amer. zool.-1991-wainwright-680-93(1)

8/13/2019 Amer. Zool.-1991-WAINWRIGHT-680-93(1)

1/14

AMER. ZOOL., 31:680-693 (1991)

Ecomorphology: Experimental Functional AnatomyforEcological ProblemsPETER C. WAINWRIGHT

Department of Biological Sciences, Florida State University Tallahassee, Florida 32306SYNOPSIS. It is generally believed that the functional design of an organism relates to itsecology, yet this ecomorphological paradigm has historically suffered from the lack of arigorous framework for its implementation. I present a methodology for experimentallyexploring the ecological consequences of variation in morphology. The central idea is thatmorphology influences ecologyby limiting the ability of the individual to perform key tasksin its daily life. In this scheme the effect of morphological variation on behavioral perfor-manceis first tested in laboratory experiments. As the behavioral capability of an individualdefines the range of ecological resources that i t can potentially make use of (the potentialniche),the second step inthe scheme involves comparing the potential niche of an individualto actual patterns of resource use (the realizedniche).This permits a quantitative assessmentof the significance of an organism s maximal capabilities in determining actual patterns ofresourceuse.An exampleis presented from work on the feeding biology of fishesn the family Labridae(wrasses and parrotfishes). Most labrids feed by crushing shelled prey in their powerfulpharyngeal jaws. This example exploresthe dietary consequences of variation in crushingstrength amongand within species. Crushing strength was estimated from biomechanicalanalyses of the crushing apparatus in severalspecies,and these predictions of relative strengthwere tested in laboratory feeding experiments with hard-shelledprey. Morphology accuratelypredicted relative crushing ability, and the final sectionof the study explored the effect ofvariation in crushing ability on diet. Within each of three species crushing strength appearsto underliea major ontogentic dietary switch from soft-bodied prey to a diet dominatedbyhard-shelled prey.In each species this switch occurred a t about the same crushing strength,around 5 Newtons (N), in spite of the fact that this crushing strength is achieved by thethree speciesat different body sizes. Diet breadth increases during ontogeny in each species,untilacrushing strength of5Nisachieved, when diet breadth begins to decline. The strongestfishes specialized almost entirely on molluscs and sea urchins. Thus, these labrids takeadvantage of ontogenetic and interspecific differences in crushing strength by including harderand harder preyin their diet, and ultimately specializing on hard prey types. The specializedorganization of the labrid pharyngeal jaws can be viewed as a key innovation that haspermitted this lineageof fisheso invade the mollusc eating niche, a relatively empty trophicniche within the highly speciose and diverse communities of coral reef fishes.

INTRODUCTION its converse, the influence of functionalEcomorphology is the study of the rela- morphology on the ecology of an organism,tionship between the functional design of I n t h e former, the environment is recog-organismsand the environment. It shares a n i z e d as a central forcein shaping functionalconceptual framework with several other systems during their ontogeny and evolu-disciplines within organismal biology, such t l 0 n - M o s t evolutionary mechanismsas physiological ecology, biophysical ecol- emphasize the environmentasa major causeogy,and ecomechanics, and no distinction o f organismal design (see for exampleis implied here other thanan emphasis on James, 1991),and the majority of ecomor-functional morphology. Within ecomorphological research has focused on adaptivephologytwo primary axes of research have explanations for observed design patternsemerged that concentrate on either the effect (Hespenheide, 1973; Leisler, 1980; Barel,of the environmenton functional design or 1 9 8 3 ;Alexander, 1988). Recent advanceshave brought to the forefront the role ofphylogenetic historyas an alternate expla-nation for design (Lauder, 1981, 1990;'F romtheSymposiumonExperimental Approaches Ridley 1983 Huey 1987)and integrativetotheAnalysis of FormandFunctionpresented a t the annrnarhes that a w the relative rnntriCentennial Meetingof the American Societyof Zool- approac nes Uiat assess therelative con tnogists, 27--30 December 1989,at Boston, Massachu- button of phylogeny an d adaptation aresetts. emerging (Cheverud et ah, 1985; Huey and680

atUniversidadNacionalAutnomadeMxicoonFebruary13,2014

h

ttp://icb.oxfordjournals.org/

Downloadedfrom
http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/http://icb.oxfordjournals.org/


2/14


3/14

68 2 PETER C. WAINWRIGHT

FIG. 1. A three-dim ension al visualiza tion of the scaling of pharyngeal jaw gape and crushing strength in theCaribbean hogfish, Lachnolaimus maximus. The range of prey sizes and prey hardne ss that fish are able tohandle are shown for individuals of 20, 350, and 2,000 g. All axes are log, 0 scales. During ontogeny crushingstrength and gape increase, causing an increase in the range of prey on which hogfish are able to feed. Data arefrom Wainwright (1987).

reso urce use by organism s (Schoener, 1986).Much ecological research is devoted toassessing th e relative significance of variousfactors in shaping resource use patterns,whether the resource be food (Osenberg andMittelbach, 1989), space (Sale, 1980), time(M unz and M cFarland, 1973), or reproduc-tive opportunities (Hoffman et al, 1985).In the discussion that follows I focus on thefood resource for convenience, though thestatements apply generally to any ecologicalresource.Among the many factors that influencepat tern s of prey use, two may be viewed asfundamental: (1) prey availability, and (2)the ability of the predator to utilize eachprey ty pe. Th us, the types of prey and theirrelative abundance define the food resourcefor a predator, and the predator's ability tolocate, captur e, and handle the vario us preytypes constrains the range of prey that can

