICS EVOLUTIONARY SYSTEMATICS AND CLADISTICS General topics 1 De nitions 2 Phenetics 3 Cladistics 4 Evolutionary Systematics 5 The problems with phenetics 6 Cladistics versus Evolutionary Systematics 7 The concept of relationship DEFINITIONS Taxonomy Systematics Classi cation Classi cations Branching diagrams The discovery recognition de nition and naming of groups of organisms The study of biological diversity or more speci cally the ordering of the diversity of nature through construction of a classification that can serve as a General Reference System The ordering of plants and animals into groups based on their similarity and relationship Concise lists of organisms grouped or ranked according to the pattern of branching seen in the branching diagram a product of systematic research Graphic views of the sequence of evolutionary divergence of groups of organisms through time another product of systematic research Along the horizontal axis they show the relative primitiveness of organisms along the vertical axis they show how groups of organisms have evolved from one another that is the pattern of branching through time The task of systematics is to nd the best possible General Reference System But nding the best possible reference system is not so easy and it turns out that there are several approaches or ways to go about performing this task During the 19505 and much more so during the 605 and early 705 there was much confusion and debate over the principles of systematics Re ecting this basic uncertainty about the methods and goals of systematics is the fact that during a fteenyear period from 1960 to 1975 over a dozen books were published in which the methods and goals of systematics were argued back and forth From all this intellectual fervor came three competing theories of classi cation each claiming to be more objective than the other two and each claiming to produce a better general reference system than the other two What are these three competing theories 1 Phenetic Systematics or Numerical Taxonomy 2 Cladistic Systematics or Phylogenetic Systematics 3 Evolutionary Systematics or the socalled Synthetic Method 2 PHENETIC SYSTEMATICS In this approach groups of organisms are brought together on the basis of overall similarity Similarity is calculated from the presence or absence of numerous unweighted characters This method does not establish groups by simple inspection but orders the lowest taxonomic units usually species into groups using standardized procedures The major criteria are 1 Overall similarity 2 Numerous characters are used as many as can be found and all are given 3 Equal weight the resulting branching diagram is 4 Computer generated and the branching diagram that is produced is called a 5 Phenogram a branching diagram that links organisms by estimates of overall similarity as evidenced by an analysis of characters INTERMEDIUS ALAUDAE AMERICANUS i CHELIDONIS TRANSVAALENSIS rmscurnus GALLINAE GALLINAE PROGNEPHILUS I HIRUNDINIS l masurus l L GROCHOVSKAE oumrus LLllllllllllllllllllllllllllilllllllllllllLllllill 40000 osooo ozooor o2ooo osooo lOOOO An example of a phenogram a branching diagram showing the hierarchical pattern of general overall similarity exhibited among some taxa of birds after Schnell 197036 TAXONOMIC RANK 2 4 6 TAXONOMIC RANK wm mmhwmd PETERS CATHARACTA SKUA STERCORARIUS PO ARINUS STERCORARIUS PARASITICUS STERCORARIUS LONCICAUDUS GABIANUS FACIFICUS GABIANUS SCORESBII PACOPHILA EBURNEA LARUS FULIGINOSUS LARUS MODESTUS LARUS HEERMANNI LARUS LEUCOPHTHALHUS LARUS HEMPRICHII LARUS BELCHERI LARUS CRASSIROSTRIS LARUS AUOOUINII LARUS DELAHARENSIS NUS LARUS ARCENTATUS LARUS THAYERI LARUS FUSCUS LARUS CALIFORNICUS LARUS OCCIDENTALIS LARUS DOMINICANUS LARUS SCHISTISACUS LARUS HARINJS LARUS CLAUCESCENS LARUS HYPERBOREUS LARUS LEUCOPTERUS LARUS ICHTHYAETUS LARUS ATRICILLA LARUS BRLMICEPHALUS LARUS CIRROCEPHALUS LARUS HELANOCEPHALUS LARUS BULLERI LARUS HACULIPEMIS LMUS RIDIBUNDUS LARUS GENEI LARUS PHILADELPHIA WUS HINJ URUS SAU DERSI RHODOSTETHIA ROSEA RISSA TRIOACTYLA RISSA BREVIROSTRIS CREACRUS FLRCATUS XEMA SABINI ClLIDONIAS HYBRIDA GLIDONIAS LEUCOPTERA CHLIDONIAS NIGRA PHAETUSA SIM LEX CELOGELIDON NILOTICA HYDROPROGNE TSCHEORAVA STERNA ALRANTIA STERNA HIRLDDINACEA STERNA HIRUPDO STERNA PARADISAEA STERNA VITTATA STERNA VIRCATA STERNA FORSTERI STERNA TRLDEAUI STERNA DOUGALLII ST ERNA STRIATA STERNA REPRESSA STERNA SWATRANA STERNA HELANOCASTER STERNA ALEUTICA STERNA LLNATA STERNA ANAETlETUS STERNA FUSCATA STERNA NEREIS STERNA ALBISTRIATA STERNA SUPERCILIARIS STERNA BALAENARUH STERNA LORATA STERNA ALBIFRONS THALASSEUS BERGII THALASSEUS HAXIMJS THALASSEUS BENGALENSIS THALASSEUS ZIP P ERMANNI WALASSEUS ELRYCNATHA THALASSEUS ELECANS THALASSEUS SAPOVICENSIS LAROSTERNA NCA PROCELSTERNA CERLLEA ANGUS STOLIDUS ANGUS TENJIROSTRIS ANGUS HINUTUS CYCIS ALBA RYNCHOPS NICRA RYNCHOPS FLAVIROSTRIS RYNCHOPS ALBCOLLIS H The phenetic method was all the rage in the early and midsixties popularized primarily by two individuals Robert R Sokal and Peter H A Sneath Sokal R R and P H A Sneath 1963 The Principles of Numerical Taxonomy W H Freeman and Co San Francisco 359 pp Sneath P H A and R R Sokal 1973 Numerical Taxonomy W H Freeman and Co San Francisco The 29 species of Caminalcules a group of imaginary animals created by Joseph H Camin of the University of Kansas according to rules known only to him used to study phenetics and other approaches to phylogenetic analysis Phenetic systematics was once thought to be the answer to the dilemma of how best to establish relationship among organisms but its acceptance was short lived and very few recognize this method today 3 CLADISTIC SYSTEMATICS Organisms are classi ed and ranked exclusively on the basis of recency of common descent Members of taxa are recognized by the joint possession of derived character states ie apomorphic character states Grouping and ranking are given simultaneously by the points in a branching diagram Sometimes called Phylogenetic Systematics the major criteria are 1 One criterion for classi cation recency of common descent 2 The method allows only the use of specialized or derived character states character states that we call apomorphic primitive characters states are called plesiomorphic So in this sense some characters or more precisely some character states are heavily weighted over others 3 Taxa that share derived or apomorphic characters states are said to be related Shared apomorphic character states are called synapomorphic whereas shared plesiomorphic character states are called symplesiomorphic 4 Grouping and ranking are given simultaneously by branching points in a diagram called a cladogram from the Greek claa or klados meaning to branch 93 f5 gt39RL 39 V g L N39 W 44 39 TJquot ie 23 m lophiidae Anlennariidae tetrahrachiidae lophichthyidae Brnchionichthyidu Chaunacidae Ogcoceuhalidae quotCeralioid Familiesquot A cladogram showing the evolutionary relationships of anglerfishes Let s stop a moment and talk about this concept of primitive versus derived character states This can best be illustrated by examples picking an example from vertebrate animals let s take a simple one like skeleton Skeleton is the character but thinking about it you realize that skeleton among vertebrates consists of at least two states a bony skeleton and a cartilaginous skeleton We know that a skeleton of true bone evolved very early in vertebrate history and that those vertebrates with a skeleton of cartilage are the result of a loss of the ability to ossify the skeleton A bony skeleton is thus the primitive or plesiomorphic character state while a cartilaginous skeleton is clearly the derived or apomorphic character state Let s pick another slightly more complicated example forelimbs Thinking about forelimbs among vertebrates we can list at least three character states pectoral ns arms and wings We know that pectoral ns evolved early on in vertebrate history and that these structures are the evolutionary forerunners of arms and wings Thus pectoral ns represent the primitive character state of a character called forelimbs What about arms and Wings We know that arms evolved in the earliest fourlegged vertebrates the earliest tetrapods ie the rst amphibians long before Wings rst appeared in birds or mammals bats so we conclude that arms are a derived character state relative to pectoral ns but a primitive state relative to wings Wings clearly represent the derived character state relative to both pectoral ns and arms CAT MOUSE LIZARD 3 ear ossicles hair mammary glands PERCH amniote egg 39 LAMPREY laws 3 semicircular canals paired appendages vertebral column semicircular canals chambered heart visceral arches dorsal nerve cord notochord appendages A cladogram showing the evolutionary relationships of ve kinds of vertebrates Each level in the hierarchy denoted by branch points is de ned by one or more similarities interpreted as derived character states Cladistics was rst articulated in a formal way by a German entomologist named Willi Hennig a world39s authority on the systematics of ies order Diptera He wrote a book rst published in German and later translated into English Hennig H 1950 Grundziige einer T heorie der phylogenetischen Systematik Deutscher Zentralverlag Berlin Hennig H 1966 Phylogenetic Systematics University of Illinois Press Urbana The method immediately became popular among entomologists and quickly spread to systematists working on other groups particularly ichthyologists The primary proponents of cladistics in the sh world were Donn E Rosen and Gareth Nelson both formerly working in the Department of Ichthyology at the American Museum of Natural History in New York They and a host of followers beginning in about 1971 began publishing theoretical as well as applied papers in a number of prestigious scienti c journals most important among them being Systematic Zoology recently renamed Systematic Biology 4 EVOLUTIONARY SYSTEMATICS Organisms are classi ed and ranked on the basis of two sets of factors 1 phylogenetic branching ie recency of common descent and 2 the amount and nature of evolutionary change between branching points This later factor depends on the evolutionary history of the lineage in question for example whether or not it has entered a new adaptive zone and to what extent it has undergone a major radiation This method attempts to maximize simultaneously the information content of both types of variables 1 and 2 above thus it combines components of phenetics and cladistics Sometimes called the Synthetic Method this approach relies on 1 Two criteria for classifying and ranking organisms recency of common descent and the amount and nature of evolutionary change between branching points 2 The method allows the use of plesiomorphic primitive character states as well as apomorphic specialized or derived character states Characters states thought to be more evolutionarily or inctionally signi cant are often heavily weighted over others 3 Grouping and ranking are given simultaneously by branching points in a diagram called a Phylogenetic Tree time L X 7 degree of similarity A hypothetical evolutionary tree showing the relationships of terminal taxa A through F In contrast to a phenogram and a cladogram which give only two kinds of information geological time on the vertical and a measure of similarity on the horizontal this diagram provides three kinds of information geological times on the vertical degree of similarity on the horizontal and degree of divergence by the angle of divergence The major proponents or defenders of this approach were George Gaylord Simpson and Ernst Mayr each of whom wrote classic texts on this subject Simpson G G 1961 Principles of Animals Taxonomy Columbia University Press New York Mayr E 1969 Principles of Systematic Zoology McGrawHill New York 5 THE PROBLEMS WITH PHENETICS Today very few if any systematists employ phenetics or numerical taxonomy When rst proposed the methodology seemed to resolve the problem of the lack of objectivity in evaluating characters for purposes of determining evolutionary characters But early on detractors pointed out serious de ciencies According to Ernst Mayr Evolution and the Diversity of Life 1976 p 429 the phenetic approach has been largely a failure when applied to higher organisms One of the criticisms is that it totally ignores evolutionary convergence 6 CLADISTICS VERSUS EVOLUTIONARY SYSTEMATICS The primary controversy is between those who support Cladistics and those who back Evolutionary Systematics The proponents on both sides declare that their method provides the greatest number of conclusions and predictions about the organisms being classi ed and is therefore the best approach To better understand the differences between these two methods let39s forget about shes for a moment and take a look at the famous birdcrocodile controversy This branching diagram shows how the major groups of tetrapods diverged from one another through evolutionary time Everyone agrees cladists as well as evolutionary systematists that this is the way tetrapods evolved what remains in question is how a classi cation should be derived from this sequence of branching Amphibia other Reptilia CFOCOdilia Aves Mammalia Cladists lump birds and crocodiles the latter usually thought of as a subgroup of reptiles together in a small taxonomic category called Archosauria which is given equal rank with a group that includes all other reptiles Ranking and classifying are based solely on a single criterion recency of common descent The classi cation that cladists construct from their branching diagram looks like this A CLADISTIC CLASSIFICATION OF TETRAPODS Infraclass AMPHIBIA Infraclass REPTILOMORPHA Division SAUROPSIDA Cohort REPTILIA Cohort ARCHOSAURIA Subcohort CROCODILIA Subcohort AVES Division MAMMALIA Notice a couple of things rst off the classi cation is a perfect re ection of the pattern of branching in the branching diagram Everything is laid out in pairs There are two infraclasses two divisions two cohorts etc Just as the diagram is perfectly dichotomous so is the classi cation Thus the classi cation can be constructed easily by simply following the sequence of branching in the branching diagram At the same time given the classi cation it s very easy to draw the branching diagram The concept of sistergroups notice also how crocodiles and birds are given equal rank Cladists would say that these two taxa are sistergroups that is the subcohort Crocodilia crocodiles is the sister group of the subcohort Aves birds and vice versa Aves is the sister group of the Crocodilia We would also say that the division Sauropsida containing the reptiles crocodiles and birds constitutes the sistergroup of the division Mammalia Ok so this then is how cladists View the evolutionary history of tetrapods Let s now take a look at the other side of the controversy Noncladists see this and go crazy They argue that this cladistic approach completely ignores the drastically different evolutionary fates of the groups in question That is cladists ignore genetic change that may have occurred within a group subsequent to branching away from an ancestral group To stick with the example we started with above noncladists argue that birds have invaded an entirely New Adaptive Zone that is they ve evolved wings and they y yet in the cladistic View they are given equal rank as the sistergroup of the crocodiles a group that has remained in the old Ancestral Adaptive Zone Of course the problem immediately arises how do you measure the extent to which a group of organisms has entered a new adaptive zone How new is new How does one quantify the differences In any case noncladists in constructing their classi cation of tetrapods from the same pattern of evolutionary branching accepted by cladists give birds a much higher status than crocodiles In fact they give birds equal rank with reptiles thus emphasizing the amount of evolutionary change between branching points Here is their branching diagram Amphibia other Reptilia CrOCOdilia Aves Mammalia You ll notice that the pattern of branching is identical to that in the diagram of the cladist but the angles formed between the branches vary in accordance with estimates of the amount of evolutionary change morphological divergence between branching points Here is their classi cation four classes of equal rank AN EVOLUTIONARY CLASSIFICATION OF TETRAPODS Class AMPHIBIA Class REPTILIA Subclass ARCHOSAURIA Subclass CROCODILIA Class AVES Class MAMMALIA Notice a couple of things rst off the classi cation is not at all a re ection of the pattern of branching in the branching diagram Thus the classi cation cannot be constructed by following the sequence of branching in the branching diagram And Vice versa it is impossible to draw the branching diagram based on the classi cation alone Notice also that in lumping crocodiles with other reptiles noncladists violate a major premise of the cladistic approach they Violate the concept of recency of common descent Cladists therefore View Reptilia of the noncladist as an unnatural assemblage Followers of Evolutionary Systematics say that their evolutionary tree and classi cation provide much more information than a cladogram and a cladistic classi cation Their approach provides important information about the 1 extent of radiation and the 2 amount of evolutionary divergence between groups Cladists come right back and say this is all well and good but how does one go about measuring ie quantifying the extent of radiation and the amount of evolutionary change They argue that these values are unknowable they can t be determined and thus any attempt to use these concepts to order the diversity of life is not science 7 THE CONCEPT OF RELATIONSHIP To compare these competing methodologies and provide another example that will help to differentiate between pheneticists cladists and evolutionary systematists let s take a look at the word relationship Phenetic approach for the pheneticist relationship simply means similarity Pheneticists operate on the assumption that the total phenotype accurately re ects the genotype They believe that an unweighted measure of overall similarity provides an accurate determination of relationship In so doing pheneticists ignore the possibility of evolutionary convergence Cladistic approach cladists de ne relationship in a strictly genealogical sense the measure of phylogenetic relationship is the relative recency of common descent Evolutionary or Synthetic approach for the evolutionary systematist relationship means more than just kinship in a strictly genealogical sense it also involves a measure of genetic change that may occur within a group subsequent to its divergence branching from an ancestral group 13 Let s illustrate this with a diagram 1 5 00 1 0 70 o A extinct Imagine an ancestral species A that gives rise to three modern day species B C and D Imagine irther that 15 of the genetic content of species B differs from that of species A 10 of the genetic content of species C differs from that of species A and 70 of the genetic content of species D differs from that of species A There is a maximum genetic difference of 25 between the genomes of B and C but 80 between C and D The cladist would say that C is more closely related to D than to B because of greater recency of common descent The evolutionist and pheneticist would say C is much more closely related to B than to D because there is much less genetic difference or genetic change between them that is they have a much greater inferred amount of shared genotype BIOLOGY OF FISHES FISH 311 FUNCTION RESPIRATION BUCCAL AND OPERCULAR PUMPS STRUCTURE AND FUNCTION OF GILLS AIRBREATHING FISHES General topics 1 2 3 Respiration the capture of Oz and elimination of C02 The buccal and opercular pumps The structure and function gills Respiration and blood circulation Airbreathing shes 1 RESPIRATION THE CAPTURE OF 02 AND ELIMINATION OF C02 As you know oxygen is more readily available to terrestrial vertebrates than it is to shes Air contains much more oxygen that can dissolve in an equivalent volume of water 1 liter of air contains 210 cc of oxygen whereas 1 liter of water contains only 10 cc of oxygen Fishes obtain oxygen by creating a continuous ow of water a medium that is 800 times as dense as air over the gills The more continuous and the more steady the ow the more thoroughly will the gills be able to remove the oxygen that is dissolved in the water The average human can utilize only about 25 of the oxygen in a given volume of air between inhalation and exhalation but in most shes the ef ciency of oxygen removal is much greater Fishes such as tunas family Scombridae for example can extract up to 80 of the oxygen dissolved in water passing over the gills How is this done How is this constant flow of water created and maintained 2 THE BUCCAL AND OPERCULAR PUMPS In contrast to terrestrial vertebrates in which oxygen ow across the lungs is bidirectional in ow and out ow associated with dead air space oxygen ow in shes is unidirectional Water is almost always sucked in through the mouth and exits by way of the Opercular openings on each side of the head This unidirectional ow pattern negates the waste associated with dead air space and makes possible the opportunity to maintain a constant gradient for oxygen to diffuse from the water into the blood by way of the gills Within the pattern however can be seen a de nite cycle of breathing that may be divided into a number of phases two major phases and two minor phases Phase 1 the Opercular Suction Pump Phase 2 when the pressure is reduced Phase 3 the Buccal Pressure Pump Phase 4 when the pressure is reversed Diagrammatically we can express the pressure relationships as follows Gills gt Gill resistance 39 m Buccal Opercular cavity gt cavity Opercular valve water going out only when open Oral valve prevents m backflow of water quot gt39 Water entering Phase 1 The Opercular Suction Pump both the Buccal and Opercular cavities expand creating negative pressure in both cavities But as these volume expansions take place there is strong differential pressure