Ecomorphology: Experimental Functional Anatom foyr Ecological … · 2020. 6. 1. · AMER. ZOOL. 31:680-69, 3 (1991) Ecomorphology: Experimental Functional Anatom foyr Ecological

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

Ecomorphology: Experimental Functional Anatomy forEcological Problems'

PETER C. WAINWRIGHT

Department of Biological Sciences, Florida State University, Tallahassee, Florida 32306

SYNOPSIS. 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 ecology by limiting the ability of the individual to perform key tasksin its daily life. In this scheme the effect of morphological variation on behavioral perfor-mance is first tested in laboratory experiments. As the behavioral capability of an individualdefines the range of ecological resources that it can potentially make use of (the potentialniche), the second step in the scheme involves comparing the potential niche of an individualto actual patterns of resource use (the realized niche). This permits a quantitative assessmentof the significance of an organism's maximal capabilities in determining actual patterns ofresource use.

An example is presented from work on the feeding biology of fishes in the family Labridae(wrasses and parrotfishes). Most labrids feed by crushing shelled prey in their powerfulpharyngeal jaws. This example explores the dietary consequences of variation in crushingstrength among and within species. Crushing strength was estimated from biomechanicalanalyses of the crushing apparatus in several species, and these predictions of relative strengthwere tested in laboratory feeding experiments with hard-shelled prey. Morphology accuratelypredicted relative crushing ability, and the final section of the study explored the effect ofvariation in crushing ability on diet. Within each of three species crushing strength appearsto underlie a major ontogentic dietary switch from soft-bodied prey to a diet dominated byhard-shelled prey. In each species this switch occurred at about the same crushing strength,around 5 Newtons (N), in spite of the fact that this crushing strength is achieved by thethree species at different body sizes. Diet breadth increases during ontogeny in each species,until a crushing strength of 5 N is achieved, 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 prey in 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 lineage of fishes to 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-organisms and the environment. It shares a n i z e d as a central force in 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 environment as a major causeogy, and ecomechanics, and no distinction o f organismal design (see for exampleis implied here other than an emphasis on James, 1991), and the majority of ecomor-functional morphology. Within ecomorphological research has focused on adaptivephology two primary axes of research have explanations for observed design patternsemerged that concentrate on either the effect (Hespenheide, 1973; Leisler, 1980; Barel,of the environment on functional design or 1 9 8 3 ; Alexander, 1988). Recent advances

have brought to the forefront the role ofphylogenetic history as an alternate expla-nation for design (Lauder, 1981, 1990;

'From the Symposium on Experimental Approaches Ridley 1983' Huey 1987) and integrativeto the Analysis of Form and Function presented at the annrnarhes that a w « the relative rnntriCentennial Meeting of the American Society of Zool- approacnes Uiat assess the relative contn-ogists, 27--30 December 1989, at Boston, Massachu- button of phylogeny and adaptation aresetts. emerging (Cheverud et ah, 1985; Huey and

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EXPERIMENTAL ECOMORPHOLOGY 681

Bennett, 1987; Motta, 1988; Liem, 1989;Losos, 1990).

The relationship between functionaldesign and the environment can also workthe other way, however, because the waythat an organism is constructed influencesits ability to interact with the environment.Thus, the second major branch of ecomor-phology looks at the role of functional mor-phology in shaping the ecological attributesof organisms. A tremendous literature existsdocumenting correlations between mor-phological and ecological patterns (James,1970, 1982; Karr and James, 1973; Gatz,1979; Findley and Black, 1983;Felley, 1984;Miles et al., 1987; Crome and Richards,1988; Kotrschal, 1988), and an increasingamount of work has centered on the con-sequences of morphological variation forfitness (Boag and Grant, 1981; Price et al,1984; Schluter, 1988; Jayne and Bennett,1990). However, few studies have criticallyexamined the causal role of functional mor-phology in determining aspects of an organ-ism's general ecology (Werner, 1977; Kiltie,1982; Lavin and McPhail, 1985). Clearly,functional morphology has some influenceon the ability of an organism to obtainresources from the environment, but howdoes one go about rigorously quantifying therole of functional morphology in determin-ing patterns of ecological resource use? Inthis paper I advocate an experimentalapproach for investigating this generalproblem. The method that is described takesadvantage of the link between morphologyand ecology provided by performance (Hueyand Stevenson, 1979; Arnold, 1983; Emer-son and Arnold, 1989), and emphasizes therole of experimental functional morphologyin establishing causation in morphology-ecology correlations. One contribution ofthis technique is that it supplies the answersto several questions that, taken together,quantitatively describe the "fit" of anorganism to its environment. The processis illustrated with a discussion of the feedingbiology of labrid fishes (Wainwright, 1987,1988).