potentially make u p the diet of the pred ator.Other factors tha t can shape pattern s of preyuse, such as competition, energetic consid-erations, and the threat of predation, mayfurther restrict the actual range of prey thatare used, but these factors must exert theireffect within the fundam ental range of preydeterm ined by th e feeding capabilities of thepredator {e.g. Holling, 1959; Gra nt, 1986;Osenberg and Mittelbach, 1989).To illustrate som e of these ideas an exam -ple is presented in F igure 1 based on p re-vious work with the Caribbean hogfish,Lachnolaimus maximus, a coral reef pred-ator that feeds almost entirely on molluscswhich it crushes in its powerful pharyngealjaws (W ainwright, 1987).Two factors deter-mine the upper size limit of mollusc preythat hogfish can eat. The prey first must besmall enough to fit between the jaws of thefish, and once positioned between the crush-

atUniversidadNa

cionalAutnomadeMxicoonFebruary13,2014

h


Downloadedfrom


4/14

EXPERIMENTAL ECOMORPHOLOGY 68 312

9

0 6

0 3

.Y

22 Z4 26 28 3fl 32 a 4 3BLog BODY MA SS fl)

FIG. 2. Log,0-log10 plot of hogfish {Lachnolaimusmaximus) body mass against the shell diameter of thegastropod prey, Centhium litteratum. The points onthe graph indicate the shell size of all C. litteratumfound in the stomach contents of 59 hogfish collectedin Belize. The dashed line indicates the relationshipbetween maximum pharyngeal jaw gape and hogfishbody m ass. The solid line indicates the max imum sizeC. litteratum shell that hogfish are strong enough tocrush. This relationship is derived from morp holog i-cally based estimates of hogfish crushing strength anda determination of the force required to crush shells ofdifferent sizes. The relation ship b etween shell size andforce at failure was then used to transform estim atesof maximal crushing strength offish into expected shellsizes. No snails are eaten that lie near the limits ofpharyngeal jaw gape, indicating that crushing strengthactively constrains C. litteratum predation by hogfishin this natural population.

ing jaws,thefishmustbe ableto exert enoughcrushing force to crack the mollusc shell.Jaw gape and crushing strength increaseduring ontogeny; Figure 1 illustrates th erange of prey sizes and shell strengths thatcan be eaten by fish 20, 350, and 2,000 g.As gape and crushing strength increase therange of prey that hogfish can potentiallyeat also increases.But how important are these two limi-tations in actually shaping the diets of hog-fish in natural populations? An analysis ofstomach contents of 59 hogfish collectedalong the Belizean barrier reef in CentralAmerica shows that crushing strength playa central role in determ ining patte rns ofpre-dation on at least one prey species (Fig. 2).Plotted a re the shell sizes of 331 in divid ualsof the most commonly eaten gastropod,

Cerithium litteratum, found in the intes-tines offish ranging in mass from 190 g to3,600 g (since Cerithium shells are presentin hogfish intestines only as fragments, snailsize was determined from the diameter ofopercula, which are generally left intact).This distribution is comp ared w ith the scal-ing of maximum gape (Fig. 2, dashed line)and maximum crushing strength (solid line)as they relate to Cerithium. The plot dem-onstrates that stronger fish eat larger Ceri-thium, in addition to smallersnails,and thatcrushing strength appears to be the factoractively constraining Cerithium predationby fish of all sizes. Hogfish frequently feedon snails at or near their maximal crushingcapabilities. Further, the hardness ofCeri-thium shells issuch that hogfish never appearto encounter their gape limitation whenfeeding on this prey species (Fig. 2). Theseconclusions were further supported in lab-oratory performance experiments designedto determined the size of the largest Ceri-thiumthat hogfish were able to crush (Wain-wright, 1987). The maximum size Ceri-thium that fish were able to crush wasaccurately predicted by estimated crushingstrength.By providing a formal description of theinfluence of functional morphology on pat-terns of resource use the technique sug-gested here permits a rigorous perspectiveon some major concepts in ecomorphology.One such concept is the key innovation, anevolutionary transformation in organismaldesign that causes qualitat ive changes in theperformance gradient of a lineage, and ulti-mately in the range of environmentalresources that can be used. Key inno vation smay underlie the ability of a lineage toinvade new environments or occupy pre-viously empty niches in crowded ecosys-tems (Mayr, 1960; Liem, 1974; Larson etai , 1981). Hyp othesized key innova tionscan be tested first by functional analyseswhich elucidate th e theore tical effect of thestructural innovation on whole-animal per-formance, followed by laboratory perfor-mance experiments which test these predic-tions, and finally by showing the ecologicalconsequences of variation in performance.The historical correlation between the mor-phological innovation and ecological con-sequence must also show precise congru-

atUniversidadNa


h


Downloadedfrom


5/14

684 PETER C. WAINWRIGHTsoc

EP

LE4

-F M

-UPJ

SOCEP

SO C V

LE4LE4

LPJ

FIG.3. Pharyngeal jaw structures of three species of CaribbeanHalichoeres.Most of the superficial bones andmuscles of the head are not shown to permit an unobstructed view of the pharyngeal jaws. A and B are lateraland posterior views ofH.bivittatus,respectively. C and D show lateral views of H.maculipinnaandH. pictus,respectively. Abbreviations: EP, epiotic process; FM, foramen magnum; LE4, fourth levator externus muscle;LP , levator posterior muscle; LPJ, lower pharyngeal jaw composed of fused fifth ceratobranchials; ORB, orbit;SOC,supraoccipital crest; UPJ upper pharyngeal jaw composed of left and right third pharyngobranchials. Scalebar is 5 mm. From Wainwright (1988).ence within the context of a phylogenetichypothesis (Lauder and Liem, 1989), butthe argument for causation ultimately restson our ability to link morphology with ecol-ogy through performance. The concept ofkey innovation has played a major role indiscussions of the evolution of the trophicbiology of labridfishes(Liem,1974;Stiassnyand Jensen, 1987), the subject of the casestudy discussed below.

