FEEDING ECOLOGY AND FUNCTIONAL
MORPHOLOGY OF WESTERN ATLANTIC GROUPERS (SERRANIDAE: EPINEPHELINAE)

D. C. Weaver*. United States Geological Survey
7920 NW 71st Street, Gainesville, Florida

Fisheries and Aquatic Sciences, University of Florida
7922 NW 71st Street, Gainesville, Florida
 
Presented at the 9th International Coral Reef Symposium, Bali, Indonesia.  Oct. 23-27, 2001.


ABSTRACT

 Groupers are common apex predators that occur on tropical and warm-temperate reef systems throughout the world.  The genus Mycteroperca exhibits an early onset of piscivory, and have diets dominated by fishes throughout the majority of their life history. In contrast, crustaceans dominate the diets of juveniles and remain important in the diets of adults for members of the genus Epinephelus.  Patterns of dentition, jaw morphology, and lever ratios of the lower jaw were compared for representative species within each genus to identify potential morphological adaptations for feeding. All members of the genus Mycteroperca examined have enlarged teeth in the upper jaw, a reduced number of fixed teeth in the lower jaw, and relatively low lever ratios (.10 closing/.17 opening).  In contrast, Epinephelus spp. have teeth of reduced size and a greater number of teeth in the lower jaw and higher lever ratios (.17 closing/.24 opening).  Increasing tooth size, a reduction in tooth number, and decreased jaw lever ratios are likely to increase capture success of evasive, soft-bodied prey, particularly fishes and squids, and reflect the dietary patterns observed. Groupers exhibit ecomorphological trends in feeding morphology that parallel more "specialized" reef fishes, such as wrasses (family Labridae).

INTRODUCTION

Groupers (family Serranidae, subfamily Epinephelinae) are common predatory reef fishes of worldwide tropical/warm-temperate seas and are represented by 15 genera and 159 species (Heemstra and Randall, 1993). Phylogenetic systematics and patterns of ecomorphology (defined as variation in morphology that contributes to variation in feeding ability (Wainwright and Richards, 1995)) among the groupers are poorly known. Relationships among the genera have been the subject of much disagreement, and in general groupers are classified as "unspecialized carnivores". An early paper by Randall (1967) briefly mentioned differences in dentition and feeding behavior of certain piscivorous groupers, but further investigations of feeding morphology in epinepheline serranids have not been undertaken. Analysis of mandibular shape in fishes is of interest because movement of the mandible (lower jaw depression) initiates buccal expansion in prey capture, and hypotheses concerning jaw dimensions and related biomechanical properties have been proposed for other fish taxa (Wainwright and Richards, 1995; Westneat 1995).

OBJECTIVES

Mandibular jaw dimensions were examined in two genera of groupers: Mycteroperca (M. microlepis and M tigris) and Epinephelus (E. morio and E. itajara) to identify morphological divergence among the four taxa.  The four species selected will provide a template for future analysis of the remaining epinepheline genera and species of ecomorphological interest, as there is widespread variation in diet and morphology among the subfamily.

METHODS

Grouper mandibular bones (left jaw) were dissected from whole specimens, and the overlying soft tissue removed. Mandibles were photographed using a Nikon Coolpix 900 digital camera at high resolution (1240 by 960 pixels).  Mandible length was measured as the distance from the QM joint to the anterior edge of the dentary (this measure is equivalent to the out-lever in estimating lever ratios).  Distances to the leading edge of the dentary from the QM joint, the height of the ascending process of the dentary bone, and the posterio-ventral extension of the mandible should offer insight into the morphological contributions of skeletal elements to previously hypothesized biomechanical differences among fishes in fish jaws (i.e. variation in mandible size and shape leading to a divergence of in-lever/out-lever arms and resulting lever ratios).

To identify overall shape and difference in landmark positions among the four groupers, outline drawings were made of mandibles from each taxa (Fig. 3). Digital photographs of individual grouper jaws were imported into the Freelance Graphics software package (1993-Lotus Development Corporation), and outlines were drawn of each specimen, tracing edge of the dentary, articular and retroarticular bones.   Tooth counts and measurements of canine teeth were made under a dissecting microscope. Calculations of closing and opening lever ratios follows Wainwright and Richards (1995 – See Fig. 2).

Tiger Grouper-Mycteroperca tigris

Gag - Mycteroperca microlepis

Red Grouper - Epinephelus morio

Jewfish - Epinephelus itajara

Figure 1.  Jaws and Diets of select species of western Atlantic groupers.  Dietary information is based on Randall (1967) for tiger grouper and jewfish, and Weaver ( 1996) for gag and red grouper.