Morphology, performance and ecologyIn a now classic paper, Arnold (1983)

described a method for studying the effect

of morphology on fitness. I would like toextend the point that was made in that paperand suggest that the same general frame-work is appropriate for studying the linkbetween morphology and other aspects ofan individual's ecology. The central idea inthis scheme is that morphology influencespatterns of resource use by limiting the abil-ity of the individual to perform key tasksthat are relevant to obtaining resources fromthe environment. The limits of behavioralcapabilities constrain the range of resourcesthat an individual can obtain. Thus, the pro-cess of relating morphology to ecology canbe separated into two stages. The first stepis to determine the effect of morphologicalvariation on performance, or the ability ofthe organism to perform some relevant task.This is accomplished with behavioralexperiments conducted in the laboratory.Biomechanical analyses of functional sys-tems lead to specific predictions regardingthe effect that variation in the componentsof the system have on performance. Thestrength of the functional approach lies inthe ability to assign causation to otherwisecorrelative relationships between specificdesign features and observed performance,based on independent functional analyses(Lauder, 1991).

The second step is to determine the effectof performance on actual patterns of resourceuse. It is on this problem that remarkablylittle work has been done. The basic idea isto compare potential resource use, deter-mined from the performance experiments(i.e., the potential niche), with actual pat-terns of resource use, determined from fieldstudies of natural populations (i.e., the real-ized niche). How important are the maxi-mal capabilities of an individual in shapingresource use? What is the relative impor-tance of different capabilities? Within therange of an individual's capabilities wheredoes it most frequently operate on a day-to-day basis? These questions have onlyrarely been addressed, yet their answers pro-vide a quantitative understanding of thenature of an organism's "fit" into its envi-ronment.

It is important to emphasize that a fun-damental problem in ecology is to identifythe factors that determine patterns of

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682 PETER C. WAINWRIGHT

FIG. 1. A three-dimensional visualization of the scaling of pharyngeal jaw gape and crushing strength in theCaribbean hogfish, Lachnolaimus maximus. The range of prey sizes and prey hardness 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).

resource use by organisms (Schoener, 1986).Much ecological research is devoted toassessing the relative significance of variousfactors in shaping resource use patterns,whether the resource be food (Osenberg andMittelbach, 1989), space (Sale, 1980), time(Munz and McFarland, 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 influencepatterns of prey use, two may be viewed asfundamental: (1) prey availability, and (2)the ability of the predator to utilize eachprey type. Thus, the types of prey and theirrelative abundance define the food resourcefor a predator, and the predator's ability tolocate, capture, and handle the various preytypes constrains the range of prey that can

potentially make up the diet of the predator.Other factors that can shape patterns 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 fundamental range of preydetermined by the feeding capabilities of thepredator {e.g., Holling, 1959; Grant, 1986;Osenberg and Mittelbach, 1989).

To illustrate some of these ideas an exam-ple is presented in Figure 1 based on pre-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 (Wainwright, 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-

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22 Z4 26 28 3fl 32 a4 3B

Log BODY MASS (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 mass. The solid line indicates the maximum sizeC. litteratum shell that hogfish are strong enough tocrush. This relationship is derived from morphologi-cally based estimates of hogfish crushing strength anda determination of the force required to crush shells ofdifferent sizes. The relationship between shell size andforce at failure was then used to transform estimatesof 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, the fish must be able to exert enoughcrushing force to crack the mollusc shell.Jaw gape and crushing strength increaseduring ontogeny; Figure 1 illustrates therange 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 determining patterns of pre-dation on at least one prey species (Fig. 2).Plotted are the shell sizes of 331 individualsof 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 compared with 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 smaller snails, 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 of Ceri-thium shells is such 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-thium that 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 qualitative changes in theperformance gradient of a lineage, and ulti-mately in the range of environmentalresources that can be used. Key innovationsmay 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). Hypothesized key innovationscan be tested first by functional analyseswhich elucidate the theoretical 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-