CASE STUDY: FEEDING BIOLOGY OFCARIBBEAN LABRID FISHES

Coral reefs are well known as ecosystemsthat support a tremendous diversity of life.One of the most speciose and diverse groupof fishes on coral reefs is the Labridae

(wrasses and parrotfishes), a circumtropicalfamily of some 590 known species. Mem-bers of the monophyletic Labroidei (whichincludes the Pomacentridae, Embiotocidae,Cichlidae,and Labridae), labrids possess anovel organizations of the pharyngeal jawapparatus that both characterizes this groupand has often been cited as a key innovationthat may underlie the group s remarkableecological success (Liem, 1974; Liem andGreenwood, 1981; Kaufman and Liem,1982).The crucial functional feature of thelabriod pharyngeal jaw is a direct muscularattachment between the neurocranium andlower pharyngeal jaw (Fig. 3). This is thebasis of a strong pharyngealbite,and under-lies the potential for eating hard prey(Kauf-

atUniversidadNa


h


Downloadedfrom


6/14

EXPERIMENTAL ECOMORPHOLOGY 685man and Liem, 1982; Wainwright, 1987).The generalized perciform condition fromwhich the labroids are thought to haveevolved consists of no direct muscular con-nection between the neurocranium andlower pharyngeal jaw. In these taxa preycrushing involves complex lever arrange-ments and shearing actions of the jaws(Wainw right, 1989). As a group, labrids aretrophically distinct from most other coralreef fishes in exhibiting diets typically d om -inated by hard prey, such as molluscs, echi-noderm s and coral rock, which are crushedin the powerful pharyngeal jaws.

In this study I explored the functionalbasis of prey crushing performance in sev-eral species of Caribbean wrasses in thegenus Halichoeres, with the purpose ofunderstanding the ecological consequencesof variation among and within species inpharyngeal jaw crushing strength. Like otherwrasses, thesefishcrush shelled prey in theirpharyngealjaws.Speciesof Halichoeresfeeddiurnally on a wide variety of primarily ben-thic invertebrates, including gastropod andpelecypod molluscs, ophiuroids, urchins,polychaetes, sipunculans, decapod shrimps,crabs, isopods, amphipods, and copepods.The study fell into three parts. First, thecrushing strength of six species was esti-mated based on a biomechanical analysis ofthe pharyngeal jaws. Second, these predic-tion s of relative crushing strength were teste din laboratory performance experim ents withthree species that differ in expected crushingperformance. Third, the effect of variationin crushing strength on patterns of prey useis explored in these three species.

MorphologyThe pharyngeal jaw apparatus of labridshas been extensively described (Yamaoka,1978; Liem and Sanderson, 1986; Wain-wright, 1987, 1988;Gobalet, 1989) and onlythose aspects central to a discussion of preycrushing are dealt with here. Diagrams ofthe pharyngeal jaws in three species ofCaribbeanHalichoeresare presented in Fig-ure 3. Most superficial bones and musclesare not illustrated to perm it an unobstructedview of the pharyngeal region. The pharyn-geal jaws are formed from modified gill archelements. The massive lower pharyngeal jaw

is composed of fused fifth ceratobranchialsand their associated tooth plates. The upperjaw is composed of left and right third pha-ryngobran chials, each fused with a n enlargedventral tooth plate. The upper jaw bonesarticulate with the ventral surface of theneurocranium through a well developeddiarthrosis. The key to crushing function isthe organization of the paired levator pos-terior muscles, which originate on severalbones of the posterior region of the neuro-cranium and insert on the lateral horns ofthe lower jaw (Fig. 3B). The fourth levatorexternus muscle also originates on the neu-rocranium and fuses with the tendon of thelevator posterior. In m ost species the fourthlevator externus muscle is relatively small,but in others it m ay appro ach th e size of thelevator posterior {e.g. Fig. 3D). Thus, thelower jaw is suspended from t he n eurocra-nium in a muscular sling. When prey arecrushed they are held between the upper a ndlower pharyngeal jaws, and the primarycrushing forces are generated by the twolevator posterior muscles pulling the lowerjaw against the upper jaws (Liem and San-derson, 1986; Wainwright, 1987, 1988).There are no lever arms in this system sothe maximum crushing strength is expectedto be equal to the combined maximumtetanic tension of the left and right levatorposterior muscles.Maximum tetanic tension can be esti-mated by measuring the physiological crosssectional area of a muscle and assuming atypical value of the force producing capa-bility of the muscle tissue per unit of crosssectional area (Powell et al, 1984). Physi-ological cross sectional area is no t the sameas the morphological cross sectiona l area ofthe muscle as it takes into account the ori-entation of muscle fibers as well as thethickness of the muscle. Morphologicallybased estimates of physiological cross sec-tional area were used to estimate maximaltetanic tension for the levator posterior andfourth levator externus muscles in an onto-genetic series of six species of Halichoeres(Fig. 4). A value of 20 N /c m 2 for the forceproducing capability of fish muscle tissueper unit of cross sectional area was takenfrom the literature (Altringham and John-ston, 1982;A ksterftfa/., 1985). Tw o factors

atUniversidadNa


h


Downloadedfrom


7/14

686 PETER C. WAINWRIGHT10 0

10

1

n

.0

.0

.0

1

H. poeyi

H.