the opercular cavity being considerably more negative than the buccal cavity Water is sucked in through the mouth the buccal or oral valve The opercular opening opercular valve is held tightly closed Gills gtm Gill resistance m Buccal Opercular cavity gt cavity Oral valve prevents m Opercular Valve backflow of water m e water gomg out only when open Buccal Phase 2 The mouth closes and the buccal cavity contracts creating positive pressure in the buccal cavity and causing a reduced pressure differential between the two cavities This phase is of very short duration Gills gt Gill resistance m Buccal u Opercular cavity gt cavity n Oral valve prevents m gt back ow of water H Opercular valve water oin out Buccal u g g m m Opercular Pump Phase 3 The Buccal Pressure Pump the buccal cavity is further compressed while the Opercular cavity is being compressed as well causing water to be pushed out through the opecular opening Pressure is positive in both cavities but the pressure differential between the two cavities is maximized Gills Gill resistance m Buccal Opercular cavity gt cavi ty Oral valve preVents n gt water backflow of water Opercular valve entering water going out Buccal Gills Opercular pump Phase 4 The buccal cavity expands while the Opercular cavity is still being compressed There is a slight reversed differential pressure between the two cavities but this lasts for only a very short time Mouth or oral valve Mouth or oral valve open closed Buccal chamber contracting pressure positive expanding V pressure negative ope o la Opercular r u valve valve closed open Suction pump phase Pressure pump phase The timing of the expansion and contraction of the buccal and opercular cavities ensures that the pressure in the buccal chamber exceeds that of the opercular chamber throughout nearly all of the respiratory cycle This creates a nearly steady ow of water from the buccal chamber to the opercular chamber passing over the gill lamellae which have blood owing through them in the opposite direction The application of modern sensitive and stable pressure transducers has resulted in accurate pressure measurements in both the buccal and opercular cavities The recordings show that the gills have an appreciable resistance to water ow so that a differential pressure is always present usually with the gradient from buccal to opercular cavity In other words pressure in the buccal cavity is nearly always positive with respect to pressure in the opercular cavity With sensitive pressure transducers we can also record the time course of the differential pressure between the two cavities In a typical perchlike sh for example a wrasse of the genus Crenz39labrus family Labridae the two pumps are balanced That is Phase 1 and Phase 3 have moreorless equal time duration Phase 1 Phase 2 Phase 3 Phase 4 Differential Pressure V Time 23gt But the time duration varies tremendously among shes depending on the speed with which they move through the water or on oxygen availability in the particular environment to which they are adapted In more slowly swimming species like various cods family Gadidae the opercular pump predominates In faster swimming forms like jacks family Carangidae the buccal pump predominates In other pelagic forms the pumps may not be used at all For example in shes like mackerels and tunas family Scombridae which swim continuously at a good rate of speed moving long with the mouth open and allowing the water to ow in and through the buccal and opercular cavities is enough to supply adequate oxygen to the gills The stream of water can be regulated simply by the degree of mouth opening In many bottom living shes there is a tendency to increase the duration of the inspiratory phase that is the opercular pump phase Thus phase 1 is of long duration while phase 3 is relatively short phase 1 Phase 2 Phase 3 Phase 4 Differential Pressure V Time gt In truly benthic forms especially those highly modi ed for existence on the bottom like at shes an accessory pump has evolved the Branchiostegal Pump In these forms the branchiostegal apparatus plays an important role in respiration forming an accessory pump that works along with the opercular pump The buccal pump plays a relatively minor role The inspiratory phase the time taken to draw water in through the mouth is increased Combining the accessory pumping action of the branchiostegal rays with the opercular suction pump completely eliminates the reversal of differential pressure usually characteristic of phase 4 phase 1 Phase 2 Phase 3 Phase 4 Differential Pressure V Time gt This is a great advantage for a sh with limited time spent progressing forward and with limited opportunity to meet new oxygenated water Many benthic habitats where currents may be relatively slow moving are oxygen limited to begin with anything that would increase the ef ciency of extraction of oxygen would provide a distinct advantage 3 STRUCTURE AND FUNCTION OF GILLS The gills form a sievelike structure in the path of the respiratory ow They produce resistance to water ow which in turn creates a differential pressure between the buccal and opercular cavities Gill arch Holobranch Tip of one gill filament Several abducted gill laments on two adjacent gill arches Note that each gill lament or holobranch is paired consisting of two hemibranchs Note Also that the tips of adjacent holobranchs come into contact with each other at the distal tips Each gill arch bears a number of gill filaments or holobranchs each of which is made up of two halves called hemibranchs Each hemibranch bears many ne subdivisions called gill lamellae It is the gill lamellae that form the major part of the sieve through which water passes They are primarily responsible for creating the resistance to water ow and which represent the major respiratory portion of the gills The total surface area of the gill lamellae averages about 5 cm2 per gram of body weight Efferent branchial Afferent branchial Capillary bed in lamella connecting lamental arteries Gill arch filament Efferent Lamella showing tilamental direction of blood artery ow through capillary bed Numerous gill lamellae along the length of a single enlarged hemibranch The small arrows show the direction of blood movement the large arrows show the direction of water movement In all bony shes there are muscles that move the bases of the hemibranchs that is each holobranch can open and close In this way the tips of the hemibranchs of adjacent gill arches can come into contact with one another to create maximum resistance to water ow or they can be separated to protect the gills against excess water ow qulobranch Hemibranchs Afferent Abductor branchial muscles artery Bony gm Efferent amh branchial artery at Abducted b Adducted Diagrammatic cross sections through adjacent holobranchs of a bony sh showing supporting and muscular elements that enable a abduction and b adduction These muscles thus perform a regulatory function whereby resistance of ow by the gills can be actively varied and regulated 4 BLOOD CIRCULATION AND RESPIRATION How does blood ow through the gills Arterial didquot 0f M iaierai Right lateral pseudobranchial Willis dorsal aurta dorsal aorta artery v A Hym ieaquot Etferent Dorsal aorta A afferent branchial me arteries Gaeliac artery Ophthalmi 1 w Mesenteric artery my quot Gasbladder artery Efferent Subclavian artery pseudobrarichral 4th gill arch artery with its holobranch Orbital k Gill laments artery Left andright ducts of Cuvier Hyordean Atrium pseudobranch aquot sinus venosus Mandilaular a egiha39 I Ventricla ar Sewgdary H b h l Coronary hyoi ean Afferent ypo ranc ia a cry afferent mammal 2 me Ventral Bonus artery aorta arteriosus Deoxygenated blood reaches the gills by way of afferent branchial arteries The blood passes through the gill lamellae Where it is oxygenated It then passes to efferent branchial arteries and on to the body Capillaries in the gill lamellae are extremely close to the water interface and are undoubtedly more involved in gas exchange than those in the gill filaments A vitally signi cant feature is that blood ows across the lamellae in the opposite direction to the water ow This is the counter current principle that reoccurs so often in vertebrate anatomy Secondary lamella Primary lamella 47 Afferent blood vessel 17quot g Direction of blood flow Efferent blood vessel Direction of water flow Here blood with the higher oxygen content meets water with the highest oxygen content so that oxygen diffuses into the blood along the entire length of the lamellae The effect of course is extremely ef cient interchange of oxygen and carbon dioxide between water and blood Threedimensional cutaway View through a holobranch of a bony fish showing a gill raker gr adductor ad and abductor ab muscles and afferent af and efferent ef branchial arteries AIR BREATHING FISHES In all tropical regions of the world deoxygenation is frequent in shallow and stagnant waters Whenever water is slow moving covered with vegetation and heavily shaded so that photosynthesis is slight and where cooling at night is not suf cient to produce overturn deoxygenation is bound to occur The only oxygen in these waters gets there by diffusion from the air Usually freshwater habitats are the only ones effected but also estuarine habitats are susceptible especially mangrove swamps Deep lakes like those of the East African Rift Valleys can also be affected In marine habitats entire deep basins may be deoxygenated for example the Cariaco Trench off the coast of Venezuela Many bony fishes inhabiting such waters have evolved special air breathing structures to cope with these unusual conditions Others have evolved ways to live out of the water for extended periods of time List of Airbreathing Fishes Arranged Phylogenetically Preteleostei Amia airbladder functions as a lung Lepisosteus airbladder functions as a lung Teleostei Osteoglossomorpha Arapaima airbladder Heterotis airbladder Clupisudz39s airbladder Notopterus airbladder Elopomorpha Megalops airbladder Anguilla skin and pharynx Euteleostei Ostariophysi Cyprinoids Misgurnus intestine Cobitz s intestine Characoids Erythrinus airbladder Hypopomus gill chamber Electrophorus pharynx Siluroids Clarias pharynx Dinopterus pharynx Doras intestine Callichthys intestine Plecostomus stomach Ancistrus stomach Heteropneustes outgrowths of the branchial chamber Saccobranchus outgrowths of the branchial chamber Acanthopterygii Anabantoidei specialized structures in the branchial chamber Ophicephalidae pharynx Periopthalmus phamyx Synbranchiformes esophagus and skin The accessory airbreathing structures of bony shes are all modi cations of the epithelia of the alimentary canal or gill chamber or diverticula emerging from these parts This includes a host of structures the mouth pharynx gill chamber esophagus airbladder stomach and intestine Here is an example Modified gill Arborescent organs filaments Anterior Posterior Base of Anterior naris Barbels Extension of gill cavity Respiratory membrane Respgfagg Respiratory membrane Arborescem 39 organ Respiratory fan a i Gills Gills Gills Respiratory fan First gill arch Second gill arch Third gill arch Fourth gill arch Lateral views of the gill arches of the walking cat sh Clarias batrachus showing the respiratory fans respiratory membranes of the suprabranchial chamber and treelike extensions that permit the sh to extract oxygen from air when it is out of water All have in common a specialized epithelium that is often equipped with branched treelike outgrowths to increase the surface area Lying underneath this thin epithelial layer is always a rich network of blood capillaries Gills are never used for air breathing because they are poorly adapted for it The gill lamellae are not stiff enough to support themselves and collapse when out of water The surface area is lost and the sh suffocates All air breathing organs function just as absorbers of oxygen they never have anything to do with carbon dioxide The gills andor the skin take care of the excretion of carbon dioxide 12 Here are more examples Epibra nchial apophysis Anterior chamber Hyomandibular Posterior chamber Gill with pharynx filaments Snakehead genus Ophicephalus Afferent artery to Gas bladder in 39 left air sac bony capsule Barbels 39 1 aquot Ventral aorta right air sac Airsac catfish genus Heteropneustes Suprabranchial cavity Labyrinthlform organ Cut edge of 8 V Lateral First gill arch Climbing perch genus Anabas 13 Adaptive strategies a trend toward the separation of the organs dealing with oxygen uptake and carbon dioxide discharge Most airbreathers have evolved a new organ by modifying some existing structure This new organ deals with oxygen uptake from the air elimination of carbon dioxide is done by way of the gills A few airbreathers have evolved a new respiratory organ by modifying an existing structure for oxygen uptake but at the same time the gills have become greatly reduced Scales are reduced as well and the skin is used for the discharge of carbon dioxide Synbranchiforms and the goby genus Periophthalmus fall into this latter category What is the biological signi cance of air breathing 1 Survival in oxygen poor habitats 2 Utilization of terrestrial food resources 3 Abandon drying ponds to search for better habitat 4 Invade new territories and thus enhance distribution 14 BIOLOGY OF FISHES FISH 311 FORM AND FUNCTION FEEDING MODES AND MECHANISMS PART I BIOMECHANICAL CONSIDERATIONS UPPER JAW MOBILITY AND THE EVOLUTIONARY SUCCESS OF TELEOSTS General topics 1 2 3 8 9 Feeding mechanisms the key to teleost success Feeding in jawless shes The jaws of primitive jawed shes The dermal jaws of actinopterygians and sarcopterygians Evolution of the upper jaw of actinopterygian shes Functional replacement of the teleost maxilla Functional considerations what does it all mean Biomechanics of feeding in a primitive teleost The rise of protrusible jaws 10 The unparalleled success of perciform shes 1 FEEDING MECHANISMS THE KEY TO TELEOST SUCCESS Derived bony shes particularly teleosts have been marvelously successful in their ability to speciate and to occupy diverse aquatic habitats Why has this been so To nd the answer many have turned to evolutionary changes in the feeding mechanism It seems that a number of major morphological innovations structural novelties in feeding mechanisms can be correlated with explosive radiations of shes particularly Within What is now the largest and most diverse group of teleosts the Perciformes ACTINOPTERYGIAN EVOLUTION 130 MYBP 225 MYBP 375 MYBP 390 MYBP 2 FEEDING IN JAWLESS FISHES The eating or headend of a sh is concerned with at least four primary functions that can be divided into two major categories 1 Feeding and respiration 2 Sensory perception and coordination In protovertebrates feeding and respiration were closely linked in fact they were so closely linked that they were really one and the same These protovertebrates as well as the earliest kinds of vertebrates ancient jawless shes were bottom living lterfeeding organisms As long as they maintained a moreorless continuous ow of water into their mouth eating in itself provided a suf ciently continuous ow of oxygenated water over the gills for purposes of respiration But as jaws and paired ns evolved and shes became more mobile larger prey items became a source of food and eating became a more intermittent activity Breathing on the other hand cannot be intermittentmetabolism requires constant oxygen uptake So very early on in sh evolution there occurred a separation of these two functions In fact as far as feeding is concerned the entire subsequent evolutionary history of shes may be viewed in terms of increasing specialization and separation of these two functions The ancient pteraspidomorphs those earliest of vertebrates that were upon the scene by about 490 million years before present MYBP and which became well differentiated by about 430 MYBP were jawless forms that spent all their time on soft bottoms sucking in the ooze and ltering out edible bits and pieces They did very well in their time producing 10039s of species but they began to dwindle away by late Devonian about 350 MYBP most likely because of replacement by a new kind of vertebrate one that was better able to exploit available food resources ie better able to compete with its jawless ancestors primarily because it had jaws This begins a new era in vertebrate history the invention of jaws opened up whole new possibilities never before realized The heavy dermal armor of former types began to disappear as shes became more mobile New capabilities of catching and consuming prey became available to vertebrates for the rst time The old dependency on lterfeeding was lost Jaws along with the appearance of teeth which seem to have evolved simultaneously with jaws allowed a new kind of predatory life style that involved speed An elongate streamlined shape developed and along with it came the evolution of paired ns to allow for greater stabilization and enhanced maneuverability So two very important structural innovations l Jaws and teeth 2 Paired fins 3 THE JAWS OF PRIMITIVE JAWED FISHES The earliest kinds of jawed shes are all extinct belonging to a group called the Placodermi We have no living remnants of these animals to look at but we do have an incredibly diverse fossil record We know that the jaws of these earliest jawed shes were made of endochondral bone or replacement bone that is they were constructed of bone that was rst laid down as cartilage To see the morphology of these elements in living shes we can look at chondrichthyan shes ie sharks and their allies which inherited endochondral jaws from the earliest jawed shes CRANIAL SKELETON OF A SHARK Hyomandibular articulation Hyoid gill rays WWW 39 Orbital process of palatoquadrate Mandibular cartilage Labial cartilage Basihyol Ceratohyal In Chondrichthyes the upper jaw is called the palatoquadrate cartilage the lower jaw is called the mandibular cartilage or sometimes Meckel39s cartilage OK so we39ve got a whole host of jawed shes shes with toothbearing bones on the outer rim of their mouth bones that are endochondral in origin Now if we continue to trace the evolution of jaws from these ancient forms to bony shes Actinopterygii as well as to other more highly evolved vertebrates Sarcopterygii we see some signi cant changes It turns out that the jaws of these more derived vertebrates are made up of entirely different elements elements that are not preformed in cartilage but are instead dermal in origin The old endochondral elements that once formed the jaws become internalized and take on other functions that are less directly related to feeding the palatoquadrate cartilage evolves to form elements that make up part of the suspensorium that functional unit of the cranium that supports or suspends the jaws part of it becomes the palatine bone and part forms the quadrate But in primitive tetrapods it comes to form part of the roof of the mouth ie the palate and eventually in mammals part of it forms the incus one of the three bony ossicles of the middle ear The mandibular cartilage also takes on suspensory functions in derived shes that is it comes to form an element called the articular that connects to the quadrate bone of the suspensorium to suspend the lower jaw In mammals part of it becomes the malleus another of the three bony ossicles of the middle ear 4 THE DERMAL JAWS OF ACTINOPTERYGIANS AND SARCOPTERYGIANS So these endochondral bones are lost as jaws but they are replaced with dermal elements thick overlying bony plates homologous to the primary dermal armor of extinct pteraspidomorphs come to lie in a position surrounding the mouth The upper jaw consists of two dermal elements premaxilla and maxilla The lower jaw is called the dentary SKULL OF A PRIMITIVE ACTINOPTERYGIAN FISH middle pitl ine mm a 39 postenor 39 dc lel lane piHine 39 x premaxilla 5 EVOLUTION OF THE UPPER JAW IN ACTINOPTERYGIAN FISHES Within actinopterygians the most signi cant changes in jaw morphology begin with the freeing of the posterior end of the maxillary bone from the bones of the cheek In the most primitive actinopterygians the maxilla was a large bone expanded posteriorly and sutured to the elements of the cheek largely attached to the preopercle It was immobile relative to the cranium In the most primitive actinopterygians the maxilla was a large bone expanded posteriorly and sutured to the elements of the cheek largely attached to the preopercle It was immobile relative to the cranium In more derived actinopterygians the posterior end of the maxilla has lost attachment to the cheek and is now mobile relative to the cranium Now when the mouth is opened the maxillae one on each side rotate forward and downward to close off the corners of the mouth providing a convenient way to help prevent the escape of prey SKULL OF A DERIVED PRETELEOSTEAN ACTINOPTERYGIAN preopercular 0 subopercular suborbitals interopercular But when we turn now to teleosts we nd additional changes that further increase upper jaw mobility In addition to the posterior end of the maxilla being freed from the cheek we nd for the rst time a ball and socket joint developed between the head of the maxilla and the palatine bone This new highly mobile joint is thought to be a real improvement over the simple connective tissue hinge found here in more primitive actinopterygians SKULLS OF ACTINOPTERYGIANS A Sturgeon ancestor B Amia C Elops 6 FUNCTIONAL REPLACEMENT OF THE MAXILLA IN TELEOSTS Further additional changes appear as teleosts themselves evolve in primitive teleosts the premaxilla is small and anterior in position both the premaxilla and maxilla bear teeth but the major tooth bearing bone is the maxilla As teleosts evolve the premaxilla begins to elongate and overlap the maxilla it begins progressively to take on more of the toothbearing function of the upper jaw Eventually the premaxilla fully excludes the maxilla from the gape of the mouth and becomes the only toothbearing element of the upper jaw In the most highly evolved teleosts the anterior end of the premaxilla develops what39s called an quotascending