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soc

EP

LE4

-FM

-UPJ

SOC

EP

SOCV

LE4

LE4

LPJ

FIG. 3. Pharyngeal jaw structures of three species of Caribbean Halichoeres. 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 of H. bivittatus, respectively. C and D show lateral views of H. maculipinna and H. 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 labrid fishes (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 pharyngeal bite, and under-lies the potential for eating hard prey (Kauf-

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man 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(Wainwright, 1989). As a group, labrids aretrophically distinct from most other coralreef fishes in exhibiting diets typically dom-inated by hard prey, such as molluscs, echi-noderms 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, these fish crush shelled prey in theirpharyngeal jaws. Species of Halichoeres feeddiurnally 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-tions of relative crushing strength were testedin laboratory performance experiments 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 labrids

has 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 ofCaribbean Halichoeres are presented in Fig-ure 3. Most superficial bones and musclesare not illustrated to permit 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-ryngobranchials, each fused with an 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 most species the fourthlevator externus muscle is relatively small,but in others it may approach the size of thelevator posterior {e.g., Fig. 3D). Thus, thelower jaw is suspended from the neurocra-nium in a muscular sling. When prey arecrushed they are held between the upper andlower 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 not the sameas the morphological cross sectional 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/cm2 for the forceproducing capability of fish muscle tissueper unit of cross sectional area was takenfrom the literature (Altringham and John-ston, 1982;Aksterftfa/., 1985). Two factors

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H.

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CARIBBEAN LAB RIDS:levator posterior muscle of 25 g fish

45 100 250

BODY LENGTH (mm)

FIG. 4. Relationship between estimated pharyngealjaw crushing strength and body length for six speciesof Caribbean labrids. Both axes are log,0 scales. Sizeranges are bounded by the smallest and largest indi-vidual examined from each species. Crushing strengthestimates are based on morphological analyses. 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 dashed lines. 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).

PerformanceTo test these morphologically based pre-

dictions of relative crushing strength, sev-

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a

r =-0.964

3 4 5 6 7 8 9

GAPE (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 primarycrushing muscle, 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-ichoeres poeyi, 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 three Halichoeres spe-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 crushing strength. Resultsfrom experiments conducted with the gas-tropod Cerithium litteratum are presented

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CRUSHING FORCE POTENTIAL (N)

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PHARYNGEAL JAW GAPE (mm)

FIG. 6. Results of laboratory feeding experiments withthree species of Halichoeres designed 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; ANCOVA for species effect: /> = 0.21)and (B) pharyngeal jaw gape of fishes (ANCOVA forspecies slopes: P = 0.78; ANCOVA for species effect:P < 0.001). • = H. maculipinna, • = H. garnoti, and• = H. bivittatus. From Wainwright (1988).

in Figure 6. The largest snails eaten by H.maculipinna were not as large as those eatenby the same size fish in the other two species(see triangles in Fig. 6). However, amongall species, fish of the same crushing strengthcrushed snails of the same size. As pre-dicted, H. garnoti and H. bivittatus arestronger than similar sized H. maculipinnaand are able to eat larger, harder gastropods.Similar results were found for a heavilyarmored species of crab prey. However,pharyngeal jaw gape limited maximum preysize in experiments with a soft bodied por-tunid crab, showing that the functional lim-itation on maximum prey size depends onthe physical characteristics of the prey(Wainwright, 1988). Soft-bodied preybecome too large to fit between the pharyn-

geal jaws of wrasses before the limits ofcrushing strength are reached.

EcologyWhat are the dietary consequences of

variation among and within species in pha-ryngeal jaw crushing strength? It is clear fromthe performance experiments that, for hard-shelled prey, crushing strength limits themaximum size prey that the three Hali-choeres species can feed on. But variationamong species in crushing strength need notlead to differences in patterns of prey use.There is no reason a priori to expect thatstronger fish will necessarily take advantageof their greater performance capabilities.Indeed, it is generally not well known howclose to their maximal capabilities preda-tors tend to feed.