H. radiatusH. garnoti / * . .

\SCr H- bivittatus

y^ H. maculipinna

pictus

CARIBBEAN LABRIDS:levator posterior muscle of 25 g fish

45 100 250BODY LENGTH mm)

FIG. 4. Relationship between estimated pharyngealjaw crushing strength and body length for six speciesof Caribbean labrids. Both axes are log,0scales. Sizeranges are bounded by the smallest and largest indi-vidual examined from each species. Crushing strengthestimates are based on morphologicalanalyses. Furtherlaboratory and field investigations were made into thefeeding performance and diet of the three species indi-cated with solid lines. Only dietary data were obtainedfor the three species indicated with dashedlines.FromWainwright (1988).

contributed to extensive interspecific dif-ferences in estimated crushing strength (Fig.4). First, species varied in the mass of thelevator posterior muscle(Fig.3). Second, inall species the levator posterior muscle hada bipinnate structure and the angle of pin-nation formed by muscle fibers inserting onthe central tendon varied from 20 in H.pictus to 37.2 in H. poeyi.By increasing theangle of pinnation of fibers in the levatorposterior muscle (up to a fiber angle of 45)relative crushing strength is increased (Calowand Alexander, 1973). However, a trade-offoccurs in the extensibility of the musclewhich decreases as the angle of pinnationincreases (Alexander, 1971). The extensi-bility of the levator posterior muscle deter-mines maximum pharyngeal jaw gaperesulting in an inverse relationship betweenangle of pinnation of the levator posteriorand pharyngeal jaw gape among Caribbeanlabrids (Fig. 5).Performance

To test these morphologically based pre-dictions of relative crushing strength, sev-

30Oa

r =-0.964

3 4 5 6 7 8 9GAPE mm)

FIG.5. Relationship between the mean angle of pin-nation of muscle fibers of the levator posterior muscleinserting on that muscle s central tendon and pharyn-geal jaw gape in seven species of Caribbean labrids.Each point represents data collected from between 8and 20 individuals per species. Pinnation angles weremeasured on at least 10 muscle fibers per muscle. Inno species was body size found to be correlated withangle of pinnation. Angles of pinnation up to 45 increaserelative force producing capability of this primarycrushingmuscle, but as the angle of pinnation increasesabove zero the extensibility of the muscle is restricted.The extensibility of this muscle directly determinesmaximal pharyngeal jaw gape. See Wainwright (1988)for further details of angle measurements. Species indi-cated from left to right,Lachnolaimus maximns, Hal-ichoerespoeyi, H. garnoti, H. radiatus, H. bivittatus,H. maculipinna, and H. pictus.

eral individuals from three species(H. gar-noti,H.bivittatus,and H. maculipinna)werebrought into the laboratory where perfor-mance experiments were conducted withseveral commonly eaten prey species,including a gastropod and two decapod crabs(Wainwright, 1988). In these experimentsthe largest individual of each prey speciesthat could be consistently crushed and con-sumed was determined for individual fish.The basic expectation was that, when eatinghard-shelled prey, fish with the same esti-mated crushing strength should be able tocrush the same maximum size prey, in spiteof the fact that these threeHalichoeresspe-cies achieve the same crushing strength atvery different body sizes (Fig. 4).These experiments produced strong con-firmation of the morphologically based pre-dictions of relative crushingstrength.Resultsfrom experiments conducted with the gas-tropod Cerithium litteratum are presented

atUniversidadNa


h


Downloadedfrom


8/14

EXPERIMENTAL ECOMORPHOLOGY 687

5 10 15 20 25CRUSHING FORCE POTENTIAL N)

3 0

6 8 10 12 14PHARYNGEAL JAW GAPE m m )

FIG.6. Results of laboratory feeding experiments withthree species ofHalichoeresdesigned to determine thelargest size gastropod, Cerithium litteratum, that eachfish could successfully crush and consume. Maximumshell size is plotted against (A) estimated crushingstrength of fish (ANCOVA comparisons of speciesslopes: P =0.91;ANCOV A for species effect:/>= 0.21)and (B) pharyngeal jaw gape of fishes (ANCOVA forspecies slopes:P = 0.78; ANCOVA for species effect:P


9/14

688 PETER C. WAINWRIGHT

Eo 90

1 10CRUSHING FORCE POTENTIAL N)

110BODY LENGTH mm )

130 150

FIG.7. Mean volume percent of hard prey types (mol-luscs, echinoids, and ophiuroids) found in the stomachcontents of three species of CaribbeanHalichoeres.Eachspeciesisbroken down into 10mm sizeclasses.Percenthard prey plotted against(A)estimated crushing strengthof fishes (ANCOVA comparisons of species slopes:P= 0.31; ANCOVA for species effect:P =0.31) and (B)body length offish (ANCOVA for species slopes:P =0.19; ANCOVA for species effect:P =0.001). = H.maculipinna, = H. garnoti, and = H. bivittatus.from Wainwright (1988).

percent of hard-bodied prey types found inthe diet was calculated for all size classes ofthe three species. In each species there wasa switch during ontogeny from small fishthat eat very little hard prey, to larger fishwhose diets are dominated by hard-shelledprey types (Fig. 7). The switch, however,occurred at different body sizes in each spe-cies.Thus, H. maculipinna, the weakest ofthe three species, switches to hard prey ataround 120 mmS L,while the switch occursbetween 70 and 80 mm in the two strongerspecies (Fig.7B).In contrast, this diet switchoccurs at about the same crushing strengthin each of the three species. At around 3-5Newtons crushing strength all three speciesswitch over to a diet dominated by hardprey (Fig. 7A).To test the prediction that stronger fish

10 20CRUSHING FORCE POTENTIAL N)