Figure 2.  Mandibular anatomy and estimates of lever ratios in groupers. Numbers in upper figure identify measurements taken for morphometric analysis.  Abbreviations are as follows: ART: articular, AP: ascending process, CAN: canine, DEN: dentary, FOR:foramen, FOS: fossa, QM: quadrato-mandibular joint, RET: retroarticular, SUL: sulcus.  Methods of calculating lever ratios are taken from Wainwright and Richards (1995): Closing levers are calculated as the ratio of the closing in-lever (distance from QM joint to insertion of adductor mandibulae muscle) divided by the outlever distance. Opening in-lever is calculated as the distance from the insertion of the interopercular ligament (lop-lig) to the QM joint divided by the outlever distance.

Figure 3. Trends in jaw morphology of groupers

RESULTS

Mandibular shape among the species examined shows considerable variation (Fig. 3). Gag and tiger grouper mandibles bear a relatively straight edge along the dorsal margin, as a result of increased dentary width at the foramen and fossa. Gag and tiger grouper mandibles display reduced height of the ascending process, greatly reduced width of the articular/retroarticular bones along the posteriovental (PV) margin of the jaw, and reduced mandible width along the entire ventral margin (Fig. 3). The rear margin of the dentary is greatly constricted in gag and tiger grouper and expanded in red grouper. This pattern is further exemplified by jewfish, which develop the greatest height of the ascending process and greatest expansion of the PV region.  These features result in an extremely narrow mandible for gag and tiger grouper, increasing height in red grouper, and the greatest mandibular height in jewfish. Closing lever ratios were .09 and .10 in tiger grouper and gag, .17 in red grouper, and .18 in jewfish (Fig. 4). Opening ratios ranged in value from .17 in gag and tiger grouper to .24 in red grouper, and .31 in jewfish.  Dentition patterns vary dramatically among species, as tiger grouper have the largest teeth with decreased tooth number, and jewfish have the highest number of teeth, and smallest tooth size (Figs. 5 and 6).

Figure 4.  Lever Ratios. Hatched boxes represent closing lever ratios, and closed boxes indicate opening ratios.

Figure 5.  Dentary Tooth Number

Figure 6.  Bottom Canine Tooth Size (mm)

DISCUSSION

Analysis of jaw shape reveals variation in mandibular jaw shape that likely contributes directly to functional (~biomechanical) differences among the taxa examined.  Gag have relatively slender mandibular bones and a reduced distance from the QM joint to the PV margin of the jaw, causing the insertion of the interopercular ligament to be closer to the mandibular joint.  This arrangement partially explains the low lever ratio values exhibited by gag and tiger grouper. Assuming bone density and thickness do not vary among taxa, reduced jaw height also may lead to increased velocity of jaw opening due to reduction of overall bone mass. Gag and tiger grouper feed on highly evasive prey such as pelagic schooling fishes and squids, and actively pursue and capture their prey, and increased jaw velocity likely aids in prey capture.  The reduction in numbers of teeth in the tiger grouper and gag dentary results in tooth spacing that serves to increase penetration of soft bodied prey (dentary teeth are visible along the upper margin of each jaw in Figure 1). Bite force may not be as important for this species, since penetration by the enlarged canines would serve to grip and immobilize prey. Red grouper and jewfish, however have diets that differ dramatically from gag and graysby. The inclusion of high proportions of crabs and other hard-bodied, slow-moving prey poses different problems in prey capture. Both red grouper and jewfish are likely to be ambush predators, and may rely heavily on suction feeding for prey capture.  Mandibular shape in red grouper and jewfish reflect this requirement, as increased height likely strengthens the lower jaw and may support more forceful jaw opening, indicated by the high lever ratios measured for each species. Increased jaw height/thickness allows the generation of greater bite force and lower risk of jaw torsion when feeding on hard-bodied prey. Stronger jaws would be particularly advantageous for jewfish, which continue to feed on large, hard-shelled lobsters (and sea turtles!) throughout all body sizes (Randall, 1967). The divergent pattern of jaw shape in the four taxa examined may offer some insight into evolutionary changes among epinepheline serranids as a number of morphological features in groupers have diverged and parallel their ecological roles in the marine environment.

REFERENCES

Heemstra, P. and J. Randall. 1993. Groupers of the World. FAO Species Catalogue 125(16):1-382.

Randall, J. E. 1967. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanogr. (Miami).
5:665-847.

Wainwright, P. and B. Richards. 1995. Predicting prey use from morphology. Env. Biol. Fishes
44:97-113.

Weaver, D. C. 1996. Feeding ecology and ecomorphology of three sea basses (Pisces: Serranidae) in the northeastern Gulf of Mexico. Masters Thesis. University of Florida, Gainesville, FL.

Westneat, M. W. 1995. Phylogenetic systematics and biomechanics in ecomorphology. Env. Biol. Fishes
44:263-283.

ACKNOWLEDGEMENTS

I would like to thank A. M. Eklund of NMFS, Miami for providing jewfish photographs and specimens, and B. Brown of the American Museum of Natural History for providing access to skeletal preparations for tooth measurements and jaw photographs.