processquot that extends upward and backward to overlap the snout region of the head This ascending process functions as part of a highly mobile upper jaw that allows the jaw to be protruded away from the snout the maxilla behind which has lost its old tooth bearing function now functions as a level to help thrust the premaxillae forward While all this is happening the original bony connection of the premaxillae with the snout in preteleosts was replaced with a much more exible cartilaginous and connective tissue hinge all providing for a highly mobile upper jaw 39 i 2 Representation of types of associations be tween the two upper jaw bones of teleostean shes diagrammatic In the primitive condition j pre maxilla to the left maxilla to the right in series in the most derived condition js the two bones are in tandem 5 7 FUNCTIONAL CONSIDERATIONS WHAT DOES IT ALL MEAN Obviously this loosening of the premaxillae from the cranium can only weaken the bite It sounds like a distinct disadvantage who wants weak easily damaged jaws How do teleosts compensate for this apparent disadvantage To understand this problem a bit better it helps to take a closer look at how shes feed In a very general sense we can group sh feeding into three principle categories 1 Hit and run 2 Filter feeding 3 Gape and suck The rst of these hit and run is a strategy used by mostly fastswimming open water forms that simply run down engulf and swallow more slowly swimming prey or bite off a chunk on the way by For shes that obtain food in this way the biting or grasping apparatus formed by the rims of the jaws is of primary importance they require a rm jaw construction and placement as well as large powerful muscles to get the jaws shut rmly and quickly at the proper time Their requirements seem to be the same as those for most terrestrial vertebrates whose upper jaw is fused to the cranium Filter feeders rely on their ability to open their mouths and to hold them open for long periods of time as they swim through the water straining or ltering out small planktonic organisms Cape and suck feeding is quite different from lter feeding and hit and run in that it depends on the ability to create suf cient negative pressure to suck individual food items from the surrounding water In these last two approaches to feeding lter feeding and gape and suck the strength of the bite loses signi cance and what becomes important instead is the shape and size of the mouth when it is opened It turns out that the vast majority of shes are gape and suck feeders They don39t grab hold of prey or bite off pieces but select individual prey items for capture and engulf whole organisms They do this partly by extending their jaws around the prey and partly by creating negative pressure in the oral cavity that draws the prey and the surrounding water toward the mouth Here again its the shape and size of the mouth opening as well as the ability to open the mouth quickly that are of primary signi cance Because the jaws themselves seldom make any contact at all with the prey in gape and suck feeders it becomes easy to understand why strong rm grasping jaws could be sacri ced for loose relatively fragile gape and suck type feeding mechanisms We can also conclude that gape and suck feeding must be an ef cient and highly successful way to feed since the vast majority of living shes do it this way 8 BIOMECHANICS OF FEEDING IN A PRIMITIVE TELEOST Let39s now take a look at the biomechanics of feeding in a primitive teleost The tenpounder genus Elops provides a good example The lower jaw is hinged to the quadrate at letter A The maxilla forms a ball and socket joint with the palatine bone at letter B The maxilla and lower jaw are connected by a double layer of skin so that the skin unfolds as the mouth is opened and folds again when it closes JAW MECHANISM OF ELOPS QUADWE A PRIMITIVE TELEOST There is a ligamentous connection at letters C and D that connects the posterior end of the maxilla to the lower jaw As the lower jaw is depressed the posterior end of the maxilla is pulled forward Remember that this is a primitive teleost the maxilla is well toothed and forms a large part of the gape of the mouth while the premaxilla is small and only slightly mobile there is no upper jaw protrusibility 9 THE RISE OF PROTRUSIBLE JAWS A primitive gape and suck feeding mechanism similar to what we nd in Elops seems to have provided the raw material for the evolution of protrusible jaws setting the stage for an explosive radiation of forms primarily within a group of teleosts called the Perciformes DIAGRAM OF RELATIONSHIPS OF THE MAJOR GROUPS OF LIVING TELEOST TETRAODONTIFORMES I PLEURONECTIFORMES I I L PERCIFORMES SYNBRANCHIFORMES to GASTEROSTEIFORMES SCORPAENIFORMES ATHERINIFORMES 39 GOBIESOCIFORMES ZEIFORMESto LAMPRIFORMES LOPHIIFORMES to BATRACHOIDIFORMES OPHIDllFORMES and GADlFORMES B PERCOPSIFORMES SCOPELOMORPHA STOMlIFORMES SALMONIFORMES 39 OSTARIOPHYS CLUPEIFORMES ELOPOMORPHA I r T PHOLIDOPHORIFORMES Generalized diagram of relationships of the major groups of extant teleosts All lines indicat ing postulated relationships are shown as the same regardless of whether the affinity is consid ered highly speculative or relatively certain The area of the blocks is roughly proportional to the number of species recognized in the indicated group the black area represents the percent age of species normally confined to fresh water In the most derived groups of teleosts particularly in perciforms the premaxillae have developed a long ascending process that overlaps the dorsal surface of the snout When the mouth opens the maxilla acts as a lever to push the premaxillae forward the ascending processes slide along on the upper surface of the snout providing contact with the cranium even when the mouth is fully protruded PROTRUSIBLE JAWS IN A PERCIFORM FISH In addition to the ascending processes perciforms have evolved a set of ligaments that connect the bones of the upper jaw to the cranium These ligaments which seem to be a prerequisite for upper jaw protrusion stabilize the upper jaw while at the same time provide for mobility a system of crossed ligaments that provides multidirectional strength as well as the exibility required for protrusion CROSSED LIGAMENTS IN THE SNOUT OF A PERCIFORM FISH ar articular process of premaxilla as ascending process of premaxilla eth ethmoid bone mx maxilla mxh articular head of maxilla pl palatine pmx premaxilla 10 THE UNPARALLELED SUCCESS OF PERCIFORM FISHES The culmination of upper jaw evolution reached in perciform fishes has been called a tremendous improvement over former ie more primitive biomechanical approaches to feeding The great improvement however is not so much re ected in an individual sh but rather in perciforms as a whole It39s true that protrusible jaws do increase slightly the overall effectiveness of the feeding mechanism they allow for the creation of a slightly larger more circular mouth opening and thus help to increase the suction pressure created when the mouth is opened But the big improvement really lies in the greatly increased evolutionary potential of the mouth parts to evolve in a whole host of different directions to exploit any and all available food resources It is primarily the perciform mouth that has enabled the enormous variety of specialized predaceous as well as nonpredaceous feeding mechanisms that we see in derived teleosts And it is the evolution of this jaw mechanism that has promoted the highly successful exploitation of food resources that were up until this time largely unavailable to actinopterygian shes The protrusible mouth of perciforrn shes and their derivatives groups was and continues to be a major factor in their success 12 BIOLOGY OF FISHES FISH 311 FORM AND FUNCTION SENSORY MECHANISMS ELECTRIC ORGANS AND ELECTRORECEPTION OBJECT LOCATION AND IDENTIFICATION ELECTROCOMMUNICATION General topics 1 2 3 Distribution of electroreception among living shes Passive electroreception Active electrosensory systems Electrolocation object location and identi cation Electrocomrnunication 1 DISTRIBUTION OF ELECTRORECEPTION AMONG LIVING FISHES ALL FISHES NONELECTRORECEPTIVE FISHES ELECTRORECEPTIVE FISHES specialized receptors absent normally use electrical signals most all teleosts ie the vast present in the environment majority of shes specialized receptors present NONELECTRIC FISHES ELECTRIC FISHES electric organs absent specialized electric organs passive electroreception present active electroreception sharks rays polypterids 13 families in six relatively eels cat shes lung shes unrelated orders MARINE SPECIES FRESHWATER WAVE SPECIES PULSE SPECIES sharks rays the SPECIES cat shes electric organ discharge electric organs discharge eel genus Anguilla freshwater rays is sinusoidal usually in short widely separated marine cat shes Paramotrygon and high frequency pulses repetition lung shes with very small rate usually low variation Gymnarchidae and widely variable and some gymnotids Mormyridae some eg Sternopygus gymnotoids e g Eigenmannia Electrophorus and Apteronotus Gymnotus Hypopomus some skates Torpedinidae Malapteruridae and Uranoscopidae As shown here electroreceptive shes include taxa that are nonelectric as well as electric The numerous nonelectric forms possess electrosensory tuberous organs polypterids eels cat shes and lung shes ampullae of Lorenzini sharks and rays or similar organs they are said to have passive electrosensory systems because they only react to external electric stimuli they are strictly electroreceptive In active electrosensory systems the shes provide electrical stimuli they are electrogenie to which their own electroreceptors are sensitive electroreceptive the receptors in active systems can of course react also to external stimuli 2 PASSIVE ELECTRORECEPTION A number of different relatively unrelated groups of shes including sharks rays the39bichirs and reed sh Polypteridae eels cat shes and lung shes have specialized sensory receptors that allow them to detect minute electrical currents in the water tiny electrical elds that are produced by the muscle contractions of other aquatic organisms These receptors are called external pit organs open to the surrounding water by way of canals that are lled with an electrically conductive gelatinous substance There are generally two kinds of external pit organs tuberous electroreceptive organs and ampullary electroreceptive organs Conductive gel can unannnnnaannanaa SellHing 39 Receptor cell I Sensory neuron SenSOry neuron Tuberous Organ Ampullary Organ A 8 Schematic diagram of the structure of tuberous A and ampullary B electroreceptive organs Both organs are surrounded by layers of attened cells that are tightly joined to one another This helps prevent current from bypassing the organs Tight junctions between the receptor cells and supporting cells help focus incoming electrical current through the base of the receptor cells where they synapse with sensory neurons Supporting cells in ampullary organs produce a highly conductive jelly that lls the canal linking the sensory cells to the surrounding water Of these various pit organs the best understood are the Ampullae of Lorenzini of elasmobranches very similar structures are also found in the marine cat sh genus Plotosus rst discovered and described in the torpedo ray by the Italian anatomist Stefano Lorenzini in 1678 Mandibular ramus V Trigeminal nerve V Ampullae Supraorbital Superficial FaCial nerve VII supraorbital canal Opthalmlc Acoustic nerve VIII group ramus VII Vagus nerve X Deep ophthalmic Eye f ramus V Lateral line canal quotL 39 m Semicircular ear canal o I Supraorbital canal 11 Hyomandibular ramus 39 395 39 39239 5 of facial nerve Ampullae 39 4 9 internal buccal k 539 214 3 E a t l v u n Qa in a f39 r y quotquot quotquotquot quot G39ll sl39 Nasal capsule 3955 475 I it lnfraorbital canal C AmPUllaEZ hyoidean group Internal buccal manGPSEgiaerzou ramus of g p Hyomandibular canal fac39a39 nerve Mandibular canal Ampullae External buccal ramus VII external buccal group Infraorbital canal Distribution of the ampullae of Lorenzini and sensory canals and their innervation in the head of shark The ampullae of Lorenzini are located primarily on the snout but also on the lower jaw and just anterior to the rst gill opening They are important in locating hidden prey for example small shes and invertebrates hiding on the bottom beneath mud or sand by sensing the electric elds produced by small muscular movements such as those made during respiration Actual experimental proof that certain shes use electroreception as the primary modality in prey detection was reported by Andrianus J Kalmijn in 1971 The Electric Sense of Sharks and Rays Journal of Experimental Biology 55 3713 83 In this classic study the spotted dogfish Scylz39orhinus canicula feeding on juvenile at sh Pleuronectes platessa that had taken refuge beneath the sand was shown to ignore olfactory cues when electric potentials produced in part by contracting respiratory muscles of the at sh were present The shark even ignored visual cues in preference to electrical stimuli received by way of the ampullae of Lorenzini Feeding responses of Scyliorhinus canicula toward a flat sh a Pleuronectes platessa under sand b flat sh enclosed within an electrically transparent agar chamber c pieces of sh in an agar chamber 1 flat sh in an agar chamber covered with an electrically insulating plastic lm e electrodes simulating the bioelectric eld of a flat sh and f a piece of sh and an electric eld Solid arrows indicate responses of the shark dashed arrows indicate flow of seawater through the agar chamber After A J Kalmijn 1971 3 ACTIVE ELECTROSENSORY SYSTEMS Fishes are the only animals that are sometimes equipped with organs speci cally adapted to generate an electric discharge Yet within elasmobranchs and teleosts electric organs appear in a number of relatively unrelated groups occupying a wide variety of environments Such structures have evolved independently at least six times Although belonging to diverse taxonomic groups active electroreceptive shes share a number of attributes they are all generally slowmoving or sedentary they are active at night or in murky waters of low visibility and have thickened skin that acts as a good insulator Most have reduced eyes and some torpedo rays are blind Remarkable adaptations in their brains set shes With active electrosensory systems apart from all other shes generally the cerebellum is enlarged greatly so in the African mormyrids LATERAL LINE NERVES BRAIN AND NERVE ADAPTATIONS of electric sh are readily apparent Brain of typical nonelectric sh top has prominent cerebellum gray Regions associated with electric sense color are quite large in Gymnarchus middle and even larger in the mormyrid bottom Lateralline nerves of electric shes Ire larger nerves of nose and eyes smaller 6 In all thirteen families of shes representing six orders are recognized as having active electrosensory systems These are divided into strongly electric forms ve families and weakly electric forms eight families STRONGLY ELECTRIC FORMS 1 Torpedo or electric rays families Torpedinidae and Narcinidae 10 genera about 40 species all major oceans and seas of the world benthic some of the larger species eg Torpedo nobiliana capable of delivering a shock of 220 volts 2 Electric cat sh family Malapteruridae a single species Malapterurus electricus freshwater tropical Africa known to reach a length of about 1 meter and to produce shocks of 350 volts Diagrams illustrating positions of electrical organs in strong electric fishes A electric eel Electrophorus B electric ray Torpedo C Stargazer Uranoscopus D electric catfish Maapterurus 3 Electric eel family Electrophoridae a single Species Electrophorus electricus freshwater Amazonia reaches a length of nearly 3 meters shocks of 350 volts are common but said to produce maximum shocks of 650 volts 4 Electric stargazers family Uranoscopidae a single genus Astroscopus and ve species Atlantic and Paci c coast of tropical and subtropical North America usually found burrowed up to their eyes in soft sandy or mud bottoms can deliver up to 50 volts The function of strong electric organs appears to be stunning prey and discouraging intruders or predators Use of electricity to obtain prey has been observed in torpedo rays and its use for this purpose in other strong electric forms seems probable considering the circumstances under which the electric species live All are secretive living near the bottom often in turbid water Electric stargazers can be especially well concealed nearly totally buried in mud or sand with only their eyes protruding and allowing sometimes luring small crustaceans or shes to approach unaware of impending disaster WEAKLY ELECTRIC FORMS 5 Skates family Rajiidae 14 genera about 230 species all major oceans and seas of the world 6 Elephant shes families Mormyridae and Gymnarchidae 17 genera about 190 species tropical Africa and the Nile River 7 Knife shes and featherbacks families Sternopygidae Rhamphichthyidae Hypopomidae Apteronotidae and Gymnotidae 22 genera and about 54 species restricted to freshwater habitats of tropical Central and South America Diagrams illustrating positions of electrical organs in weak electric fishes A Mormyridae B Gymnarchidae C Rajidae Electricity in weakly electric fishes except in the skates in which the function is unknown functions in location and identification of nearby objects and in electrocommunication 4 ELECTROLOCATION OBJECT LOCATION AND IDENTIFICATION H W Lissman in a series of papers published in the early 1950s especially his 1958 classic quotOn the function and evolution of electric organs in shesquot Journal of Experimental Biology 35156191 was the rst to propose the idea that weakly electric fishes locate nearby objects by detecting the distortions that are produced in the sh39s own electric eld Nonconducting object Flow of electric current Electroreceptors Electric organ The principle of active electrolocation The location of the electric organ is indicated by the black bar The solid lines give the current ow associated with electric organ discharge The electroreceptors which monitor voltage changes across the epidermis are found in pores of the anterior body surface Each object with conductivity different from that of the surrounding water distorts the current pattern and thus alters transepidermal voltage in the area of skin nearest to the object OBJECTS IN ELECTRIC FIELD of Cymnarchus distort the lines and converge toward a good conductor right Sensory pores in the of current ow The lines diverge from a poor conductor left head region detect the effect and inform the sh about the object Lissman showed further that the weakly electric fish Gymnarchus niloticus could be trained to respond to the presence of a glass rod 2 mm in diameter even though the rod was placed in a porous pot that excluded mechanical and visual detection Other workers demonstrated that the mormyrid Gnathonemus petersi can even utilize capacitive and resistive characteristics for object discrimination r V A 41WIH nevi m up i Mal M5 l mquot EXPERIMENTAL ARRANGEMENT for conditionedre ex train of different electrical conductivity placed in the pots and to seek ing of Gymnarchus includes two porous pots or tubes and record bait tied to string behind the pot holding the object that con ing mechanism The sh learns to discriminate between objects ducts bestGymnarchus displaysaremarkable abilityto discriminate EVOLUTIONARY CONVERGENCE IN AFRICAN MORMYROIDS AND SOUTH AMERICAN GYMNOTOIDS In numerous morphological and behavioral details weakly electric shes of the phylogenetically unrelated Mormyridae and Gymnarchidae Osteoglossomorpha of Africa and the families of the Gymnotoidei Ostariophysi of Amazonia are highly convergent Q Gymnofidae a D a J Mormyridac Electrophoridae Gymnarchidae One of the most obvious indications of this evolutionary convergence is mode of swimming Characteristic of all the weakly electric shes is an elongate stiff body posture with locomotion generated by the long anal n in the case of gymnotoids or dorsal n mormyroids that helps to ensure symmetry of the electric eld Body undulations ie anguilliform swimming would continually change the distances and orientations among the electric organs and receptors thereby complicating the processing of electroreceptive information An analogous form of swimming in other electric shes e g skates functions in the same way see p 12 The general body plan is similar in all weakly electric shes eg Gymnarchus top a gymnotid from South America middle and a skate bottom All swim with the body held rigid in order to keep the electric generating and detecting organs aligned Gymnarchus is propelled by a long undulating dorsal n the gymnotid by a similar long anal tin the skate by large pectoral ns that resemble wings 5 ELECTROCOMMUNICATION The active electrosensory system of weakly electric fishes is also used in shortrange intra and interspecific communication Electric communication occurs when one sh the sender emits an electrical signal that evokes a behavioral response from another sh the receiver Electric shes can detect each other39s presence by using their highfrequency electrical receptors to sense the electricorgan discharge of a member of the same species or closely related species Under laboratory conditions the range at which signals can be detected by a recipient sh may be as much as 135 cm 45 ft Hypopomus 5 I l He j Staetogenes 5p Wag Gymnotuscampo Sternopygux marrurus mmwmmmnmmnmmmmw WA Eigenmannia virescem Sternarclzus alln39frons A r A I O M V V 100 msec quotl msec Electric organ discharges from tiection means positivity of the head end several species of the South American family The last two are wave species all the others Gymnotidae Each discharge is shown beside arc pulse species the fish it comes from and on both slow left and fast right time bases Upward de Electrocommunication is used in courtship aggression appeasement and sometimes in identifying the species sex and even the individual In addition to the recognition function