30

g 3.0

13PHARYNGEAL JAW GAPE mm )

15

FIG. 8. Diet breadth (Shannon-Wiener index) for sizeclasses of species of Halichoeres plotted against (A)estimated crushing strength offish, and (B) pharyngealjaw gape. Below 5 N crushing strength diet increasesas afunction of crushing strength, above 5N diet breadthdeclines. The strongest fishes specialized on hard preylike molluscs and echinoderms. = H. maculipinna, =H. garnoti,and H. bivittatus.From Wainwright(1988).have broader diets the Shannon-Wienerdiversity index (Shannon, 1949) was cal-culated as a measure of diet breadth. Thetwo stronger species,H. garnotiand H. bi-vittatus, showed similar patterns of dietbreadth scaling with crushing strength andbody size (Fig. 8). During early ontogenydiet breadth increases with crushingstrength, until around 5 N crushing strengthwhen diet breadth begins to decline. Thelargest, strongest members of these two spe-cies exhibited the narrowest diets, special-izing almost entirely on gastropod andpelecypod molluscs. Individuals of H.maculipinna never achieved crushingstrengths above 5 N, and diet breadth inthis species increased continuouslythroughout ontogeny (Fig. 8). Thus, whilethe range of prey that these CaribbeanHal-ichoeresare able to consume increases con-tinuously during ontogeny, diet breadth

atUniversidadNa


h


Downloadedfrom


10/14

EXPERIMENTAL ECOMORPHOLOGY 68 9increases only up to a crushing strength ofabout 5 N. Fish stronger than 5 N becomeincreasingly specialized on hard-shell preytypes.

DISCUSSIONThe major conclusion that is drawn fromthis study is that pharyngeal jaw crushingstrength plays a central role in shaping thediets of Caribbean Halichoeres. Crushingability is a performance characteristic thathas a clear morphological basis in the sizeand architecture of the crushing muscula-ture.From the ecological stand poin t, a large

component of the variation in patterns ofprey use that occur among and within spe-cies can be explained by the correlated dif-ferences in feeding ability, specificallycrushing strength. Within the three speciesstudied the ontogeny of prey use was char-acterized by a transition from a diet of soft-bodied prey to a diet dominated by hardprey in fishes with an estimated crushingstrength above about 5 N. The evidencesupporting the causal nature of this rela-tionship is two-fold: (1) crushing strength,as estimated from morphological analyses,limited the hardness of prey that fish wereable to successfully crush in laboratory per-formance experiments (Fig.6),an d(2) fisheswith the same estimated crushing strengthconsumed similar amounts of hard-bodiedprey, in spite of the fact that the sam e crush-ing ability occurred at very different bodysizes in the th ree species (Figs. 4, 7). Hence,H. garnoti, a relatively powerful species,achieved the feeding ability and diet of theweaker jawed H. maculipinna at a smallerbody size (Fig. 7).Cross-species comparisons of die taryhabits among the threeHalichoeresrevealedpatterns similar to those observed ontoge-netically. Based on estimates of pharyngealjaw crushing strength, individuals of H.maculipinna at 100 mm body length willhave the same constraints on crushing abil-ity that occur in H. garnoti at only 45 mmbody length (Fig. 4). These p redictio ns w eresupported in the feeding experiments (Fig.6), but do these differences between speciesin feeding ability re sult in significant differ-ences in dietary habits? How im portant arethese differences in potential niche for struc-

turing the realized niches? When viewedfrom the standpoint of crushing ability acommon pattern of prey use emerges acrossspecies (Figs. 7, 8). Not only do fish of thesame crushing ability eat about the sameamount of hard prey, but crushing strengthalso appears to underlie the narrowing ofdiet breadth in fish stronger than 5 N (Fig.8). Thus, no other mechanism need beinvoked{e.g. competition or foraging strat-egies) to explain th e major differencesbetween the current diets of these two spe-cies.At any given bod y sizeH. maculipinnasimply cannot successfully handle much ofthe prey eaten byH. garnoti.It is possible,however that past interactions between thesespecies influenced the evolution of pharyn-geal muscle design, contributing to the dif-ferences seen today.

If crushing strength plays such an impor-tant role in co nstraining the feeding biologyof labridfishes,hen whyiscrushing strengthnot maximized in all species? One possiblereason for the interspecific variability thatis observed would be historical constraints.Perhaps the weaker jawed taxa i.e., H.maculipinna an dH. pictus)share an ances-try of weaker jawed predecessors. Unfor-tunately, thi s possibility canno t be criticallyexamined because little is presently knownof the phylogenetic relationships amongHalichoeres species. Alternatively, two ormore strategies may be represented here.There are known trade-offs in the design ofthe primary crushing muscle, the levatorposterior (Fig. 3), that result in a sacrificein pharyngeal jaw gape associated with theincrease force prod uction that isgained fromlarger angles of pinn ation within the m uscle.The two extr emes of this trade-off are foundin the previously discussed hogfish, Lach-nolaimus maximus, an dH alichoeres pictus.The hogfish's diet is made up almost entirelyof molluscs, and th is species has the highestpinnation angle known among Caribbeanlabrids, 45. However, due to the trade-offbetween angle of pinnation and the exten-sibility of the levator posterior muscle ofgape of a 25 g hogfish is only 3.5 m m, com-pared to a gape of 8.3 mm for a H. pictusof the same size. H. pictus feeds almostentirely on midw ater zooplankton and phy-toplankton, including large, soft-bodied

atUniversidadNa


h


Downloadedfrom


11/14

690 PETER C. WAINWRIGHTsiphonopho res that m ake up 24% of the diet(Wainw right, 1988). Unf ortuna tely, nocomp arisons were made in this study ofspe-cies feeding on softer prey, such as poly-chaetes, which may require very differentskills than the crushing strength used indestroying mollusc shells.Labrid success and the mollusccrushing niche

