Ecomorphology of Feeding in Coral Reef Fishes Peter C. Wainwright David R. Bellwood Center for Population Biology Centre for Coral Reef Biodiversity University of California at Davis School of Marine Biology and Aquaculture Davis, California 95616 James Cook University Townsville, Queensland 4811, Australia I. Introduction fish biology. We have attempted to identify generalities, II. How Does Morphology Influence Ecology? the major patterns that seem to cut across phylogenetic III. The Biomechanical Basis of Feeding Performance and geographic boundaries. We begin by constructing IV. Ecological Consequences of Functional a rationale for how functional morphology can be used Morphology to enhance our insight into some long-standing eco- V. Prospectus logical questions. We then review the fundamental me- chanical issues associated with feeding in fishes, and the basic design features of the head that are involved in prey capture and prey processing. This sets the stage I. Introduction for a discussion of how the mechanical properties of fish feeding systems have been modified during reef fish di- nce an observer gets past the stunning coloration, versification. With this background, we consider some O surely no feature inspires wonder in coral reef of the major conclusions that have been drawn from fishes so much as their morphological diversity. From studies of reef fish feeding ecomorphology. Because of large-mouthed groupers, to beaked parrotfish, barbeled space constraints we discuss only briefly the role of goatfish, long-snouted trumpet fish, snaggle-toothed sensory modalities--vision, olfaction, electroreception, tusk fish, tube-mouthed planktivores, and fat-lipped and hearingmbut these are also significant and diverse sweet lips, coral reef fishes display a dazzling array elements of the feeding arsenal of coral reef fishes and of feeding structures. And, even the most casual fish entire review chapters could be written on each one. watcher quickly gets a sense that this diversity means something, that fish form is related to what the animals eat. Clearly there is something to this impression, but just how are head and body morphology connected II. How Does Morphology to prey choice? Are we really able to predict what a Influence Ecology? reef fish eats from studying its jaws and teeth? What are the major axes of diversification that are seen There is a strong intuitive awareness of the link between in reef fishes? Which morphological and ecological the design of organisms and their natural history. We in- trophic types show the most common convergence? stinctively see the connection between the large mouth What ecological insights into reef processes have been and sharp raptorial teeth of the coral trout, Plectropo- gained from consideration of the functional design of mus leopordus, and the observation that it preys largely fish feeding mechanisms? on other fishes. Similarly, the massive platelike jaws and In this chapter we explore the relationship between the bulky jaw muscles of the porcupine fish, Diodon fish anatomy and feeding habits. Our overall goal is to hystrix, seem well suited to this fish's diet of hard- show how an understanding of the functional morphol- shelled molluscs. Why do these associations between ogy of fish feeding mechanisms can be a powerful tool gross morphology and feeding habits appeal to our when considering several ecological issues in coral reef sense of order? We see in these examples morphological Coral Reef Fishes Copyright 2002, Elsevier Science (USA). All rights reserved. 33 34 Wainwright and Bellwood attributes that we expect to enhance the ability of these system functions, one can make well-informed predic- fishes to perform the key tasks that are involved in feed- tions about the performance of similar systems in which ing on their prey. Our experience with other fishes sug- performance has not been measured. The significance gests that Diodon has unusually large jaw muscles and of this point lies in the common practice of using corre- bones to enable an exceptionally powerful bite capable lations between morphological and ecological variables of crushing the hard shells of gastropods and bivalves. as a basis for generalizing to unstudied taxa. Such an The key here is that there is a causal connection be- approach will be strongest when thorough functional tween morphology and performance, or the ability of analyses underlie the selection of key morphological the fish to perform key tasks. The connections between traits for study. Spurious correlations between morpho- morphology and performance on the one hand, and logical and ecological traits can come about for many between performance and ecological patterns on the reasons, such as underlying phylogenetic patterns, or other hand, are the focus of ecomorphology, the study the fact that often many morphological features are in- of the functional and ecological consequences of or- tegrated so tightly that correlations will appear even ganismal diversity (van der Klaauw, 1948; Barel, 1983; when there is no causal connection. For example, the Motta and Kotrschal, 1992; Wainwright and Reilly, size of almost every structure in the body changes with 1994; Koehl, 1996). growth in concert with overall body size, so that many structures will show a correlation with an ontogenetic A. Linking Morphology change in feeding habits even if they are not related to and Performance feeding behavior. The design of physiological systems determines B. The Role of Behavioral Performance their performance properties. Just as the component in Shaping Ecological Patterns parts of man-made machines can be modified to pro- duce engines with differing performance qualities, so In general, the performance capacity of individual too are the elements of biological machines modified animals is a central factor in determining patterns of re- during evolution to produce diversity in performance source use, such as space and prey, and ultimately their of the overall system. So, in principle, understanding fitness. This link may be starkly direct, as in the conse- how physiological and biomechanical systems func- quences of escape locomotor performance for avoiding tion and knowing the role of the various component predation, but, direct or indirect, the ability to perform parts provides the foundation for interpreting their various tasks enters into the equations that determine ecological role. Research fields such as functional usage of virtually all resources that an animal seeks dur- morphology, physiology, and biomechanics aim to ing its life. Here we are concerned with understanding learn how biological systems work, providing insights the factors that shape the feeding habits of reef fishes, in into design and thus a framework for interpreting particular the connection between feeding performance diversity. These disciplines establish our best under- and prey consumption. standing of the causal connection between design and The first and most obvious effect of performance performance. on feeding habits is that limits on performance place Biological function involves more than gross constraints on the range of prey that potentially can be anatomy, and significant modifications to functional utilized. A consequence of this observation is that all in- systems can occur at many levels of organization. Thus, dividuals will be functionally incapable of successfully one might consider the consequences of changes in the feeding on most of the possible prey in their environ- mechanical advantage of the jaw muscle as it crosses ment. Many reef fishes use suction feeding to capture the jaw joint, the consequences of different myosin iso- prey that they swallow whole. In suction-feeding preda- forms for muscle contraction speed, the spectral prop- tors, the size of the oral aperture directly limits the size erties of different visual pigments, or the digestive prop- of prey that can be eaten (Werner, 1977; Wainwright erties of various enzymes. But, whether the problem is and Richard, 1995) [in some taxa it is the size of the one of mechanics or physiology, there are two valuable pharynx (Lawrence, 1957)]. Given the tremendous va- consequences of accomplishing a thorough analysis of riety of possible prey items available to a fish on a coral how a functional system works. First, a complete study reef, its feeding performance places discrete boundaries of a system provides a rigorous framework for under- on what it can eat. Thus, the limits of feeding perfor- standing why differences in design have the specific con- mance define a potential feeding niche. sequences for performance that they have. It becomes There is considerable room for further refinement possible to interpret morphological diversity in a per- of this potential niche and it is usually the case that formance landscape. Second, if one understands how a fishes do not feed randomly on the prey that they Ecomorphology of Feeding in Coral Reef Fishes 35 are minimally capable of eating (Wainwright, 1988; into coral reef fishes as yet. Competitive interactions Huckins, 1997). Here again, feeding abilities are a between bluegill and pumpkinseed sunfish in North central factor in determining the ultimate shape of American lakes result in bluegill emerging superior in prey-use curves. Consider the forms of foraging mod- utilizing zooplankton, the preferred prey of both species els that estimate net energy return as a function of (Mittelbach, 1984). However, pumpkinseed sunfish three primary factors: rates