of electrocommunication at the level either of species or of sex weakly electric shes may generate signals to warn of impending attack to signal submission or for courtship Possible displays include discharge cessations brief accelerations bursts buzzes and rasps A sharp increase in discharge frequency for example may indicate threat Whereas discharge arrests or cessations may indicate submission in the losing sh In some mormyrid species electrical signaling serves in schooling behavior SUMMARY OF MODES AND ROLES OF ELECTRORECEPTOR FUNCTION MODE Passive animal detects elds from external sources Animate membrane potentials of other organism dc eg gill potentials acslow dc modulated by slow movements acfast muscle heart electric organ action potentials Inanz mate sources motion of water mass in earth s magnetic eld electrochemical atmospheric geological processes Active animal detects elds caused by its own activity Anz39mate membrane potentials from own body do acslow acfast same as for passive mode above Inanz39mate sources induced potentials from swim ming in earth s magnetic eld ROLE Electrolocation Close range passive detection of other sh active detection of objects and spaces Long range directional navigation Electrocommunication Constant signals related to place kind sex individual Czangz39ng signals related to food threat attack submission mating THE LlVlNG MUSEUM Peter Moller Q d His Talking Fish by Herrry S E Cooper Jr On the second oor of the American Musetrm of Natural History a long wind ing corridor leads to the Department of Ichthyology and a laboratory full of tzmks stocked with eels cat sh and elephant nosed sh All are electric Peter Moller a trim man in his ezu39ly fties moves swiftly about the room almost as il he were being propelled by the electric sh he has been studying for twenty ve years He dips a pair of electrodes into a tank containing a black ghost eel from South America and listens to the static emanate ing from a cheap white plastic speaker The veeinch sh which undulates as mysteriously as ectoplasnr generates a highpitched piercing hum Next Moller drops the electrodes into a large tank housing a school of ungainly sixinchlong blackbrown elephant nosed sh with forked tails and trunklike aps drooping from their snouts The cacophe ony that fills the room sounds as if someone had dropped an elece tric heater into the tank The explosion of sound from the arm pli er means nothing to me but is full of meaning for Moller You can hear several sh talkingquot he says I can discriminate two different voices Now a third chimes in 1 am reminded of the fictional Dr Doolittle of Pud dlebyon theMarsh who lacking Mol ler s electrodes eavesdropped on sh 62 NATURAL HISTORY 196 by dipping one car into an aquarium These talkative sh did not t the corn mon perception of the deadly electric eel but as Moller explained there are two groups of aquatic electriciansquot weakly and strongly discharging ones He hap pened to be particularly well versed in the subject he said having spent ve years writing Electric Firres History and Be havior Chapman and Hall The strongly discharging freshwater eels and cat sh are hi ghevoltage and hence highepro le creav tur39es who use their SOOeodd volts to stun their prey To achieve a similar effect tor pedo rays which are marine animals use a strong current of several amps instead of high voltage which would be easily short circuited in the highly conductive saltwae ter Reportedly but not in reality accord ing to Moller electric eels can fell an ox The strong disehargers have been known Li irtg their sliellcrfmm the aquarium PeterMoler reveals a school of electric elephantnosed fir1 since antiquity although the ancients did not know about electricity Fivethousand year old hieroglyphics in Egyptian tombs identity the cat sh as the protector of shes presumably because shermen netting a rich haul from the Nile that in cluded the odd cat sh or two would feel a mysterious emanation when they touched their catch the jolt would cause them to release the entire net ll Unlike the strong dischargers the weakly discharging ones are scarcely known at all Charles Darwin knew of a weakly discharging skate that seemed to shortcircuit the theory of evolution In a chapter in The Origin of Species in which be dealt with some unresolved questions he asked why it was that the weak dis charges had evolved at all And where were all the intermediate strengths And what was their use Equipment sensi tive enough to mea sure the exceedingly weak discharges was not invented until the turn of the century In the 1950s British sci entist Hans W Liss mann proposed that these discharges might have some sort of sensory role If so he postulated the sh must have organs sensitive to electric currents This proved to be the caseiin deed the organs had been discovered fty years earlier by a German scientist who had not known their signi cance New J Beckett AMNH called electroreceptors they had evolved all over the body from mechanorecep tors organs that allow a sh to sense me chanical distmbances in the water So here in the twentieth century we have a new sense an electric sensequot Moller told me when I saw him in early July quotWhenever a pulse is emitted the sh is surrounded by an electric eld Each time the sh pulses there is a eld when it stops the eld is gone Why does the sh do this Imagine an object near the sh Each time the sh pulses the object will distort the eld It changes the way the current ows through the sh s body i creates a sort of electric shadow on the an imal39s body surface which is packed with electroreceptors The in will 39see39 an image and discriminate what it is by its size shape movement and electrical propertiesquot Almost all electric sh are nocturnal which makes the evolution of an electric sense reasonable The electric sense would also help sh orient themselves a subject of particular interest to Moller In the midP9605 as a graduate student at the Free University of West Berlin he studied orientation in spi ders with zoologist Pctcr Gomer One day a French scientist Thomas Szabo ot39 the Centre National tle la Recherche Scien ti que visited the spider laboratory in Berlin and told Mol lcr about his own work involving the ability of electric sh to per ceive discharges from other shihe in fact had discovered the physiological bases of the electrorcccptor39s in African weakly discharging lish He invited Moller39s collaboration on a study of how electroreceptors were involved in social behavior Now in New York Moller and his stu dents work on the behavioral significance of electroreceptors and social behavior We know electric sh have the capacity for interaction for communicationquot Moller said And now the story really gets exciting How do lish go about signal ing and communicating And what do they say to one tutotherquotI That s what my students and l have been studying for the last twenty ve yearsquot Much of Moller s eldwork has been done in Africa on elephantnosed sh and their relatives and although he has never been to South America his laboratory is ftrll of sh from both continents The electrical sense appears to have evolved separately in Africa and in South America after they split apart Moller explains that the relationships evident in the vertebrate family tree show that ancestral vertebrates a4 NATURAL Hrs r39onv lQo evolved an electric sense early on and that only some primitive sh lineages survive ing todayisuch as lzunpreys sharks and sturgeonsiretained this ubi t In mod em sh the teleosts the electric sense has evolved again in several species indepenv dcntly on the two continents In the eld we re interested in such things as the shes distribution abune dance and behavior both territorial and social he said During the day we lay out our electrodes and set up a central sta tion with oscilloscopcs speakers tape recorders and acoustic sh monitors Then at night we look at the electric trail c pouring through our electrodes We see the pulses vary in shape and sizelw tricwave form is a good indicator of types of sh In several species different pulses We khow that these sh use electric sighctls to comrhUhicote but what are they soyihg also signal male or female So the different wave l omis may serve to keep different species apart or attract the other sex quotWhat we want to do is to ask certain questions For example what are the meanings of the pulse ver the elec trodes there is a terri c cacophony How do the sh tell one another apart I think they can recognize signals of individual sh just as we can make out a familiar voice or hear our own name mentioned across the room over the chatter of a cock tail party How do they do it We cannot answer these questions in the eld So dur ing the day we catch sortie of the sh with the help of local shermen put them in plastic bags lled with oxygenated water and bring them back to the laboratory in New York We also btry sortie sh from importers herequot Listening to the clcphantnosed sh Mollcr translated the seemingly random signals for me quotSoon you realize sh can change the rhythm of their pulses They can discharge faster And the tacetacetac will vary When you study the interactions ot two sh as I m doing now after a w 39 you see that what sounds like an incoher ent pattern is no longer chaotic but pre dictable As one sh increases its rate the other one slows down Then the quiet sh will start speaking in a different rhythm turd the rst one will stop as though to hear him better What are they talking about Here in my lab we look at sh in different situa tions We study them at rest and when they 2u e interacting with one another We try to record their different patterns and then play them back to other sh to see how they r39eactian old ethological trick used successfully with birds and mzmy other species And we get quite sophisticated We have the sh decide whether a pattern is attractive or repellentquot He took me to a long narrow tank where he explained an experiment that he is working on with a French colleague Jacques Serrier of the Centre National de la Recherche Scienti quc A hollow tile similar to a section of drain pipe which the nocturnal sh often use during the day for shelter was at one end a second move able hollow tile was suspended from a track above the tank The idea is to move the sh in the suspended shelter closer to or farther from the sh in the stationary shelterquot Moller said quotClose up one sh will stop discharging Is be making him self invisible Or is he listening closely to the other sh Both theories may be cor rect We ve learned that sh can commu nicate at a distance ten times that from which they can locate each other So you have to be very close to locate another sh with your own eld If you are common eating and l tun locating you your come munication can disturb my electrical eld So while I m doing this I can block out your chatter There39s a neat neural cir cuit discovered by Curtis Bell 1 colv league in Portland Oregonithat does iisquot Sometimes Moller or Scr39ricr will re placc the sh in the movable tile an elee pliantnosed sh or another African weak discharger called a baby whale with a dummy sh that pulses ottt some of the signals the scientists want to decipher In the stationary tileI ptrt a sh I know one whose pattem is familiar lIis tactactacs are so fast they come in bursts we call him a bursting sh He loves to burst Then I drive the dummy sh emitting its signal toward the bursting sh When the dummy enters the live sh s communica tions range it will answer with a burst I move the dummy away I can teach the live sh to change its signal il it wants to doesn t like the dummy patient the live sh can go on bursting and drive the dummy away again Their maybe we ll change the dummy s rune il the live sh likes it it will change its tune to bring the durrrmy closer ln this wav we can begin to know what the dummy aying One intriguing puzzle is that the sh in the tanks never talk sex Fish caught in the wild lose their ability to signal their sex in captivity Robert Landsman a graduate student in Muller39s lab was assigned to the problem and discovered that they also lose sex hormones itr their blood Many wild arriirrals become less sexually active in captivity arid the same is true of people under str39es quotThis shows that sh are people tooquot Moller saidia sentiment worthy of Dr Doolittle Moller and his students want to nd out which stresses in the seemingly placid environs of a sh tank can cause sexual dysfunction Moller39 is now trying to crack the code of the strongly discharging sh Most of the sensory and it C i done with the weak drsclrargcrs perhaps because there is less danger of electrocut ing lab assistants The weak dischargers E 9 7 E5 1 5quot m w lh strOhg discharges the whole sh is me big power plant used to sturt prey generate their signals from modi ed mus cle tissue usually near the tail or in a va riety called star gazers from tissue near the eyes quotWith the strong dischargers the whole sh is one big power plantquot Moller said quotin the eel and many others the head is positive the tail is negativequot Only if people grab the sh by its head with one hand and its tail with the other are they apt to get a sizable shockiin which case the whole body becomes part of the electric circttit Some distance from the sh a person would lee only a slight tingle because the electric held diminishes in force with the inverse cube of dis taneeiwhich is why Moller i skeptical of accounts ol electric eels stunning oxen The primary purpose ol the strong dis charges 0139 course is to stun prey Electric cat shigrayubrown bcwhiskered sh that grow to a length ol three feet in Africa although Mollcr s under one foot lack the ability to discharge weakly These protectors ol shes give off a few strong pulses during the day btit alter nightfall their volleys last longer and are at a higher frequency 500 cycles per second If Moller drops a gold sh into the tank the volleys last longer yet until the prey is stunned into edible quiescence In the wild cat sh are eclectic eaters after a night of highvoltage activity their stoma achs reveal a good cross section of the river with one major exception strongly discharging electric cat sh stay away from their weakly discharging relatives While working on her PhD thesis one of Moller39s l39ormcr students Catherine Rankin band that they switch off their power plant in the presence of other elece tric cat sh possibly because they smell F them Two Catlile even itquot they are rivals for the same territory will not shock each other although they might lock on to each others39 mouths and west c Tire cat sh apparently also use their suong discharges in communieatiotrgor at least they have the capacity to do so This was discovered by John Van Wetter ing a student in the laboratory who has been playing back the strong pulses into the tank to see if the cat sh can liscrimie nate between the length and strength of a volley of dis 39 rarges They can quotSo they are able to signal although we don t know that they actually do signalquot he said Unlike the cattish electric eels have the ability to emit both strong and weak dis charges very likely they locate their prey with the low discharge then zap it with the strong one Presumably they do a bit of talking as they errt pass the hol landaisequot that sort of thing Moller has a couple ol baby ccls in one of his tanks cl egant black lislr about six inches long they undulate gracefully across the tank They will grow to be sixlooters Moller showed me a photograph of a colleague holding a fullgrown one by its head and its tail The eel is deadquot Muller said If it were alive he would never dare do that Henry S F C mpci39 IIZ Maric about rr39imv Iislsjiu39 The New Yorkerhr rivetinghie years and is Itc curltar rgfcigil books on space 7ll39lllr11 BIOLOGY OF FISHES FISH 311 FORM FUNCTION AND BIODIVERSITY EARLYLIFE HISTORY EGGS AND LARVAE TECHNIQUES AND APPROACHES ONTOGENY AND PHYLOGENY General topics 1 2 3 Introduction Sampling of eggs and larvae Development of eggs Development of larvae Identi cation of eggs and larvae Ontogeny and phylogeny 1 INTRODUCTION The earlylife history of shes or the egg and larval stages of shes is a fascinating subject and its importance has been recognized by scientists for more than 140 years The range of developmental patterns is broad and the morphological diversity of sh eggs and larvae matches and in some cases exceeds that seen in adult shes 39 MM 58 mm 100 mm TL 33 mm 83 mm 3395 mm 3L N 190 mm SL However the early development or ontogeny of most sh species is not known or has not been described In fact it has been estimated that of all sh species worldwide the eggs of only 4 and the larvae of only 10 are known In the Eastern North Paci c the eggs of approximately 10 and the larvae of about 44 of the species are relatively well known Fish eggs and larvae differ anatomically physiologically behaviorally and ecologically from the adults that they eventually become and so studies aimed at examining these early stages must be done to get a complete picture of the biology of shes In addition information about the earlylife history stages of commercially important sh species is closely tied to proper management of these sheries An understanding of the early stages of noncommercial fishes is equally important because they belong to the same ecosystem and interact extensively with commercial shes 2 SAMPLING OF EGGS AND LARVAE The collection or sampling of sh eggs and larvae help to provide a number of things about sh species populations and communities First we can determine the species present in a given area and in a given time of the year By sampling at different times of the year and over several years we learn whether the species present change seasonally or from yeartoyear because of changes in the physical environment Sampling can also be used to determine the geographic distribution of eggs and larvae This is important because the distribution of eggs and larvae is often not the same as that of adults especially in places where currents transport freely oating eggs and larvae Currents affecting transport of blue sh larvae Pomatomus saltatrix in North Atlantic Ocean Especially for species that lay pelagic eggs sampling can help to determine the spawning area of the adults By knowing the developmental stage of the eggs and something about the water currents in the area we can trace the eggs back to the location of the spawning area For example this has been done to determine the location of the spawning area of walleye pollock T heragra chalcogramma in Shelikof Strait Alaska A Semidi ls gShumagin Is a zquot 39 a 5839N 58 N 5m 67 quot 56 56m 55m 55 45 39I 54 182 I 1534 I mixw 1 151quot I 1521 54 is 15th I 152339 I 15quot I 12quot Sampling can also be used to study larval ecology Egg and larval collections have been used in studies of starvation predation disease competition and the condition of the physical environment eg effects of storms water temperature and pollution In addition quantitative samples of eggs and larvae can be used to make relatively accurate estimates of the number of spawning adults or the spawning biomass in the population Collections of eggs and larvae are also frequently used in taxonomic and phylogenetic studies A number of different methods are used by researchers to collect planktonic pelagic sh eggs and larvae Eggs are usually collected by vertical egg tows in which a net is lowered to 70 meters and then retrieved at a constant rate Larvae are usually collected in oblique net tows in which the net is lowered to a particular depth and then pulled back to the boat as the boat moves forward Some collecting gear employ multiple nets with each net collecting at a speci c depth range This allows us to determine how the larvae are distributed vertically in the water column Another method used to collect larvae is the neuston tow sampling just the upper 10 cm of the water Once the nets are back on board the boat they are washed down with formalin and the samples are sorted The eggs collected are then preserved and stored in 3 5 formalin Eggs are never stored in ethanol because it makes them cloudy so that the embryos are not visible Larvae are rst placed in 35 formalin and then later transferred to 70 ethanol erem shlp net release messenger bridle chalnstharamd o tripping mechanism Vertical Egg Tow V 60 cm Bongo sitting net bars M r poms ofnet utnchmemt Tucker There are several considerations that must be addressed when collecting sh eggs and larvae Extrusion from the net or the loss of organisms after capture can be a serious problem Collectors can limit the amount of extrusion by considering what mesh size to use and the speed of the tow Collectors also need to consider how large a volume of water needs to be sampled in order to collect rare taxa or taxa with patchy distributions If particular species are being targeted collectors need to know whether the eggs and larvae are found only in special habitats such as near the bottom near the surface or around structure One problem associated with collection is unique to larvae because larvae can swim though not very quickly avoidance of the sampling gear is possible The ability of larvae to do this is a function of several factors the degree of sensory development of the larvae their size and speed and the size and speed of the net being used to collect them 3 DEVELOPMENT OF EGGS There has been a great deal of confusion over the years about the best way to de ne the developmental stages of eggs and larvae This is because there is an incredible amount of variation in the pattern of early development among shes The most commonly used de nitions are shown in the table below Full finray complement Attain present juvenile Attain adult squamation body body propor Notochord Notochord begun loss proportions tions Blastopore Tailbud Yolk sac starts to flexion Metamorph of larval pigment pigment END P0NT EVENTS Spawning closure free Hatching absorbed flex complete osis begun characters habits habits I l l l I I I I I l I I 39 I I I l L 391 er devempmemal I E g g I L a r