The novel organization of the labroidpharyngeal jaw app aratus has been h ypoth-esized to be causally linked to the remark-able ecological and evolutionary success ofthis group (Idem, 1974). It was suggestedthat the presence of a direct muscularattachment between the neurocranium andthe lower pharyngeal jaw provide s a strongbite and results in tremendous plasticity infeeding function and, therefore, underliesmuch of the ecological diversity seen withinthe group. This proposal has been exten-sively discussed in the literature as a modelcase study in key innovations (L auder, 1981;Kaufman and Liem, 1982; Stiassny andJensen, 1987). Attempts to test the hypo-thetical key innovation have centered onhistorical arguments that look for similardiversity in other lineages possessing labroidcharacteristics of the pharyngeal jaws (seeStiassny and Jensen, 1987, for an excellentreview). These tests have met with limitedsuccess, largely due to the difficulties in find-ing replicated instances of such a majorinnovation in the feeding apparatus.

But what are the ecological consequencesof a strong pharyngeal bites? Are increasesin crushing ability associated with breadthin feeding habits? Though more compara-tive data are needed before generalizationscan be made, the present study speaksdirectly to these issues. Scaling of dietbreadth with crushing ability in the threespecies studied in detail showed that above5 N crushing strength, these species did notcontinue to include a broader and broaderrange of prey in their diet, as was the casefor fish below 5 N (Fig. 8). Instead, dietsbecame increasingly specialized until thestrongest fish fed almost entirely on mol-luscs and sea urchins, all prey with hard,protective shells. One interpretation of thispattern is that hard-shelled prey represent

a very rich and unde r utilized food resourceon coral reefs, and fish that possess the abil-ity to take advantage of this resource canfeed free of competition from those speciesthat are not able to eat molluscs and echi-noderms. Support for this notion is foundin the patte rns of prey use seen in coral reeffishes arou nd the world. In a study of thefeeding habits of 212 species of Caribbeanreef fishes (Ran dall, 1967), only 12 specieswere found to consume large amounts ofmolluscs (>2 0% of the diet by volume). Ofthe 12 species, six were labrids, one was aneagle ray{A etobatis narinari) that averagedover one meter in diameter, one a sparid{Calamus bajonado), one a carangid Tra-chinotusfalcatus), and three were diodontidspiny puffers. Each of these species exhibitsmorphological specializations in the pha-ryngeal jaws o r the oral jaws (Ran dall, 1967;Palm er, 1979; Wainw right, 1987, 1988).Similar patterns are seen in the Hawaiianreef fish community (Hobson, 1974) and inthe central Indo Pacific (Hiatt and Stras-burg, 1960), where reef fish diversity reachesits highest level. Th us, only abou t5%offishspecies on reefs have the ability to overcom ethe defenses of heavily armored molluscs,and among those in the Caribbean that do,all feed almost exclusively on hard prey(Randall, 1967).No causal connection between feedingability and diversity of labrids per se can bedrawn from the present study, but if theresults obtained here prove to be general,crushing ability clearly has major conse-quences for the trophic biology of labrids.Perha ps the labrid pharyngeal jaw c onditionis best viewed as a key innovation in thesense that it underlies the capability to effec-tively crush hard prey, and thus has per-mitted labrids to exist in a relatively unoc-cupied trophic niche. This reduces theopportunities for interspecific competitiveinteractions over prey, thus fulfilling onerequirement of a key innovation in that arela tively unoccupied environment isopened up for those taxa possessing the spe-cialized pharyngeal jaws. The causal con-nection between crushing strength and mol-luscivory was demonstrated here throughcombined biomechanical analyses, behav-ioral performance experiments, and ecolog-

atUniversidadNa


h


Downloadedfrom


12/14

EXPERIMENTAL ECOMORPHOLOGY 691ical investigations. Whether this arrange-ment of the pharyngeal jaws is also causallyrelated to the diversity of labrids and otherlabrids groups is a historical question thathas been notoriously difficult to test (Stiassnyand Jensen, 1987). In contrast, the meth-odology proposed and illustrated here pro-vides a direct means of experimentallyexploring the ecological consequences ofmorphological innovation. Hypotheses ofcausal connections between morphology andecology can be tested by demonstrating theeffect of morphology on performance capa-bilities, and the latter on patterns of eco-logical resource use.

ACKNOWLEDGMENTSI thank Sharon Emerson, George Lauder,Karel Liem, Phil Motta, Steve Norton, andSteve Reilly for several years worth of valu-able conversations concerning ecomor-phology. George Lauder, Steve Reilly, andtwo anonymous reviewers read the manu-script and offered critical comments. Car-olyn Teragawa prepared Figure3.Funds forthe research were provided by the LernerGray Foundation, NSF grant BSR-8520305to George Lauder, and The Smithsonian

Institution s Caribbean Coral Reef Ecosys-tems program (Supported in part by ExxonCorporation) of which this is contributionNumber 297.1 thank its project leader KlausRuetzler and Mike Carpenter for the oppor-tunity to work in Belize. I was supportedduring the preparation of this manuscriptby NSF grant DCB-8812028 to Albert Ben-nett. Special thanks to Jim Hanken andMarvalee Wake for organizing the sympo-sium. Symposium support was provided bya National Science Foundation grant (BSR-8904370) to J. Hanken and M. H. Wake.REFERENCES