To explore the relationship betweencrushing strength, gape, and patterns of preyuse stomach contents were analyzed for anontogenetic series of each of the three spe-cies used in the performance experiments.Each species was broken down into 10 mmsize classes and the stomach contents of atotal of 499 specimens of the three specieswere sorted into 11 taxonomic prey cate-gories. These categories were primarilyordinal or lower levels (e.g., gastropods,pelecypods, isopods, polychaetes, echi-noids, ophiuroids) so that the conclusionsthat were drawn concerning prey use pat-terns reflect the use of relatively broad phy-logenetic groups of prey taxa. This level ofanalysis was chosen so that prey with sim-ilar defense characteristics tended to begrouped together (i.e., gastropods are mostlyhard-shelled, isopods were usually small andsoft-bodied). All specimens were collectedalong the barrier reef off the Caribbean coastof Belize in Central America.

Two specific questions were addressedconcerning the role of crushing strength inshaping patterns of prey use. First, do stron-ger fish eat harder-bodied prey? Second,given that the range of prey that these fishare able to crush and consume varies amongspecies and increases continuously duringontogeny, (hence, the potential niche isbroader for stronger fish) do stronger fishactually have broader diets?

To answer the first question the volume

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CRUSHING FORCE POTENTIAL (N)

110

BODY LENGTH (mm)

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FIG. 7. Mean volume percent of hard prey types (mol-luscs, echinoids, and ophiuroids) found in the stomachcontents of three species of Caribbean Halichoeres. Eachspecies is broken down into 10 mm size classes. 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 mm SL, 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)

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PHARYNGEAL JAW GAPE (mm)

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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 a function of crushing strength, above 5 N 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. garnoti and 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 Caribbean Hal-ichoeres are able to consume increases con-tinuously during ontogeny, diet breadth

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

DISCUSSION

The 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 standpoint, a largecomponent 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), and (2) fisheswith the same estimated crushing strengthconsumed similar amounts of hard-bodiedprey, in spite of the fact that the same crush-ing ability occurred at very different bodysizes in the three 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 dietaryhabits among the three Halichoeres revealedpatterns 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 predictions weresupported in the feeding experiments (Fig.6), but do these differences between speciesin feeding ability result in significant differ-ences in dietary habits? How important 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 the major differencesbetween the current diets of these two spe-cies. At any given body size H. maculipinnasimply cannot successfully handle much ofthe prey eaten by H. 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 constraining the feeding biologyof labrid fishes, then why is crushing 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 and H. pictus) share an ances-try of weaker jawed predecessors. Unfor-tunately, this possibility cannot 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 production that is gained fromlarger angles of pinnation within the muscle.The two extremes of this trade-off are foundin the previously discussed hogfish, Lach-nolaimus maximus, and Halichoeres pictus.The hogfish's diet is made up almost entirelyof molluscs, and this 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 mm, com-pared to a gape of 8.3 mm for a H. pictusof the same size. H. pictus feeds almostentirely on midwater zooplankton and phy-toplankton, including large, soft-bodied

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siphonophores that make up 24% of the diet(Wainwright, 1988). Unfortunately, nocomparisons were made in this study of spe-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 apparatus has been hypoth-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 provides 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 (Lauder, 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 under 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 patterns of prey use seen in coral reeffishes around the world. In a study of thefeeding habits of 212 species of Caribbeanreef fishes (Randall, 1967), only 12 specieswere found to consume large amounts ofmolluscs (>20% of the diet by volume). Ofthe 12 species, six were labrids, one was aneagle ray {Aetobatis 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 or the oral jaws (Randall, 1967;Palmer, 1979; Wainwright, 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. Thus, only about 5% offishspecies on reefs have the ability to overcomethe 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.Perhaps the labrid pharyngeal jaw conditionis 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 arelatively 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-

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ical 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.

ACKNOWLEDGMENTS

I 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 Figure 3. Funds forthe research were provided by the LernerGray Foundation, NSF grant BSR-8520305to George Lauder, and The SmithsonianInstitution'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.

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