v a I J u v e n i 9 J 5 ag I I I I I l l l TERMINOLOGY r I 39 I I I Yolksac I Transforma I I l39 larva I tI39on larva I I 4 I I I I 39 39 r Preflexion Flexion Postflexmn Pela It or SudeVISIons I Early I MIddIe I Late I ha I Iarva I larva I speciialjuven 7 I l I I I I I Transitional stages OTHER I I l l I TERMINOLOGIES I I I I I I I I I I I I l I l I I I I l I I I l I PrejuvenileI I I m Hubbs19431958 Embryo Prolarva I Post arva I I I I Sette1943 I I L a r v a I I l I I l l I I I I I l I I Nikolsky 1963 I E m I I A Eleuthero Protoptery I39 Y 0 embryo giolarva Pteryg olarva I I 39 I L I Protolarva I merit M e t a a r v a If I I ryo J l I l I l I I I I I Hattori 1970 l39 I I Snyder 19761981 phases I l I I I I I l l I I l l I l l Postlarva I T I I l I l l I I l I I l l l I I I I I I I l I I I I JIr 039 t 0quot I I l 39 I I I Salon 1975 phases Cleavage egg I E m T I I I I I The development of sh eggs is usually divided into three basic stages Early Fertilization to blastopore closure Middle Blastopore closure to embryo tail bud free of yolk Late Embryo tailbud free of yolk to hatching However a complete description of the eggs of a particular species is often divided into more than three stages in some cases many more For example the development of English sole Parophrys vetulus eggs is divided into 15 stages as shown below Some are even more complex for example the development of walleye pollock eggs is divided into 21 stages 4 DEVELOPMENT OF LARVAE As indicated in the table of developmental terminology given above the development of sh larvae is also generally divided into three stages Pre exion Absorption of yolk sac to start of notochord exion Flexion Start of notochord exion to completion of notochord exion Post exion Completion of notochord exion to start of metamorphosis There are also transitional stages between eggs and larvae and between larvae and juveniles The larval development of the horse mackerel T rachurus trachurus is a good example of larval development in general YOLK SAC S PRE ltU FLEXION gt rn FLEXION POST FLEXION J JUVENILE 5 IDENTIFICATION OF EGGS AND LARVAE The identi cation of fish eggs and larvae is not an easy task The specimens are small fragile and usually look very different from the adults And to complicate matters even more eggs and larvae can change dramatically in appearance as they develop 184 mm TL Ocean sunfish Moa mola However there are many characters that are useful for identifying sh eggs and larvae For sh eggs the following characters are often used shape size chorion texture size and number of oil globules size of perivitelline space and embryonic characters late stage only 10 For sh larvae useful characters for identi cation can be divided into ve categories Morphology Shape and length of gut pigmentation melanophores Meristics things you can count Myomeres muscle bands that run along the length of a sh n spines and rays vertebrate Specialized larval characters Elaborate spines especially on head stalked eyes trailing guts enlarged n folds etc Osteology timing of bone and cartilage development Genetics DNA of unknown larvae matched to DNA of known adults 73 mm NL ll There are two main approaches to identifying unknown eggs and larvae The rst approach is called the serial method This method uses adult characters to identify juveniles and progressively links them to smaller specimens through a continuous sequence of shared or similar characters Using this method a developmental series is assembled of identi ed specimens from the largest to the smallest A complete developmental series usually has between 50 and 100 specimens This approach can be used to identify both eggs and larvae Bigeye squaretail Tetragonurus atlanticus Pacific argentine Argentina sialis Mane sh M Caristius maderensis 39 r 39i A second approach involves the use of aquaculture methods to raise collected specimens of unknown eggs or larvae until they can be identi ed or to spawn adults of a species for which the eggs or larvae are unknown and raise the offspring These method are usually only used in cases where the serial method has not been successful 6 ONTOGENY AND PHYLOGENY Though not used nearly as often as adult morphology or molecular characters ontogeny provides an excellent suite of characters for the study of phylogenetic relationships This is particularly true for larvae All of the characters used to identify larvae can potentially be used to construct phylogenetic trees Earlylife history characters can sometimes even solve phylogenetic problems that cannot be resolved by character sets based on adult morphology There are many examples of how ontogeny can be used to determine phylogenetic relationships One good example is the leptocephalus larvae of the orders Anguilliformes eels and Elopiformes tarpon and lady shes Similarly there are no adult characters that support the hypothesis that the order Atheriniformes silversides rainbow shes etc is a natural group However there are several larval characters the preanal length is short approximately 13 of body length there is a single row of melanophores on the dorsal margin of the body and n rays are not visible at hatching Odontesthes debueni family Atherinidae 39 V lso hawaiiensis family lsonidae Bedotia geayi family Bedotiidae l3 The family Myctophidae lantern shes is divided into two tribes This division is well supported by adult characters It has also been found that these two tribes can be distinguished during the larval stage by the shape of the eye one tribe has round eyes and the other has narrow elliptical eyes Tribe Myctophini The superfamily Argentinoidea is composed of four families the Argentinidae herring smelts Microstomatidae Bathylagidae deepsea smelts and Opisthoproctidae barreleyes As adults they don39t look particularly similar Family Argentinidae Family Microstomatidae Family Opisthoproctidae However there are two excellent ontogenetic characters that de ne this group First the chorion has distinctive pustules on the inner surface Second the dorsal and anal fins form in the nfold away from the body connected to the trunk by what are called hyaline strands Nansenia candida family Microstomatidae MICFOStoma SP family Microstomatidae V i j I I and u t 9quotF P 5 quotf 5985 u 39 quot Bathylagus ochotensis family Bathylagidae Bathylychnops exilis family Opisthoproctidae Microstoma sp family Microstomatidae Argentina silus family Argentinidae Although this second character is an excellent one for recognizing the common descent of the superfamily Argentinoidea it is also a good example of convergent evolution because this character also exists in two other relatively unrelated families Myctophidae lantern shes and Icosteidae the rag sh 039 102 mm SL lcosteus aenigmaticus family lcosteidae BIOLOGY OF FISHES FISH 311 FORM AND FUNCTION MODES OF REPRODUCTION OVIPARITY AND VIVIPARITY PARENTAL CARE HERMAPHRODITISM AND SEX REVERSAL General topics 1 Introduction 2 Reproductive guilds of shes 3 Oviparity egg layers and external fertilization OViparity in marine shes OViparity in freshwater shes ViViparity internal fertilization Parental care Hermaphroditism gtSquot S3V 39gt Sex reversal 1 INTRODUCTION You know by now that shes are by far the most diverse of any vertebrate group and that teleosts in particular constitute an assemblage that is larger than all other vertebrates put together In a way we can say that shes do almost everything They have experimented in an evolutionary sense with nearly every kind of adaptation that can be seen modi ed in more derived vertebrates These adaptations may be structural physiological as well as behavioral In the same sense shes are incredibly diverse in how they reproduce Fishes reproduce using nearly every mechanism and strategy you can think of and then some Most of these mechanisms are utilized by more derived vertebrates although it is important to keep in mind that these structural physiological and behavioral adaptations have been independently derived It surely goes without saying that placentallike arrangements in shes have nothing at all to do with the placenta of mammals Despite the diversity and variety of reproductive modes found in shes little is known Compared with what we know about reproduction in other vertebrates shes have been badly neglected Of the 28000 or so known species of living shes breeding habits and subsequent reproductive events are well described for only about 500 species We might be able to add another 500 species to the list about which something is known but the total still adds up to only about 4 percent of living shes This perhaps wouldn39t be so bad if the taxa containing species we know well were not for the most part restricted to aquarium shes primarily Ostariophysi and members of the family Cichlidae and a few commercially important groups Reproduction in itself is an exceedingly complex subject WHICH SPAWNS i OR FAILS Sometimes lo extuminate species To give rise to new Species Role of reproduction in the survival and evolution of species 2 2 REPRODUCTIVE GUILDS OF FISHES The complexity of reproductive modes and strategies in shes is re ected in the following attempt to construct an ecological and ethological classi cation of reproductive systems As envisioned by Eugene K Balon of the University of Guelph Ontario see Journal of the Fisheries Research Board of Canada 326821864 1975 thirty two guilds are proposed to encompass all 28000 living species of shes Ecoethological guilds of shes Section Subsection Guild A Nonguarders A1 Open substratum spawners A11 Pelagophils A l 2 Lithopelagophils A l 3 Lithophils A14 Phytolithophils Al5 Phytophils A l 6 Psammophils A2 Brood hiders A21 Lithophils A22 Speleophils A23 Ostracophils A24 Aeropsammophils A25 Xerophils B Guarders B1 Substratum choosers Bll Lithophils RI 2 Phytophils Bl3 Aerophils B 1 4 Pelagophils B2 Nest spawners B21 Lithophils B22 Phytophils B23 Psammophils B24 Aphrophils B25 Speleophils B26 Polyphils B27 Ariadnophils B28 Actinariophils C Bearers C1 External C11 Transfer brooders C12 Forehead brooders C13 Mouth brooders C14 Gillchamber brooders C15 Skin brooders C16 Pouch brooders C2 Internal C21 Oviovoviviparous C22 Ovoviviparous C23 Viviparous 3 OVIPARITY EGG LAYERS AND EXTERNAL FERTILIZATION By far the vast majority of shes are oviparous that is they produce eggs that are laid and made fertile after they have been laid Something like 96 percent of all living shes are egglayers Fishes exhibit a great variety of egg types and adaptations Morphologically and physiologically they are tremendously diverse EGGS AND EGGCAPSULES A Egg capsule of Spotted Dog sh Scyliorhinus 51 X g B Of PortJackson Shark Heterodontus phillippi X 1 C Of Spotted Ray Rain maculata gtlt D Of Chimaera Chimaera phantasma X a E Eggs of Californian Hag sh Polistotrema stouti gtlt about 5 E Animal pole of a single egg greatly enlarged F Egg of Gar sh Belone belone X about 2 G Eggs of the Black Goby Gobius niger X about IO I L i z I 4 OVIPARITY IN MARINE FISHES Very generally speaking eggs come in two kinds 1 Pelagic eggs eggs that oat 2 Demersal eggs eggs that sink By far the majority of marine shes start out life as pelagic eggs This includes 1 Most all shes that live over the continental slope 2 Nearly all those that range over surface waters of the open ocean and 3 All pelagic deepsea fishes The eggs of these kinds of shes are made buoyant by lowdensity uids acquired from the follicle cells of the ovary or they develop an oil droplet independent of ovarian tissue The upper sunlit layers of the ocean epipelagic zone especially in summer are literally packed with oating eggs and larvae of many different kinds of shes and invertebrates They drift about in the currents gradually becoming widely dispersed from the spawning grounds The eggs hatch releasing small usually colorless larvae that live off the stored reserves in their yolk When this reserve is used up the larvae begin to feed on tiny phytoplankton and zooplankton These rich upper sunlit layers are able to support this myriad of developing forms and are appropriately called the nursery grounds of the sea The kinds of shes that develop oating eggs must be able to produce large numbers of small eggs A fairsized hake Merluccius productus lays about 1 million eggs fecundity in cod Gadus morhua ranges from 2 9 million eggs the gadiform genus Molva may produce in excess of 28 million eggs The ocean sun sh Mola mola is known to produce as many as 300 million eggs The ling Molva molva a deepwater gadoid from the Eastern Atlantic known for its high fecundity High numbers of eggs are necessary for successful recruitment because thousands of eggs and larvae are dispersed into areas far beyond the optimal conditions for survival and thousands die long before hatching or metamorphosis to juvenile stages As you might expect these forms are characterized by having wide geographic distributions Some marine shes lay demersal eggs that is eggs that are heavier than water and thus sink to the bottom after being laid or they are laid directly on the bottom or placed in nests or fastened to rocks shells seaweed sponges and a whole host of other objects Most of these kinds of shes live in nearshore waters and a good many spend their entire lives between the tide marks Examples include blennies family Blenniidae gobies Gobiidae and many other tidepool forms In coastal waters the tides are higher and currents are stronger Tidepool environments are much more rigorous than the open ocean Eggs that sink or even better if anchored to some kind of substrate are much better suited to this kind of environment Obviously oating eggs would be smashed or washed up on shore Eggs and larvae of shes that inhabit these kinds of environments are much less likely to be swept away than a pelagic egg into regions unfavorable to their development In general these forms have a much more restricted geographic distribution These kinds of shes also produce larger eggs with a much larger concentration of yolk than buoyant pelagic eggs The larvae generally emerge in a more advanced state of development Because these shes generally are smaller than true oceanic types and because their eggs tend to be larger they lay fewer eggs Numbers are in the hundreds rather than the thousands or tens of thousands or millions Although an attached egg is much less likely to be swept away by currents or tides it is much more vulnerable to predation Attached eggs make good food for many shes And because there are fewer eggs per spawn it is important to protect them in some way Thus many forms hide their eggs by burying them in silt or sand or by placing them under rock etc Some guard their eggs and others display more complicated degrees of parental care both before and after the eggs hatch 5 OVIPARITY IN FRESHWATER FISHES While most marine species lay pelagic eggs demersal or non oating eggs are the rule in freshwater they sink to the bottom There are several reasons for this 1 It is physiologically more difficult to produce an egg with a speci c gravity less than freshwater 2 Freshwater does not provide the rich food resource in its upper layers as does the marine environment 3 Fast moving rivers and streams would remove nearly all eggs and larvae from a local population preventing recruitment So like inshore marine species nearly all freshwater shes deposit eggs that sink or are sticky and become attached to various substrates Most take no care of their spawn which in nearly all cases involve a great many eggs that are nonadhesive and simply scattered over the bottom Other species with more derived strategies bury their eggs or lay them in some kind of nest usually involving complex behavioral displays Still others hide and protect their eggs within other organisms for example the European bitterling Rhodeus amarus that deposits its eggs inside freshwater mussels 7 as 2 l 39 39 439 w 39 i quot IRAN A quotC g I u 2 q I 39 O 39 I 39 f 27 39 I u z u 4 n n r g n i I I A t e x e Eaquot v a owy lt lIM quot NW quot quot ftvi ll 39 Aw 23gt 39 39 I a All 1 ll f I39 Qt v l v gql o Ru n u I quot 39 M v 39 a r quot 39 quot391 A r A 39 39 39 Ug h f quot hv39 r 5 quot 39 w 26 w s i If 39q a 39 f Male and Female Bitterling Rhodeu amarus with freshwater Pond Mussel X 1 From a photograph The female sh is about to deposit her eggs k us f5 w s m 3 N o 3 Q QM amp Q a g H amp I Q N 3 a E amp H a V a amp V N aw a m a amp 14 July Q amp gm A mg a 1961 Vol 134 No 3472 33 6 OVOVIVIPARITY AND VIVIPARITY INTERNAL FERTILIZATION Ovoviviparous and viviparous shes are similar in that both are livebearing forms that require internal fertilization However they differ fundamentally with regard to the source of nutrition for the developing young In ovoviviparous forms the eggs are retained and fertilized within the body but the young receive no nutrients from the mother they must rely solely on what is provided in the yolk In viviparous forms the young are nourished by some kind of placental connection with the mother Ovoviviparity and viviparity are relatively rare among shes they include only about 4 percent of all living shes but they are among the most interesting When it comes to reproduction Representatives are found among the following taxa Chondrichthyes sharks and their allies livebearers ie guppies and their allies family Poeciliidae the Malaysian freshwater halfbeak genus Dermogenys scorpion shes family Scorpaenidae surfperches family Embiotocidae eel pouts family Zoarcidae clinids family Clinidae and the coelacanths genus Latimeria Internal fertilization involves the use of some kind of intromittant organ a structure used to pass sperm to the female Most live bearing shes have males with such an organ They are usually modi ed anal or pelvic fins Ischiopubic cartilage Base of anal fin Modified anal soft quotWI hm aa quotvu b Gambusia gonopodium Male intromittent organs of two shes a left pelvic n of a horn shark Heterodontus francisci showing its modi cation into a myxopterygium ventral view 39 b anal in modi ed into a gonopodium in the mosquito sh Gambusia a inis lateral view The guppy genus Poecilia is the best known case of ovoviviparity in shes the eggs are fertilized within the egg follicles of the ovary where they develop for some time On rupture of the follicles the embryos are released into the cavity of the ovary where they complete their development They are sustained all this time by the nutrients stored in the yolk of the egg In viviparous forms the young are nourished by some kind of placental connection with the mother A simple kind of pseudoplacenta is found in some cyprinids the best known of which belong to the genus Heterandrz39a In this case the walls of the ovarian follicle acquire an elaborate network of capillaries that extend out as villi and make intimate association with the external surface of the developing embryos A more ef cient pseudoplacenta is found in another cyprinid group species of the genus Jenynsz39a Here the lining of the ovary forms highly vascularized folds that make contact with the gills of the developing ovaries This is called a branchial placenta Branchial placenta in embryos of Jenynsia lineata 0V T ovarian tissue OP 0 opercular opening In still other forms nutrients are obtained by way of food absorbing processes that grow out of the hindgut of the embryo These processes are called trophotaenia or trophonema Trophotaenia Tr emerging from the hindgut of embryos of the viviparous goodeiid genus Zoogoneticus The trophotaenia are highly vascularized and serve for respiration as well as for the absorption of nutritive materials In members of the surf perch family Embiotocidae as many as 20 eggs are fertilized in the ovarian follicles but are soon released into the cavity of the ovary where development is completed In some species the embryos and young may not be released from the female until they reach sexual maturity Q Sun perch 7 PARENTAL CARE Some marine forms and many more freshwater forms retain their eggs after they are laid that is they practice parental care Parental care takes on a host of different modes from simple to highly complex Forms of parental care A Male parental care sea cat shes Ariidae sticklebacks Gasterosteidae pipe shes Syngnathidae and greenlings Hexagrammidae B Female parental care 1 Oviparity with postspawning care the cichlidae genus Oreochromis 2 Ovoviviparity without post spawning care rock shes genus Sebastes 3 Viviparity Without postspawning care Elasmobranchs livebearers eg genus Poecz lia surfperches Embiotocidae C Biparental care bullheads Ictaluridae several cichlid genera e g Cichlasoma and Symphysodon D Juvenile helpers some African cichlids e g genus Lamprologus Within the rst of these categories are many of the oral incubators or mouth brooders In the marine cat sh Bagre marinus as many as 55 large about 20 mm in diameter eggs are laid After fertilization the male retrieves the eggs in his mouth keeping them all well oxygenated and very well protected from predation After about a month the young emerge but remain near the male retreating to the shelter of his mouth whenever there is a nearby disturbance The male continues to protect the young for another two weeks or so Q Mouthbreeding catfish A very similar thing occurs in cardinal shes family Apogonidae which are also marine again it39s the male that does the brooding In freshwater shes members of the family Cichlidae are the best known oral incubators In this group the females do the incubating as much as the males Still others have a different way of taking their eggs with them Egg carriers come in all sorts of adaptations For example cat shes of the family Loricariidae restricted in distribution to tropical South America carry their eggs in folds of skin near the lips Bunocephalid catfishes have evolved a strange system in which the female lies down on the eggs after they have been laid and fertilized The eggs sink into the soft spongy skin of her underside under the head thorax and abdomen The eggs stick there and eventually each egg is carried on a stalked cup that grows from the skin Q Obstetrical catfish Here s an example of eggcarrying in a