Akster, H. A., H. L. M. Granzier, and H. E. D. J. terKeurs. 1985. A comparison of quantitative ultra-structural and contractile characteristics of musclefibre types of the perch,Percajluviatilis.J. Comp.Phyiol. B 155:685-691.Alexander, R. M. 1971.Animal mechanics.Sidgwickand Jackson, London.Alexander, R. M. 1988. The scope and aims of func-tional and ecological morphology. Neth. J. Zool.38:3-22.Altringham, J. D. and I. A. Johnston. 1982. ThepCa-tension and force-velocity characteristics of skinned

fibers isolated from fish fast and slow muscles. J.Physiol. 333:421^149.Arnold, S. J. 1983. Morphology, performance andfitness. Amer. Zool. 23:347-361.Barel, C. D. N. 1983. Towards a constructional mor-phology of cichlid fishes (Teleostei, Perciformes).Neth. J. Zool. 33:357-424.Boag, P. T. and P. R. Grant. 1981. Intense naturalselection in a population of Darwin s finches. Sci-ence 214:82-85.Calow, L. J. and R. M. Alexander. 1973. A mechan-ical analysis of a hing leg of a frog (Rana tempor-aria). J. Zool., London 171:293-321.Cheverud, J. M., M. M. Dow, and W. Leutenegger.1985. The quantitative assessment of phyloge-netic constraints in comparative analyses: Sexualdimorphism in body weight in primates. Evolu-tion 39:1335-1351.Crome, F. H. J. and G. C. Richards. 1988. Bats andgaps:Microchiropteran community structure in aQueensland rainforest. Ecology 69:1960-1969.Emerson, S. B. and S. J. Arnold. 1989. Intra- andinterspecific relationships between morphology,performance, and fitness.In D. B. Wake and G.Roth (eds.),Complex organismal functions: Inte-gration andevolutioninvertebrates pp. 295-314.Wiley Press, New York.Felley.J. D. 1984. Multivariate identification of mor-phological-environmental relationships within theCyprinidae (Pisces). Copeia 1984:442-455.Findley, J. S. and H. Black. 1983. Morphological anddietary structuring of a Zambian insectivorous batcommunity. Ecology 64:625-630.Gatz, A. J. 1979. Ecological morphology of fresh-water fishes. Tulane Stud. Zool. Bot. 21:91-124.Gobalet, K. W. 1989. Morphology of the parrotfishpharyngeal jaw apparatus. Amer. Zool. 29:319-331.Grant, P. R. 1986. Ecology andevolutionof Darwin sfinches.Princeton University Press, Princeton.Hespenheide, H. A. 1973. Ecological inferences frommorphological data. Annu. Rev.Ecol. Syst. 4:213-229.Hiatt, R. W. and D. W. Strasburg. 1960. Ecologicalrelationships of the fish fauna on coral reefs of theMarshall Islands. Ecol. Monogr. 30:65-127.Hobson, E. W. 1974. Feeding relationships of tele-ostean fishes on coral reefs in Kona, Hawaii. Fish.Bull., U.S. 72:915-1031.Hoffman, S. G., M. P. Schildhauer, and R. R. Warner.1985. The costs of changing sex and the ontogenyof males under the contest competition for mates.Evolution 39:915-927.Holling, C. S. 1959. The components of predation asrevealed by a study of small-mammal predationof the European pine sawfly. Can. Entomal 91:293-320.Huey, R. B. 1987. Phylogeny, history, and the com-parative method. InM. E. Feder, A. F. Bennett,W. E. Burggren, and R. B. Huey (eds.),Newdirec-tions in ecologicalphysiology pp. 76-97. Cam-bridge University Press, New York.Huey, R. B. and A. F. Bennett. 1987. Phylogeneticstudies of coadaptation: Preferred temperature

atUniversidadNa


h


Downloadedfrom


13/14

692 PETER C. WAINWRIGHTversus optimal performance temperature of liz-ards.Evolution 41:1098-1115.

Huey, R. B. and R. D. Stevenson. 1979. Integratingthermal physiology and ecology of ectotherms: Adiscussion of approaches. Amer. Zool. 19:357-366.James, F. C. 1970. Geographic size variation in birdsand its relationship to climate. Ecology 51:365-390.James, F. C. 1982. The ecological morphology ofbirds:A review. Ann. Zool. Fennici 19:265-275.James, F. C. 1991. Complementary description andexperimental studies of clinal variation in birds.Amer. Zool. 31:694-705.Jayne, B. C. and A. F. Bennett. 1990. Selection onlocomotor performance capacity in a natural pop-ulation of garter snakes. Evolution 44:1204-1229.Karr, J. R. and F. C. James. 1973. Ecomorphologicalconfigurations and convergent evolution in speciesand communities. InM. L. Cody and J. M. Dia-mond (eds.),Ecology and evolution of communi-ties,pp. 258-291.Belknap Press, Cambridge.Kaufman, L. S. and K. F. Liem. 1982. Fishes of thesuborder Labroidei (Pisces: Perciformes): Phylog-eny, ecology, and evolutionary significance. Bre-viora 472:1-19.Kiltie, R. A. 1982. Bite force as a basis for nichedifferentiation between rain forest peccaries (7a-yassu tajacu and T. pecari).Biotropica 14:188-195.Kotrschal, K. 1988. Evolutionary patterns in tropicalmarine reef fish feeding. Z. Zool. Syst. Evolut.-Forsch. 26:51-64.Larson, A., D.B.Wake, L. R. Maxson, and R. Highton.1981. A molecular phylogenetic perspective onthe origins of morphological novelties in the sal-amander tribe Plethodontini. Evolution 35:405-422.Lauder, G. V. 1981. Form and function: Structuralanalysis in evolutionary morphology. Paleobiol-ogy 7:430-442.Lauder, G. V. 1990. Functional morphology and sys-tematics. Annu. Rev. Ecol. Syst. 21:317-340.Lauder, G. V. 1991. Biomechanics and evolution:Integrating physical and historical biology in thestudy of complexsystems. InJ. M. V. Rayner(ed.),Biomechanics inevolution.Cambridge UniversityPress,Cambridge. (In press)Lauder, G. V. and K. F. Liem. 1989. The role ofhistorical factors in the evolution of complexorganismal functions.In D. B. Wake and G. Roth(eds.),Complex organismal functions: Integrationandevolutioninvertebrates pp.63-78.Wiley Press,New York.Lavin, P. A. and J. D. McPhail. 1985. The evolutionof freshwater diversity in the threespined stickle-back (Gasterosteus aculeatus) Can. J. Zool. 63:2632-2638.Leisler, B. 1980. Morphological aspects of ecologicalspecialization in bird genera. Okol. Vogel. 2:199-220.Liem, K. F. 1974. Evolutionary strategies and mor-phological innovations: Cichlid pharyngeal jaws.Syst. Zool. 22:424-441.Liem, K. F. 1989. Functional morphology and phy-logenetic testing within the framework of syme-

comorphosis. Acta Morphol. Neerl.-Scand. 27:119-131.Leim, K.F.andP.H. Greenwood. 1981. A functionalapproach to the phylogeny of the pharyngognathteleosts. Amer. Zool. 21:83-101.Liem, K. F. and S. L. Sanderson. 1986. The pharyn-geal jaw apparatus of labrid fishes: A functionalmorphological perspective. J. Morphol. 187:143-158.Losos, J.B. 1990. Ecomorphology, performance, andscaling of West IndianAnolis lizards: An evolu-tionary analysis. Ecol. Monogr. 60:369-388.Mayr, E. 1960. The emergence of evolutionary nov-elties.InS. Tax (ed.), Evolution after Darwin,pp.349-380. University of Chicago Press, Chicago.Miles, D.B.,R.E.Ricklefs, and J.Travis. 1987. Con-cordance of ecomorphological relationships in threeassemblages of passerine birds. Amer. Natur. 129:

347-364.Motta, P. J. 1988. Functional morphology of thefeeding apparatus often species of Pacific butterflyfishes (Perciformes: Chaetodontidae): An eco-morphological approach. Env. Biol. Fish. 22:39-67 .Munz, F. W. and W. N. McFarland. 1973. The sig-nificance of spectral position in the rhodopsins oftropical marine fishes. Vision Res. 13:1829-1874.Osenberg, C. W. and G. G. Mittelbach. 1989. Effectsof body size on the predator-prey interactionbetween pumpkinseed sunfish and gastropod. Ecol.Monogr. 59:405^32.Palmer, A. R. 1979. Fish predation and the evolutionof gastropod shell sculpture: Experimental andgeographic evidence. Evolution 33:697-713.Powell, P. L., R. R. Roy, P. Kanim, M. A. Bello, andV. Edgerton. 1984. Predictability of skeletalmuscle tension from architectural determinationsin guinea pig hindlimbs. J. Appl. Physiol. 57:1715-1721.Price, T. D., P. R. Grant, H. L. Gibbs, and P. T. Boag.1984. Recurrent patterns of natural selection inpopulation of Darwin s finches. Nature 309:787-789.Randall, J. E. 1967. Food habits of reef fishes of theWestIndies.Stud. Trop. Oceanog. (Miami) 5:665-847.Ridley, M. E. 1983. The explanation oforganicdiver-sity: The comparative method and adaptations formating.Clarendon Press, Oxford.Sale,P. F. 1980. The ecology of fishes on coral reefs.Oceanogr. Mar. Biol. Annu. Rev. 18:367-421.

Schluter, D. 1988. Estimating the form of naturalselection on a quantitative trait. Evolution 33:849-861.Schoener, R. W. 1986. Resource partitioning. In J.Kikkawa and D. J. Anderson (eds.), Communityecology:Pattern andprocess pp. 91-126. Black-well Scientific, Melbourne.Shannon, C. E. 1949. The mathematical theory ofcommunication.InC. E. Shannon and W.Weaver(eds.), The mathematical theory of communica-tion, pp. 91-126. University of Illinois Press,Urbana.Stiassny, M. L. J. and J. Jensen. 1987. Labroid inter-relationships revisited: Morphological complex-

atUniversidadNa


h


Downloadedfrom


14/14

EXPERIMENTAL ECOMORPHOLOGY 693ity, key innovations, and the study of comparativediversity. Bull. Mus. Comp. Zool. 151:269-319.Wainwright,P .C. 1987. Biomechanical limits to eco-logical performance: Mollusc-crushing in theCaribbean hogfish, Lachnolaimus maximus(Labridae). J. Zool. (London) 213:283-297.Wainwright, P. C. 1988. Morphology and ecology:Functional basis of feeding constraints in Carib-bean labrid fishes. Ecology 69:635-645.

Wainwright, P. C. 1989. Functional morphology ofthe pharyngeal jaw apparatus in perciform fishes:An experimental analysis of the Haemulidae. J.Morphol. 200:231-245.Werner, E. E. 1977. Species packing and niche com-plementarity in three sunfishes. Amer. Natur. I l l :553-578.Yamaoka, K. 1978. Pharyngeal jaw structure in labridfish.Pub.Seto Mar. Biol. Lab. 24:409^126.

atUniversidadNa


h


Downloadedfrom

amer. zool.-1991-wainwright-680-93(1)

Documents