shallowwater antennariid anglerfish Somehow the female attaches a cluster of eggs to the side of the male and he canies them in a bundle until they hatch COPEIA 1980 NO 3 l Attlemmrl side B Closeup ol pus ertor on fish by rloullleestranded threaddike structures to tlmrlmmcurtiut those spawned by closely related terms that uti lize the typical lophiil39orm reproductive mode described above Further the embryos are con siderably larger more highly developed and supplied with a much greater amount of yolk than embryos of Closely related species For ex ample Rasquin 1958 described embryos ol A tmlw at a stagejust prior to hatching that mea sured less than onethird the length 0139 those of A ramImamtznu the pectorallit bud consisted of nothing more than a mass of undifferene l Photomicrogmph 01 two eggs of Antenmtr in caullimm39ulamt CAS 40369 showing threadlike extensions that form closed loops GAS 0369 male 85 mm SL A Whole sh showing egg ClUSlL T on ehall39 of egg cluster showing attachment to spinulose epidermal surface of tinted rapidly dividingr cellsquot compared to the large pectoral n lobes ofA mtulimrttzulnmi ap proximately 25 of total length and the di ameter of the yolk mass was considerably less than onee fth that oill I39IllIIVIIIM39MIIUML In fact the embryos of A crutrlt39mnwlam appear to be approximately comparable in development to foureday old freeswimming larvae ofA rutm yet even at this staged M39lLlll T larvae are still less than onethird the size of the embryos oi39A C114lmtlltliux It seems apparent that this an tennariid species is employing a mode of re cruitment that is atypical for lophiilbi39tns re taining and caring for a small number of large eggs that hatch into relatively large advanced young Apparently as a result of this alternative mode ol recruitment I attulimtzctlm ux has a narrow geographic range compared to other antennariids being restricted to an area bountlr ed by Sumatra the Philippine Islands and the northwest coast 0139 Australia It has been well documented that antennariid anglerh39shes are ef cient at luring prey by maintaining the immobile inert appearance of a sponge or coralline algaeencrusted rock while wriggling a highly conspicuous bait Wickler 1968 Pietsch and Grobecker 1978i Since eggs provide excellent food for shes it seems apparent that having a visually conspicv uous Cluster ol eggs attached to the substrate like flank of an angler sh would appreciably enhance the overall luring effect If this is true the unusual example of parental care in A mu The males of the nursery shes genus Kurtus which lives in brackishwater habitats of the IndoAustralian region are equipped with a bony hook on their forehead The hook is used to carry the eggs which are in two bundles connected by a brous thread 39 l a n quot t d Forehead brooder 8 HERMAPHRODITISM Some shes are not necessarily male or female many are functional hermaphrodites They can produce both eggs and sperm Examples include sea basses family Serranidae porgies family Sparidae some cyprinids and some deepsea myctophiform shes One part of the gonad usually the inner portion forms the male sex cells Whereas the remaining part forms the eggs Usually one part ripens before the other so that selffertilization doesn t occur but this is not always the case In the serranid genus Serranellus species that occupy coral reef habitats off Florida each mature individual bears both ripe eggs and sperm During the spawning season there occurs cross fertilization between hermaphrodites each sh alternatively playing male and female roles Occasionally selffertilization occurs Ovotestes are found in many deepsea shes In the order Myctophiformes there is a de nite trend toward an increase in the number of hermaphroditic species with depth Shallow epipelagic forms are bisexual while deeper living species tend to be hermaphrodites This trend is easily explained The increasing scarcity of food with increasing depth causes a reduction in population size Meetings between members of the opposite sex become fewer Mutual exchange of sex cells between any two members of the population provides a signi cant advantage The advantage is even more signi cant if a single individual can reproduce all by itself 9 SEX REVERSALS In some forms the gonad is not divided into male and female parts but has the ability to completely change over from one sex to the other In certain sea basses family Serranidae the females when under stress in the absence of males switch sex they produce viable sperm and take on the coloration and behavioral patterns of the male She can then go around and fertilize the eggs of other females Still other species normally go through a change of sex as they mature All of the younger sh in a population may be males until they reach a certain age when they then switch over to become females If the rst half of the lifecycle is spent in the male state the condition is called protandry and the species is called protandrous first maleness The opposite situation is called protogyny and the species are called protogynous rst femaleness Fishes are the only vertebrates that can spontaneously change sex BIOLOGY OF FISHES 39 FISH 311 FORM AND FUNCTION GASBLADDER EVOLUTION AND STRUCTURE SWIMBLADDERS AND BUOYANCY RESPIRATION AND SOUND PRODUCTION General topics 1 Lungs versus swimbladders 2 Evolutionary history of gasbladders 3 Gasbladders as hydrostatic organs 4 Structure of swimbladders 5 Biological signi cance of neutral buoyancy 6 Gasbladders as respiratory organs 7 The role of gasbladders in sound production 8 Bioacoustic studies on reef shes 1 LUNGS VERSUS SWIMBLADDERS Practically all living vertebrates have a gasfilled organ lying somewhere among the viscera of the trunk region Living j awless shes lampreys and hag shes sharks rays and chimaeras a few bony shes and one family of salamanders do not and most available evidence indicates that they never did but see p 3 below This means that gasbladders most probably evolved within a lineage that give rise to the Teleostomi that is the Actinopterygii bony shes and Sarcopterygii coelacanths lung shes and all terrestrial vertebrates 1 2 3 4 5 Sarcoptcrygii Actinopterygii Teleostomi 5 Chondrichthyes 5 Gasbladders Gnathostomata Phylogenetic relationships of jawed vertebrates indicating the most likely point of origin of gasbladders 1 Polypteriformes 2 Acipenseriformes 3 Lepisosteiformes 4 Amiiformes 5 Teleostei 6 Crossopterygii 7 Dipnoi 8 Tetrapoda There are two kinds of gas lled structures 1 Lungs TetrapOd39s 39 Sturgeon 2 Swimbladders 7 and many F39 39 TeleOst Although homologous ie they share an identical evolutionary origin they perform very different functions lungs are used for respiration while swimbladders function to provide buoyancy Both arise developmentally as outpouchings of the embryonic foregut but beyond that they differ considerably in anatomical details One of the most signi cant anatomical differences between the two is that lungs arise from the ventral margin of the foregut while swimbladders emerge from the dorsal margin 2 EVOLUTIONARY HISTORY OF GASBLADDERS Evidence supports the notion that lungs evolved earlier than swimbladders despite the fact that swimbladders are best developed in shes while lungs are best developed in tetrapods Two kinds of evidence Phylogenetic evidence some surviving shes that have functional lungs are not closely related to early tetrapods but come from extremely ancient lineages Examples include the bichir genus Polypterus gars Lepisosteus and the bow n Amia all have functional lungs used for aerial respiration Anatomical evidence certain morphological details of the gas bladders of primitive living shes such as sturgeons paddle shes gars and the bow n are very much like those of lungs of certain tetrapods eg they have alveoli resembling those found in the lungs of amphibians Lepisosteus and Amla A few paleontologists eg Robert H Denison would like to believe there s fossil evidence as well Remains of the extinct placoderm genus Bothriolepis dating from about 380 million years ago appear to have had paired sacs or pouches that extended posteriorly but opened anteriorly into the pharynx an important detail is that these pouches seem to arise from the ventral margin of the foregut just like modern lungs Denison argues that these structures represent the earliest known lung no doubt capable of retaining air gulped in through the mouth But this idea has not received widespread acceptance although no one has yet come up with an alternative interpretation of these structures posterior dorsal fin hypochordal lobe pelvic finJ pectoral appendage Bothriolepis canadensz39s Restoration in lateral view In any case despite the fact that lungs are most characteristic of tetrapods lungs did not appear on the scene with tetrapods they are phylogenetically much older and probably originated within early teleostome vertebrates Let39s now take a closer look at the evolutionary history of gasbladders in all the major groups of living vertebrates and trace the pattern of change with time EVOLUTIONARY HISTORY OF LUNGS AND SWIMBLADDERS QQQs ac bw Sharks Sturgeons Gars Bow n Teleosts Coelacanth Lung shes Tetrapods Swimbladdcr Sm39mhladder Bothriolepis In this diagram lungs and swimbladders are superimposed on a phylogeny of vertebrates Most evidence indicates that lungs evolved early in vertebrate history perhaps they were present in the earliest vertebrates jawless forms perhaps they were present in at least some now extinct placoderms eg genus Bothriolepis fossils of which date back to approximately 380 million years before present perhaps they originated in early gnathostomes and were later lost in the lineage leading to sharks and their allies Chondrichthyes But most evidence indicates a telestome origin The subsequent evolutionary history of lungs is characterized by two independent nonhomologous modi cations of lungs to form swimbladders in sturgeons Chondrostei and teleosts Lungs are retained and elaborated in the single living crossopterygian coelacanth genus Latimeria in lung shes and in tetrapods The notion that swimbladders evolved independently in sturgeons and teleosts is based in part on anatomical differences the swimbladder of sturgeons originates from the stomach while in primitive teleosts the swimbladder develops from the esophagus 3 GASBLADDERS AS HYDROSTATIC ORGANS The primary function of gasbladders in the vast majority of living shes is to provide neutral buoyancy by serving as hydrostatic organs When gasbladders function as hydrostatic organs they are called swimbladders The hydrostatic function of the swimbladder depends on its ability to 1 Maintain a gasfilled space inside the body cavity of the fish 2 Vary the volume of gas in response to changing hydrostatic demands The problems connected with these two anctions are tremendous when you realize what enormous pressures can be created and maintained inside the swimbladder of a sh Most natural water as well as the arterial blood of shes has a partial pressure of oxygen of about 02 atmospheres and a partial pressure of nitrogen of about 08 atmospheres But inside the swimbladder these partial pressures may be 100 atmospheres and 20 atmospheres respectively Water Arterial blood Swimbladder Partial pressure of Oxygen 02 atm 02 atm 100 atm Partial pressure of Nitrogen 08 atm 08 atm 20 atm There is even some evidence that swimbladders of certain deepsea shes are able to create and maintain pressures as great as 200 atmospheres The ability of the swimbladder to concentrate these gases some 500 times in the case of oxygen and 25 times in the case of nitrogen is a unique property of this organ 4 THE STRUCTURE OF SWIMBLADDERS As hydrostatic organs gasbladders are called swimbladders and come in two kinds 1 Physostomous Sturgeons and primitive teleosts 2 Physoclistous Q Egg52 Physostomous swimbladders are connected to the foregut by a duct called the pneumatic duct In ation often requires swallowing air at the surface and forcing it back into the bladder by way of the pneumatic duct de ation usually requires a release of air directly into the water by way of the mouth belching But some shes with this open type of swimbladder have an elaborate system of blood vessels that function to force gases into the swimbladder Via a gas gland and remove gases by diffusion via the pneumatic duct This type of swimbladder is characteristic of sturgeons and primitive teleosts Species that have this kind of a swimbladder are called physostomes to liver capillaries of ca illarie f resorptive area D s 0 gas gland pneumatic duct gas bladder esophagus Swimbladder of a physostomous sh showing the relationships of the gas gland and the resorptive area on the pneumatic duct Physoclistous swimbladders are completely closed separated from the gut through loss of the pneumatic duct The volume of gas inside the bladder is increased and decreased entirely through secretion or resorption of gases from or to the blood This type of swimbladder is found only in derived teleosts Species that have this kind of a swimbladder are called physoclists resorptive area to heart cyan gas bladder gas gland to liver Swimbladder of a physoclistous sh showing relationships of the gas gland and resorptive area Assuming that the goal is neutral buoyancy most physostomes intending to swim at a certain depth have to gulp suf cient air from the surface to attain neutral buoyancy at that depth and then swim down to that depth the sh is positively buoyant throughout the descent Every adjustment to an increased depth again assuming neutral buoyancy is the goal requires a visit to the surface for another gulp of air Every adjustment to a decrease in depth requires a release of gas directly into the water from the mouth In physoclists without pneumatic ducts things are a bit more complex the volume of gas inside the bladder is increased or decreased entirely through secretion or resorption of gases from or to the blood The physostomous condition is certainly the more primitive condition the physoclistous condition is clearly derived The distribution of the two kinds of swimbladders among the major groups of living teleosts is as follows Perciform derivatives Lophiiformes Gobiesociformes PARACANTHOPTERYGH Botrochoidiformes 3 ATHERINOMORPHA i Percopsiformes If Anguilliformes Notoconthiformes ELOPOMORPHA Godiformes Ctenothrissiformes Neoscopelidlike fish egSardinioides M r PROTACANTHOPTERYGII yc h 39ds PhySOCIISts Osteoglossiformes OSTEOGLOSSOMORPHA quot 7 CLUPEOMORPHA Division Presumed Jurassic Protoelopoid Pholidophoroid holosfeons Diagram showing our conception of the evolutionary relationships of the principal groups of teleostean shes Uncertain relationships are shown by a broken line and question mark GonorynchifOrmes Physostomes OSTARIOPHYSI Elopiformes Salmonoids lchthyodectidoe Division III Division I 7 5 THE BIOLOGICAL SIGNIFICANCE OF NEUTRAL BUOYANCY A swimbladder serving as a hydrostatic organ provides neutral buoyancy thus enabling the sh to save energy in two ways 1 The sh is able to remain motionless in midwater without neutral buoyancy the sh would have to swim continuously to either counteract gravity or the tendency to oat up toward the surface 2 A sh with neutral buoyancy requires much less power to swim horizontally at a given speed than does a similar sh with negative or positive buoyancy 6 GASBLADDERS AS RESPIRATORY ORGANS Although hydrostasis is the primary function of gas lled organs in the vast majority of modem day bony shes these structures often perform several additional functions Respiration function in some species gasbladders have retained or have secondarily acquired a respiratory function ie they use their gas bladders as a lung A phylogenetically diverse array of shes breathe air through their gasbladder This trait has evolved and been lost numerous times throughout the evolutionary history of shes Obviously airbreathing through the use of a gasbladder is restricted to those shes that have retained a connection between the esophagus and the bladder physostomes Functional lungs are therefore found among relatively primitive fishes There are many examples among preteleosts and sarcopterygian shes the bichirs Polypteridae the gars Lepisosteidae the bow n Amiidae and the lung shes Dipnoi Family POLYPTERIDAE bichirs Freshwater Africa Family LEPISOSTEIDAE gars Freshwater occasionally brackish very rarely in ma rine water eastern North America Central America south to Costa Rica and Cuba Family AMIlDAE bowfin Freshwater eastern North America Air breathing though the use of the swimbladder is also evident in a diverse assemblage of primitive teleosts for example the bony tongue fishes Osteoglossoidei the tarpons Megalopidae and the trahiras Erythrinidae Family OSTEOGLOSSIDAE osleoglossids 0r bonylongues Freshwater circumtropi cal South America Africa and Southeast Asia to northern Australia Family MEGALOPIDAE Jarpons Mainly marine enters freshwater tropical and subtropical oceans Family ERYTHRINIDAE trahiras Freshwater South America 7 THE ROLE OF GASBLADDERS IN SOUND PRODUCTION Hearing is the most effective mechanism for longrange communication under water Pressure waves are very effectively propagated in water and this form of acoustic energy is the most rapid and most effective means of longrange interactions between shes It seems that all shes have the capability of receiving acoustical stimuli Underwater sounds are made by shes in a host of different ways but most all can be categorized in one of two ways 1 Stridulatory mechanisms 2 Swimbladder mechanisms Stridulatory sounds are produced by friction of teeth n spines or various bones rubbing or grinding against each other or similar hard parts of the head or body Fishes well known for grinding their pharyngeal teeth include the grunts Pomadasyidae the gouramies Anabantoidei and the puffers Tetraodontiformes Family HAEMULIDAE Pomadasyidae grunts Marine many in brackish water rarely in freshwater Atlantic Indian and Pacific Family TETRAODONTIDAE puffers Marine with several entering and occurring in brackish and freshwater tropical and subtropical Atlantic Indian and Pacific Other stridulators well equipped with special n rays and spines designed to make sounds include many of the cat shes Siluroidei the sticklebacks Gasterosteioidei and trigger shes Balistidae cleithrum socket of cleithrum motion of spine pectoral spine view of area of spine that moves against cleithrum Right cleithrum and pectoral spine of a sea catfish family Ariidae showing roughened flange with which stridulatory sounds are made Family ARIIDAE Tachysuridae sea catfishes Mainly marine tropical and sub tropical Swimbladder soundproducing mechanisms generally fall into two categories 1 Indirectly the swimbladder acts as a resonator to change the quality of the sound emitted by some other organ For example stridulation of pharyngeal teeth or moving the bones of the pectoral girdle may set up vibrations that are picked up by the swimbladder and ampli ed 2 In a direct way swimbladders are used to produce underwater sounds either by pushing gas from the bladder out through the mouth belching or by contraction of either the muscular wall of the bladder itself or of specialized muscles that cause the bladder to resonate drumming the sound vibrations are then passed out through the body tissues Belches are produced by gas expulsion from the swimbladder by way of the pneumatic duct Obviously this ability is limited to physostomous shes ie relatively primitive bony shes like eels cat shes and characins Swimbladders can be used as drums in a number of ways either by l beating the pectoral ns against the side of the body 2 beating the opercular apparatus against the body wall where it covers the swimbladder or 3 through use of sonic muscles In drums and croakers family Sciaenidae there are muscles that originate in the lateral body musculature and insert on the swimbladder Rapid contractions of these muscles called Extrinsic Sonic Muscles causes them to beat against the sides of the swimbladder The vibrations take place in short bursts producing drumlike beats or knocking sounds Very similar situations are found in some cat shes Siluroidei squirrel shes Holocentridae brotulids macrourids and many deepsea taxa In some shes the sonic muscles both originate from and insert on the walls of the swimbladder called Intrinsic Sonic Muscles In these forms for example some toad shes genus Opsanus and sea robins family Triglidae the bladder can be dissected out and can function as a sound producing mechanism all by itself just by stimulating the nerves that 1nnervate the sonic muscles Opsanus Batrachoididae tau OYSTER TOADFISH 38 cm I5 in It is found in shallow waters along the e seaboard of N America from Cape Cod to Cuba occasionally straying as far N as Maine It is commonest on sandy or muddy bottoms hiding amongst eel grass It eats a wide variety of invertebrate animals and many small shes intrinsic muscles They have considerable noise producing mil ability and grunt loudly if handled and at night naturally They spawn in summer the Sw1mbladder of a toa39dfish of the genus Opsanus large eggs 5 mm in diameter being laid in showmg intrinsic sonic muscles along outer edges cavities under stones in old tin cans or dis carded shoes The male guards the nest for the 3 weeks of incubation The skin is scaleless and covered with thick mucus How can you tell whether the source of sound emitted by a sh is stridulatory in origin or produced by the swimbladder Stridulatory sounds are nonharmonic they sound like rasps scratches and clicks that occur at irregular intervals Swimbladder sounds on the other hand have a tonal quality to the ear and occur at regular intervals 8 BIOACOUSTIC STUDIES ON REEF FISHES Certain underwater habitats can be a very noisy place While some sounds are produced by various invertebrate animals most are produced by shes Let s now listen to an array of sounds recorded underwater on a patch reef in the US Virgin Islands by marine biologist Torn Bright RESULTS OF THE TEKTITE PROGRAM ECOLOGY OF CORAL REEF FISHES BIOACOUSTIC STUDIES ON REEF ORGANISMS By THOMAS J BRIGHT1 CONTENTS ABSTRACT 45 INTRODUCTION 46 METHODS 46 ACKNOWLEDGMENTS 50 DESCRIPTION OF SOUNDS 50 Background noise 50 Purposeful sounds 54 Adventitious sounds 58 Miscellaneous sounds 62 DIEL CYCLES AND BEHAVIORAL OBSERVATIONS 62 CONCLUSIONS 68 ABSTRACT Underwater habitatbased studies into acoustical behavior of several species of reef shes resulted in correlations between the follow ing sounds and their sources in Lameshur Bay St John Virgin Islands three types of STACCATOS COOS and GRUNT SOUNDS from Holocentrus ascensionis POPS from H Coruscus QUACKS and SQUEAKING DOOR SOUNDS from H mari anus GRUNT SOUNDS from Epineplzelus striatus ROARS and FROGLIKE SOUNDS from unknown sources CRUNCHES from parrot shes Scaridae goat shes Mullidae and Aulostomus maculatus FLUTTERS from Myripristis iacobus and Lactophrys triqueter and FLAPPING from Epinephelus cruentatus Most of the sounds were correlated with either aggressive territorial behavior feeding or escape Diel cycles were demonstrated for the STACCATOS coos POPS QUACKS and FROGLIKE SOUNDS whose occurrence corresponded directly to daytime territorial occupation by or nighttime wanderings of the sound producers l3 The primary objective of this study Los Angeles County Museum of Natural History Science Bulletin 14 1972 was to gather information concerning the nature origin and signi cance of biologically generated sounds in and around a tropical reef habitat Using a variety of underwater recording devices 17 stations were monitored over a twoweek period Various sounds were described as crackling snapping frying pan noises sounds like cold bacon being thrown into hot grease staccatos and coos pops quacks squeaking door sounds roars frog sounds and grunts crunches uttering sounds apping and sounds like marbles being dropped into a plastic cup and rolled around In summary we are only now beginning to realize the importance of sound in sh behavior A lot of highly variable sounds are being produced by shes but we hardly know anything about it We don t know for the most part what shes are making what sounds and when we do know most of the sounds being produced cannot be linked to any speci c observed behavior BIOLOGY OF FISHES FISH 311 FUNCTION LOCOMOTORY MECHANISMS MODES OF SWIMMING ANGUILLIFORM VERSUS CARANGIFORM SWIMMING UNDULATION VERSUS OSCILLATION THE FUNCTIONS OF FINS General topics 1 Forward progress versus directional control 2 Anguilliform locomotion 3 Subcarangiform locomotion 4 Carangiform locomotion 5 Thunniform locomotion 6 Ostraciiform locomotion 7 Swimming by means of ns 8 Nonswimming locomotion 9 Directional control and the function of ns 10 Unpaired ns dorsal anal and caudal 11 Paired ns pectorals and pelvics 1 FORWARD PROGRESS VERSUS DIRECTIONAL CONTROL Locomotion is usually thought of in terms of forces that give rise to forward progress but equally important is the control of forward progress that is the various forces that actually determine where the animal will go These two aspects of locomotion forward progress and directional control are obviously inseparable functions as far as the existence of a sh or for that matter almost any animal is concerned but for purposes of discussion it s convenient to separate the two 2 ANGUILLFORM LOCOMOTION Almost all forward movement in shes originates in the contraction of body musculature Sinusoidal undulation of the body throwing the body into a series of successive Sshaped curves seems to be the basic or primitive mode of swimming in vertebrates This notion is supported by at least two independent lines of evidence 1 Sideways undulation is used to varying degree by all the primitive living shes from hag shes and lampreys to many sharks and lessderived bony shes such as the eels and even salmon and trout 2 Vertebrates are bilaterally symmetrical forms with body segmentation developed principally in the musculature and nervous system suggesting a basic underlying relationship to undulating locomotion Locomotion in an eel or the larval stages of the herring Clupea harengus as shown here which greatly exaggerates the undulating mode of swimming provides a good example I O M W L Anguilliform swimming by herring larva Clupea harengus about 65 mm long with yolk sac Successive cinephotos at 0021 sec intervals are displaced to the right Lower broken line represents a fixed position on background Movements of snout and tail tip indicated by dots Position of wave crests shown by crosses and circles u As the eel moves forward successive waves of muscular contraction pass backward along alternate sides of the body The moving body exures press against the water behind them as shown in the gure above The lateral components of force on the two sides of the body cancel each other out so that the resultant force is directed backward and the resulting movement is forward To slow down or stop the eel or larval herring can simply hold the curved body rigid Water then pushes against the anterior surface of each bend rather than the posterior surface Backward progression can be accomplished by passing the exures along the body from tail to head This mode of swimming is called Anguilliform locomotion named after the true eels Order Anguilliformes which demonstrate this kind of locomotion so well Anguilliform swimming involves virtually the entire body length The side to side amplitude of the wave is relatively large along the body and increases in size towards the tail Because so much of the body participates there are increased drag and vortex current forces associated with this type of swimming making this a relatively inef cient mode of locomotion High speed is impossible Nevertheless Anguilliform locomotion is an obviously successful way to get around in water Although considered to be primitive it is found across many unrelated and evolutionarily distant groups of shes But it turns out that most shes don t swim this way by far most are tailwaggers Instead of using moreorless the entire body to push against the water and thereby propel themselves forward they rely on a much smaller part of the body A smaller part of the body and tail participates in sideways undulations resulting in greatly reduced yaw side to side movement of the head Forward movement of a tailwagger or caudal swimmer appears totally different from that of the eel but in principle it is the same The differences are due to the distribution of body bulk most of which is forward in a typical sh and to the fact that the effect of contracting the body muscles is concentrated in the tail region Throughout the evolutionary history of shes there has been a gradual shift away from the undulating type of locomotion found for example in hag shes lampreys eels and many sharks toward the caudal type of propulsion found in most bony shes Cradation of swimming modes from A anguilliform through B subcuran giform and C carangiform to D thumiiform The black silhouette dorsal View is superimposed on successive positions onehalf tail bent earlier broken outline and onehalftail beat later stippled A Anguilla anguilla 7 cm long about 15 beatssec B Cadus merlangus 24 cm long about 17 beatssec C Scombcr scombrus 40 cm long about 24 l ll39 t D LUIIHIHHUS i inis length unknown perhaps about 40 cm about 24 beatssea The basic advantage of caudal locomotion is that far greater speed can be attained than is possible by undulation Caudal swimming is usually referred to as Carangiform locomotion named after the jacks bony shes of the family Carangidae which exemplify this mode of swimming especially well The extent to which this mode of swimming occurs in various sh taxa varies considerably and at least four subcategories are recognized subcarangiform carangiform thunniform and ostraciiform 3 SUBCARANGIFORM LOCOMOTION In shes that use subcarangiform locomotion the musculature of approximately twothirds to onehalf of the body is involved in producing the propulsive wave responsible for forward motion In comparison with anguilliform swimmers side to side movement of the head yaw is greatly reduced but nevertheless no one point on the body moves constantly in or parallel to the direction being traveled Subcarangiform swimmers are a diverse group including for example salmon and trout Salmonidae minnows and carps Cyprinidae and cods Gadidae They typically have large welldeveloped but exible caudal ns that can be opened or shut to increase or reduce n area by as much as 10 percent during a single tail beat But surprisingly the caudal n does not appear to be the major propulsive force during normal forward swimming Surgical amputation of the caudal n has little adverse effect Instead the large welldeveloped caudal n appears to have evolved in response to the need for rapid acceleration fast turning and highspeed maneuverability 4 CARANGIFORM LOCOMOTION In this form of swimming only the posterior part of the sh is capable of large exure Side to side undulations are con ned to the last third of the length of the body The caudal n is stiff and often deeply forked with elongate upper and lower lobes This n design reduces the amount of water that is displaced laterally and thereby reduces turbulence and frictional drag with no loss of propulsive power To counteract yaw in the head region which might I otherwise result from such high amplitude exures in the posterior part of the body two major evolutionary developments have occurred rst as bony shes have evolved they have become more laterally compressed and deeper bodied that is there is a greater concentration of body mass toward the anterior end of the sh and the median or unpaired ns dorsal and anal have become stiffened by spines and second the depth of the caudal peduncle has become greatly reduced A narrow caudal peduncle reduces the side to side movement of the water and thereby reduces turbulence and drag at the same time increasing the frequency with which the tail can beat CARANGIFORM Drag is further reduced by the development of keels on the side of the caudal peduncle which increase the hydrodynamic shape of the caudal peduncle and the ease with which it can pass through the water Like the other modes of swimming carangiform locomotion occurs in a broad array of sh taxa Examples include many of the herrings Clupeidae some characins Characidae the mackerels Scombridae jacks family Carangidae and many more 5 THUNNIFORM LOCOMOTION Thunniform locomotion is carangiform locomotion developed to the extreme It represents the extreme endpoint in an evolutionary trend toward greater speed in underwater locomotion among shes Burst swimming speeds of greater than 20 meters per second have been recorded in certain shes that employ thunniform locomotion and prolonged swimming speeds have been observed in excess of 4 meters per second In thunniform swimmers very little of the body musculature is involved in providing forward progress Instead thrust is generated almost exclusively by a high lunate stiff and deeply forked caudal n mounted on an extremely narrow caudal peduncle This form of swimming is found among several distinctly related groups but best exempli ed by the tunas suborder Scombroidei and the lamnid sharks suborder Lamnoidei It is also found in many marine mammals whales and dolphins and in the extinct marine reptiles ichthosaurs 4 3 0 O Oo I l THUNNIFORM Thunniform swimming by kawakawa Euthynnus af nis Length unknown perhaps about 40 cm Cinephoto intervals 006 sec 6 OSTRACIIFORM LOCOMOTION Ostraciiform locomotion is restricted to those kinds of shes with bodies that are incapable of lateral exure of any kind All propulsion comes from wagging the tail rather than by passing a wave of musculature contraction down the length of the body Ostraciiform swimmers vary greatly in body shape They are usually not streamlined and tend to be slow swimmers Not surprisingly they tend to OSquot ACHFORM be shes with bodies encased in armor for example the box shes family Ostraciidae But also included here are the distantly related electric rays Torpedinidae 19998 o N Swimming by electric ray Torpedo nobiliana approximating the ostraciiform mode Length about 150 cm Cinephoto intervals 05 sec 7 SWIMMING BY MEANS OF PAIRED FINS OR UNPAIRED MEDIAN FINS There are a wide variety of relatively unrelated shes that often swim without the use of body and quot quot tail musculature at all Instead they propel m themselves by passing waves of movement down their elongate dorsal andor anal fins This mode AMIIFOR M of swimming is sometimes called Tetraodontiform locomotion Typical among these are the bow n Amia calva trigger shes Balistidae le shes quotquot mmmmm Monacanthidae puffers Tetraodontidae and GYMNOTIFORM diverse kinds of shes that are capable of producing electric elds TETRAODONTIFORM Other shes propel themselves by rapid undulation of the O pectoral fins called Rajiform or Labriform locomotion g for example the rays Batiomorpha sticklebacks Gastero steidae and the wrasses Labridae LABRIFORM I Qg A 4 s l a amp Lateral View of rajiform swimming by manta Mobula diabolis Length un knOWn Successive cinephotos at 064 sec intervals offish swimming from left to right are displaced upward Vertical broken line represents a fixed position on background Still others like the seahorses Syngnathidae use all their ns moreorless at the same time dorsal anal and pectoral fins pelvic and caudal ns are absent 8 NONSWIMMING LOCOMOTION We usually think of shes as animals that swim with body and ns moreorless free from the bottom and other kinds of substrate but it s important to remember that many shes spend much or all of their time engaged in locomotory activities that do not involve swimming Examples include jet propulsion water exhaled from the gill chambers eg angler shes order Lophiiformes terrestrial locomotion shes employing anguilliform motion over land eg airbreathing cat shes Clariidae the climbing perch Anabantidae and mudskippers Periophthalmidae walking on the bottom and burrowing eg benthic angler shes Antennariidae Chaunaciidae and Ogcocephalidae eels Anguilliformes and mudminnows Umbridae and jumping eg the basking shark Cetorhinus tarpon and their allies Elopidae gliding eg the ying shes Exocoetidae and ying eg the freshwater hatchet shes Gasteropelecidae the freshwater butter y sh Pantodon buchholzi PEIORAL LABRIFO M RAJIFORM cl H M lt GYMNOTIFORM a quot lt I 3 BALIsnFonM TETRAODONHFORM a AMHFORM I wMW OSYRACIIFORM u lt igt I a D lt L a F E IHUNNIFORM l c o n CARANGIFORM MWWWW l 39llllllllllllllliuulllll39 SUSCARAINGIFORM I c 39III I 39 H ANGUILLIFORM l l A mmmmm a TRUNK LTNDULATION OSCILLATIOVN Modes of39forward swimming in fish arranged aIOng the vertical axis according to the propulsive contributions of body and ns indicated by density of shading and along the horizontal axis according to a scale running from serpentine undulation more than one wavelength present to oscillation a rigid wigwag or fanlike motion Species illustrated are A Anguilla anguilla B Squalus acanthias C Gadus morhua D Salmo gairdneri E Caranx hippos F Clupea harengus C Isurus glaucus H Thunnus albacares I Ostracion tuberculatum J Amia calva K Gymnotus carapo L Balistes capriscus M Lagocephalus laevigatus N Raja undulata O Diodon holocanthus and P Cymatogaster aggregata 9 DIRECTIONAL CONTROL AND THE FUNCTION OF FINS The ns of shes function primarily to control the direction of forward progress Fins seem to be just about the shiest of sh characteristics No sh is completely without ns but there are numerous examples of taxa in which pectoral andor pelvic ns are absent mostly eel or eel like burrowing forms and in which dorsal and anal ns are greatly reduced to the extent that they are essentially functionless Examples of nearly nless shes include hag shes Myxinidae and lampreys Petromyzontidae a few groups of true eels eg spaghetti eels Moringuidae some morays Muraenidae and some swamp eels family Synbranchidae Family Myxinidae hagfishes Family Moringuidae spaghetti eels Although they often serve other functions sh ns are basically concerned with locomotion and as such they play a number of roles I They often aid in forward movement 2 They guide the course of forward movement 3 They provide a system of brakes andor a mechanism for backing up Among bony shes increasing functional efficiency and specialization of the individual ns seem to have been one of the major evolutionary themes As long as a sh moves only by undulation eg an eel the various requirements of locomotion are distributed along the entire length of the body and there is little or no differentiation of the ns But with the trend toward emphasis on caudal locomotion and the evolution of a shorter deeper more rigid body the various ns become specialized for particular functions With caudal locomotion this is related to the fact that the locomotory functions of ns work best or are most ef ciently carried out when the ns are placed over de nite regions of the body In analyzing directional control in a welldeveloped subcarangiform or carangiform swimmer we can divide the sh body into ve moreorless distinct regions Locomotory Anterior Dorsal Stabilizers Posterior organ rudders keel rudders An 1 anterior zone of rudders and a 2 posterior zone of rudders which function to change or control the direction of movement and which are best placed at the greatest possible distance from the center of gravity A 3 zone of keels a n that functions as a keel works best if placed at the level of the center of gravity A 4 zone of stabilizers ns designed to stabilize the course of forward movement must be placed behind the center of gravity A locomotory organ or 5 zone of thrust best placed well behind the center of gravity preferably at the posteriormost end 10 THE UNPAIRED FINS DORSAL ANAL AND CAUDAL The dorsal and anal ns are the least specialized of ns Although they may at times and in various taxa aid in forward motion or in braking their function in most bony shes is to act as stabilizers As stabilizers they control movement in the horizontal axis a kind of movement called yawing They also serve to control movement in the vertical axis a kind of movement k i called rolling The forward extent of the anal n is limited in most bony L shes by the ventral position of the visceral organs and vent The dorsal n however has no such limitations and in most bony shes especially more derived taxa the dorsal or part of it comes to lie over the center of gravity that is in a more anterior position where it functions as a J dorsal keel As such it helps to prevent rolling particularly important when turning The anal n functions in a similar way but because of its position on the body that is moreor less restricted posteriorly it is not as ef cient and serves to act more as a stabilizer of forward motion Stiffening of the dorsal and anal ns particularly at their anterior margins through the acquisition of spines greatly enhances their ef ciency as keels and stabilizers The caudal n functions primarily as an organ of thrust or propulsion and as such it takes on a Wide variety of shapes An elaborate terminology has been created to describe this variation see diagrams on page 13 11 THE PAIRED FINS PECTORALS AND PELVIC The paired ns have undergone considerable modi cation throughout the evolutionary history of bony shes see pages 14 and 15 They function chie y in the vertical or transverse axis to control movement called pitching and to Q moreorless control the horizontal direction of the body 39 during forward motion In most primitive fastswimming bony shes the pectoral ns are inserted horizontally on the body and located low on the belly In this position they serve as rudders to control the vertical position during forward motion 12 Caudal fin shapes and structures epichovdal ofd MODIFIED DIPHYCERCAL v gt HETEROCERCAL 39 HYPOCERCAL ISOCERCAL urostylo lEPISOSTEUS AND AMIA MODIFIED HOMO ER A Qvoxfylo POLYPTERUS D COD it 9 FIERASPIS GEPHYRQQERCAL MODIFIED HOMOQERQAL Examples of fish with modified pectoral fins A Ventral view of sisorid catfish Glyptothorax B freshwater butterflyfish Pantadon c hatchetfish Gastropelecus D threadfin Polynemi dae E gurnard Triglidae F ventral view of batfish Ogcocephalidae with armlike pectorals well behind pelvics G flying fish Exocoetldae Examples of pelvic fin placement pelvic fins circled A Abdominal sturgeon Acipenseridae B subabdominal sand roller Percopsidae C thoracic bass Moronidae D jugular pollock Gadidae Based on Jordan and Evermann 1900 Pelvic fins modified as sucking devices E Clingfish Gobiesocidae F goby Gobiidae G snailfish Liparidae During the course of evolution the pectorals have moved up on the side of the body to a position along or above the longitudinal axis of the sh At the same time the bases of these ns took on a more vertical position along the side of the body These changes in position provided new capabilities 1 An ability to maintain a stationary position in the water by fanning the pectorals 2 An ability to clap the extended pectorals sharply backward against the sides of the body to accelerate rapidly In more advanced bony shes the pelvic fins have also changed position They have moved forward to a position essentially below the pectoral ns Situated as such any tendency to force the head of the sh downward by extending the pectoral ns can be counteracted by extending the pelvics at the same time Both pairs of ns still act as rudders but now the two are able to work together to precisely control the direction of movement in the vertical plane In addition these two pairs of ns can be extended all at the same time in such a way as to form a system of brakes Fishes with this capability can stop almost instantaneously a great advantage when and where a high level of maneuverability is required The pectoral ns however remain the essential component in this system Often the pelvic ns become modi ed to take on other functions or are lost altogether In this sense the pelvics are the least important of sh ns It is important to emphasize that none of these evolutionary changes in fin placement and function would have been possible without the evolution of a swimbladder BIOLOGY OF FISHES FISH 311 BIODIVERSITY VI SARCOPTERYGIAN FISHES TETRAPOD ANCESTRY AND THE STORY OF LA T IMERIA General topics 1 2 3 4 5 Where are we Sarcopterygii the lobe nned shes Crossopterygians the coelacanths Dipnoi the lung shes The ancestors of tetrapods Origin of tetrapods inferred from their mitochondrial DNA af liation to lung shes Hans Fricke and the story of Latimeria 1 WHERE ARE WE In our review of sh biodiversity we39ve already covered the vast majority of living shes All we have left are the eight extant species of sarcopterygians highly interesting not for their 39 success in terms of number of species produced through time but for the fact that somewhere among their rich fossil history was an animal that gave rise to the rst amphibians thus leading the way to the origin of tetrapods as a whole EVOLUTION OF THE MAJOR GROUPS OF LIVING FISHES CHONDRICHTHYES Sharks Rays SARCO PTERYG I I Chimaeras Lobefinned shes CEPHALASPIDOMORPHI Lampreys MYXINI ACTINOPTERYGII Hagfishes Bony or rayfinned shes 2 SARCOPTERYGII THE LOBEFINNED FISHES Sarcopterygian shes differ most strikingly from actinopterygians as well as from other shes in the structure of their scales number of dorsal ns and n supports Probably the most important distinction especially for differentiating fossil sarcopterygians is the cosmoid scale consisting of a layer of cosmine overlain by a thin hard layer of enamel an inner layer of spongy or vascular bone and a deep layer of lamellar bone Dentine is present as well closely associated with the cosmine layer These cosmoid scales were present in nearly all of the earliest ie extinct sarcopterygians but they have been considerably modified through time for example cosmine is completely lost in modern lungfishes and is absent as well in the scales of Latimeria pore enameloid layer layer Megalz39chthys hibbertz39 Diagram to show structure of exoskelcton Primitively all sarcopterygians had two dorsal fins a feature that clearly distinguishes them from early actinopterygian shes which as you39ll recall had only a single dorsal fin posterior dorsal fin V fanterior dorsal fin epichordal lobe basal scute j 05 hypochordal lobe pelvrc fun anal fin main lateral line pectoral fin Osteolepis macrolepidotus Restoration in lateral View U But probably the most obvious and most signi cant distinguishing feature of sarcopterygians are the lobed fins Instead of n rays supported by a series of elongate more or less parallel bones the ns are connected to the girdles pectoral and pelvic by a continuous chain of bones that look similar to tetrapod limbs In the diagram below A and B represent the pectoral n of extinct sharks C and D represent that of a living lungfish and a codfish respectively SSW l or Mimic Il t o quot83 lh39u 39 M W STRUCTURE OF PECTORAL FINS A Cladoselache leri After Dean B Xenacanthus decheni After Fritsch C Australian Lung sh Neoceratodus forum D Cod Gadus morhua Not only were the pectoral and pelvic ns of these primitive sarcopterygians mounted on lobes the same condition characterized the support for the dorsal and anal ns as shown here in this diagram of E usthenopteron Vertebral column and ns of Eusfhenopieron These two gures show the quotlobedquot pectoral and pelvic ns of the Australian lungfish genus Neoceratodus upper and the living coelacanth genus Latimeria lower ULNA o RADIUS HUMERUS I w PREAXIAL RADIALS IN POSIAXIALQTION ANOCLEIIHIUM SCAl ULOCOlACOID39 BALL AND SOCKET JOINTS POSTAXIAL RADIALS IN PREAXIAL POSITION TIBIA POSTAXIAL RADIALS a aay 0 amp y a9 B g g quot Q Q12 gt wlh k FEALUR I b IIULA PREAXIAL RADIALS Neoceratodusforsteri Kre t left pectoral A and pelvic B n endoskeletons in positions of rest against body AMNH 36982 18 cm total length PREAXIAL SIDE IN POSTAXIAL POSITION POSTAXIAL SIDE IN PREAXIAL POSITION SINGLE BALL AND SOCKET JOINT 1 SHOULDER GIRDLE POSTAXIAL RADIALS PELVIC GIRDLE Latimeria chalumnae Smith left pectoral above and pelvic below n endoskeletons of unborn juvenile of 34 cm total length AMNH 32949 shown in positions of rest against body Sarcopterygian shes are divided into two primary groups 1 Crossopterygians the coelacanths 2 Dipnoi the lungfishes 3 CROSSOPTERYGIANS THE COELACANTHS The coelacanths rst appeared during the Age of Fishes that is the Devonian in deposits laid down about 380 MYBP They ourished during the remainder of the Paleozoic but disappear from the fossil record during the Cretaceous about 100 MYBP This total absence of any evidence of their existence for the last 100 million years led everyone to believe that they had became extinct So it was a big surprise that a living specimen of a coelacanth was captured off South Africa in 1938 Study of this specimen and others that followed revealed the surprising fact that very little structural change had occurred in all that time The single known living species of coelacanth which came to be known as Latimeria was structurally not much different from Paleozoic and Mesozoic crossopterygians that had been known as fossils for more than a century In addition to having lobbed ns most coelacanths are characterized by having the following combination of features 1 A large tri lobbed tail called diphycercal in which the vertebral column is not turned up in the typical heterocercal or homocercal mode but remains straight forming a central lobe anked above and below by dorsal and ventral lobes y gqu5 we 039 39 4 Latimeria 2 A division of the cranium to form anterior and posterior units that articulate with one another and which are part of a specialized feeding mechanism an intracranial joint that provides for cranial kinesis a Adductor Ot39lCFJl Levazfgiiajricus 39 Otic hyomandibularis OCClplta P Ethmotd capsule c Otico occipital Coraco mandibularis muscle Subcephalic muscle Ethmoid Sternohyoideus Urohyal bone Levator arcus VII palatini b Axial JugUlar musculature V51 V11 CRANIAL KINESIS OF COELACANTHS 4 Outline of braincase lower jaw and hyomandibular showing subcephalic muscles LPalatoquadrate indicated in dottedzlines b Braincase with palato quadrate and adductor jaw musculature c Relative movement of skull elements during feeding Straight lines indicate changes in orientation of the E L 39 and r 39 1 mr and dotted lines show outline of ethmoid As the jaws are opened the distal end of the hyomandibular swings anteriorly The palatoquadratc acts as a link between this bone and the ethmoid region of the braincase which is lifted as the palato quadrate moves forward The subcephalic muscle lowers the ethmoid and the palate and dermal bones of the snout to which it is attached Adductor mandibulae Spiracular diverticulum In addition to these two characters shared by extinct coelacanths as well as the living Latimeria the following softtissue features are found in Latimeria 3 Lungs represented by a large fat lled sac 4 Bone much reduced the internal skeletal support made largely of cartilage 5 Intestine with a large welldeveloped spiral valve 6 Osmoregulation by retention of urea 4 DIPNOI THE LUNGFISHES Lung shes are poorly represented by modern forms but they have a rich fossil history that goes back to the Devonian about 380 MYBP Evolutionary trends within lung shes are characterized by gradual reduction the earliest members of the group had heavy bony skeletons a large heterocercal or diphycercal tail and a heavy armor of thick cosmoid scales As they evolved there occurred a dramatic reduction in the amount of bone loss of the outer layers of the scales reduction in the number of skull bones and the loss of distinct ns including the tail dorsal lateralline anterior dorsal fin main lateralline posterior dorsal n denhmm 39 epichordal fin 4quot In Q9quotquot 0 00quot o39ot39 Wk gfo 39 avor 0 00 y x mwsw xx c ooooo o a WWW pleural le 10mm Conchopoma gadiforme Modern lungfishes are characterized by having 1 Welldeveloped airbreathing lungs 2 A largely cartilaginous skeleton 3 Internal nostrils 4 Large platelike teeth modi ed for crushing 5 A spiral valve in the intestine From a once large and diverse group we now have only six species placed in three families and three genera all considered to be highly divergent survivors of ancient Devonian stock Family Protopteridae African lung shes a single genus Protopterus with four species Family Lepidosirenidae South American lungfish a single species Lepz39dosiren paradoxa Family Ceratodontidae Australian lungfish a single species Neoceratodusforsteri LIVING LUNGFISHES AND THEIR GEOGRAPHIC DISTRIBUTION A The African lungfish Protopz erus aethiopicus letter A on page 9 B The South American lung sh Lepidosiren paradoxa letter B on page 9 C The Australian lungfish Neoceraz odus forsterz39 letter C on page 9 On the map the black area marked A represents the distribution of the four species of the genus Protopterus that marked B the distribution of Lepidosiren and that marked C the distribution of Neoceratodus If shown to scale the area marked C would be little more than a pin prick 5 THE ANCESTORS OF TETRAPODS One of these two major groups of sarcopterygians either the coelacanths or the lung shes was responsible for giving rise to tetrapods The question is which one In 1839 in a paper published by the famous British paleontologist Sir Richard Owen lungfishes were declared to be fishes up until that time they had always been thought of as amphibians and at the same time proclaimed to be ancestral to tetrapods Owen39s hypothesis was well accepted at the time and became the prevailing belief until the turn of the century when Edward Drinker Cope the wellknown American ichthyologist and paleontologist proposed instead that crossopterygians must be the sister group of tetrapods Nearly everyone swung over to this view COMPETING VIEWS OF TETRAPOD ORIGIN Actinopterygii Coelacanths LungfiShes TetraPOds Actinopterygii Lungfishes Coelacanths Tetrapods The Owen Hypothesis The Cope Hypothesis In 1981 Donn E Rosen of the American Museum of Natural History revived the old 19th century idea that lung shes gave rise to tetrapods What is the evidence to support this notion 1 Internal nostrils the internal nostrils of lungfishes are identical to those of Devonian amphibians as well as those of modern salamanders 2 Tetrapodlike limbs primitve lung shes have two primary joints in each paired appendage just like those of tetrapods 3 Tetrapodlike locomotion the locomotion of living lungfishes is like that of tetrapods In addition to these three characters Rosen listed another 17 features shared between lung shes and primitive tetrapods declaring that this body of evidence supports a sister group relationship that is irrefutable But as you might expect not everyone is convinced Many scientists want to stick to the Cope hypothesis that argues that a Latimerialike ancestor was responsible for the rise of tetrapods They argue that in many ways crossopterygians provide a link between shes and the earliest amphibians a group called the Labyrinthodontia Labyrinthodont amphibians A chtbyostega the earliest known tetrapod from the Devonian of Greenland a member of the Ichthyostegalia B Eryops a typical member of the Temnospondyli C Metoposaurus an advanced and completely aquatic temnospondyl D Dz plovertebron an early member of the Anthracosauria The labyrinthodonts were a varied group of primitive amphibians many of which were large and more like reptiles than the small and degenerate modern amphibians Recent papers list about a dozen characters that support a coelacanthlabyrinthodont linkage I39ll list just three 1 The paired ns of certain extinct crossopterygians especially those of the genus Eusthenapteron are more like tetrapod limbs than are those of lung shes Scapulocoracoid Cleithmm Humerus lip i m an 39 Kw MM Postaxial Radius Ulna l M l process 39 I r M Intermedium Overlap centr le Preaxial Preaxial radial 1 area for W 31 radial 2 Lepidotrichia clavicle radial 3 b Pelvic girdle Postaxial lntermedium Femur process Fibulare Q i1 jig1 Scale covering 7604 g quot 179L preaxial edge x I Orrin V Tibia g 1 Preaxial radial 1 4 V 3 Preaxial radial 2 I pidotrichia 39 391 Preaxial radial 3 ENDOSKELETON OF PAIRED FlNS OF EUSTHEN OPTERON a Pectoral girdle and n b Pelvic girdle and n 2 Most of the bones of crossopterygians particularly those of the cranium can be homologized element for element with those of Labyrinthodonts 3 Crossopterygians have a specialized tooth structure in which the outer layer of enamel is highly folded this complex folding which forms deep grooves on the outside of each tooth is also a primary character of Labyrinthodont amphibians It is in fact the feature for which they are named labyrinth complex folding dont tooth o o e of attachment dentine Eusthenopteronfoordi Section of a tooth The latest chapter in the continuing saga of tetrapod origin comes from systematic studies of living sarcopterygians and various tetrapods using molecular characters In a paper published in 1995 by Axel Meyer evidence from a comparative analysis of mitochondrial DNA supports a lung sh ancestry but the jury is still out For a full description of this work see the following pages Molecular evidence on the origin of tetrapods and the relationships he origin of land ver tebrates among the major transitions in the history of organismal diversity is a question of importance and con tention The origin of tetrapods and the identification of their living sistergroup are two separate issues but an answer to the latter question could rule out some historical scen arios of the origin of land ver tebrateszvli Although extinct groups of lobefinned fish are likely to be more closely related to tetrapods than to any living piscine relative reviewed in Refs 14 the identifi cation of the living sistergroup of tetrapods can make an important contribution to this larger issue nonetheless Molecular phylogen etic approaches can aid the more timehonored ones like comparative morphology and paleontology in achieving this goal Despite much debate and gen erations of investigators no con sensus on the identity of the closest living relative of tetrapods has yet been reached Some workers con sidered land vertebrates to be related to actinistians ie coela canths lungfish actinopterygians rayfinned fish or lungfish and coelacanth equally reviewed in Ref 5 Even a diphyletic origin of of the coelacanth Axel Meyer Coelacanths were believed to have gone extinct more than 80 million years ago until the sensational rediscovery of one surviving member of this lineage Latlmerla chalumnae In 1938 Since then paleontologists and comparative morphologlsts have argued whether coelacanths or lung sh two groups of lobefinned sh are the living sistergroup of the third extant lineage the tetrapods Recent molecular phylogenetic data on this debate tend to favor the hypothesis that lungfish are the closest relatives of land vertebrates Somewhat surprisingly the strongest molecular support for this hypothesis stems from mitochondrial rather than nuclear DNA sequences despite the expectation that the more slowly evolving nuclear genes should be more appropriate in addressing a phylogenetic issue involving taxonomic groups that diverged around 400 million years ago This molecular estimate might serve as a framework to test paleontological phylogenies and hypotheses about morphological and physiological innovations and preadaptatlons that allowed Devonian lobefinned fish to colonize land Axel Meyer is at the Dept of Ecology and Evolution and Program in Genetics State University of New York Stony Brook NY 117945245 USA texts The suggestion that the coelacanth and cartilaginous fish are most closely related which was largely based on similarities of their pituitary glands and com mon mode of osmoregulation has been soundly dismissed and will not be considered further reviewed in Ref 5 The monophyly of tetrapods the coelacanth and lungfish and the legitimacy of the outgroup position of the monophyletic Actin opterygii Box 1 for this question is widely accepted There is no de bate that lungfish Fig l hypoth esis 1a or the coelacanth Fig l hypothesis lb or both equally Fig l hypothesis 1c are more closely related to tetrapods than to actinopterygian fish leaving three alternatives to be tested for the relationships among extant lineages of lobe finned fish Fig 1 Support for each of the three hypotheses can be found based on cladistic approaches using neontological and paleontological phenotypic characters but there is no strong consensus opinion for any one of these hypotheses reviewed in Ref 5 Only if all four groups of bony fish are included in molecular phylo genetic studies will they have the tetrapods has been proposedquot with porolepiformi Box 1 fish being the sistergroup of urodels and osteolepiformi fish the sistergroup to anurans and all other land ver tebrates in a controversial paper reviewing paleontological and morphological data that included the extinct groups of lobefinned fish Rosen et 017 considered lungfish to be the sistergroup to tetrapods The vast literature on the ancestry of tetrapods from fishlike ancestors based on morphological and paleontological data has been reviewed elsewhere1v5lt79 here i will focus on biochemical data sets Lungfish were initially believed to be amphibians and their relationship to tetrapods has been debated for more than 150 years for review see Refs 78 Fig 1 After the sensational discovery of the living fossil Latimeria chal umnae reviewed in Ref 9 the last known survian species of another lineage of lobefinned fish the coelacanth rather than the lungfish was generally thought to be the missing link between aquatic and terrestrial vertebrates Fig i This is still the prevailing opinion in most general biology TREE vol 10 no 3 March I995 potential to address the question of the relationships among the extant lobefinned fish lineages Fig l ideally in such studies as many species as possible should be rep resented for each of the lineages and thousands could theoretically be included on the tetrapod and the actin opteryian branches However there are only three genera of lungfish and one coelacanth species alive and available for molecular phylogenetic work Several studies that aim to add to the understanding of the relationships among the lobefinned fish fall short because either the coelacanth or the lungfish lineage are not included These studies typi cally only reaffirm the wellestablished sistergroup relation ship of either the lungfish or the coelacanth to the tetrapods Fig 2a Fig 3a During the past five years various forms of biochemical data have been collected with the explicit goal of testing alternative hypotheses on the molecular evolutionary re lationships among lobefinned fish This review aims to sum marize the current information on this issue Knowledge of 1995 Elsevier Science Ltd 01696347950950 REVIEWS 111 FISHBIOL 31 1 Winter 2008 Lab 12 Reproduction Reproductive System Dog sh Dissection Open the gut cavity of your dog sh without damaging any internal organs ie make shallow cuts Identify the following structures of the reproductive system of the dog sh see gure 1 ovaries oviducts uterus cloaca embryos for females 2 testes vas deferens seminal vesicle sperm sac for males Be sure to examine both sexes 1 What reproductive mode do these sh use How are the eggs fertilized Some of these female dog sh may be pregnant so you might nd several embryos Describe the orientation and appearance of the embryos Obtain one for you and your partner and dissect it take it from the jar of embryos if there aren t any from today s specimens Find the following structures in the dog sh see g 2 heart liver yolk sac stalk stomach pancreas spleen intestine kidney colon 2 Is the mode of reproduction used by the dog sh generally considered to be primitive Compare your observations of dog sh internal anatomy with your notes and drawings on the internal anatomy of teleosts Preserved Specimens Find examples of male intromittent organs among elasmobranches chimaeriforms and cyprinodontiforms 3 What external feature do male holocephalans have besides their intromittent organs that allows you to distinguish their sex Locate the pregnant female surfperch Embiotocidae Compare what you see to the dog sh fin region of the male surfperch This is another example of an intromittent organ 4 What are some advantages of internal fertilization and Viviparity Considering that most sh are oviparous you should know the advantagesdisadvantages of this mode of reproduction Also you should be able to explain how eggs of oviparous shes are fertilized 5 As a general trend how is fecundity related to body size Examine specimens from the families Labridae Scaridae and Serranidae These families include species showing synchronous and sequential hermaphrodites although you won t be able to ascertain sex based on external examination Explain both types of sex reversal protogyny and protandry Look at the male sockeye salmon spawner and describe its appearance Why do these sh males take on this appearance during spawning season rrSIPHON SAL 1 C1 OAK AL APERTURE URINARY PAHU A URINARY PAPILIA CLOACAL APERIURER mwc nN ABDOMINAL FOREquot PELVIC FIN SPERMHIE SULCUS DSHUM m 4me GAME uwouu 7 77777 M AA 7 ovmurl AA mmu Hruuu Mzsomum u 1 A 7 quot 2 sum mm AwMAvURui crown avm m snvmum 7 AI A 2 777mm 39 0W 7 x um i r gt mummmmm Awn A I w mmumsm 7 mum of slomcu u A r 7 ounwi of AM mum m um Dunn m Hle Aivmo39s mun a 0mm of 3mm H ovmucl nmv 7 A A iMisoluumw AM u Dmxms as 77 7 39 39 quotquot mm 7 w mmm ImamEu HUM r 777 xmmv imam wuH memo AV mom uwmxv nun a v 5mm vwni ab 7 um nwmm A v 5mm w rn Ni r swmmskt a m nu mmwn uuMAi A m 7 7 490mm FORE m4 9 nghl mane duplnrcd mum e my lungtmlul mum umml m F 303 7 equot oba quot 2 9 External ow sac com recm gfar d GESTATIOV or 39HE Do after staw 3 can hx 3 successva Sta Lz e in cemmmw i 9 17 Prmgopods coguhwry organ of he an mum Ky andEhrcnhmm Capuhmry organs of various shes no to same scale 1 and 2 Ma Gam twin and iLs gonopodiurn from Lmdberg1934l and 4 m anomrulvj ulnaimd iu gonopodium from Kulkami 940 S and 6 male afA39mIdhm amn39mla Vilj a Man and is priapium rmm Berg 1935 5mm mmuxvmsm maeta lHyrimagus B Haralchxhys Cl L lmumllus


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