Form and performance: body shape and prey-capture success in four drift-feeding minnows
Abstract
Identifying links between morphology and performance for ecologically relevant tasks will help elucidate the relationships between organismal design and fitness. We conducted a laboratory study to quantify the relationship between variation in body shape and prey-capture success in four drift-feeding minnow species. We offered drifting prey to individual fish in a test flume, counted successful strikes to measure prey-capture success and recorded the position (X, Y coordinates) of ten landmarks on each fish’s outline to delineate the specimen’s form. We then quantified shape variation among species and related it to capture performance through thin-plate spline analysis. Body shape varied significantly among species and with specimen size and was the major determinant of capture success, explaining 45–47% of its variability. Prey-capture success at differing velocities differed among species, but once the effects of shape and size were accounted for, those differences were no longer significant. Allometric shape changes appeared responsible for most of the ontogenetic variation in capture performance, although other size-related, non-shape factors also seemed relevant. Fishes with deeper, shorter bodies, more caudally placed median fins and larger, more upward-pointing mouths exhibited greater capture success than more fusiform fish, suggesting that streamlining, which is energetically advantageous for sustained swimming, entails a cost in terms of prey-capture ability. Our findings demonstrate a strong connection between organismal shape and performance and provide empirical evidence of the cost of morphological specialization for fishes in the drift-feeding functional guild.
Keywords
Ecomorphology Ecologically relevant tasks Morphological costs Stream fishes CyprinidaeNotes
Acknowledgments
We are particularly indebted to R. Ratajczak for his constant help throughout the study. M. Wagner also helped during fieldwork. D.E. Slice provided valuable comments on an earlier draft. This research was funded by USDA McIntire-Stennis grant GEO-0086-MS, National Science Foundation grant BSR-9011661 and the Warnell School of Forestry and Natural Resources. The senior author's stay at the University of Georgia was funded through a travel grant of the Consejería de Educación of the Comunidad Autónoma de Madrid, co-financed by the European Social Fund of the European Union. The manuscript was completed while P.A.R. was supported by a postdoctoral fellowship from the same agency and by a contract of the Ramón y Cajal Program of the Spanish Ministry of Education and Science. M.B. was funded by a predoctoral fellowship from the same institution.
References
- Adams DC, Rohlf FJ (2000) Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proc Natl Acad Sci U S A 97:4106–4111PubMedCrossRefGoogle Scholar
- Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361Google Scholar
- Bachman RA (1984) Foraging behavior of free-ranging wild and hatchery brown trout in a stream. Trans Am Fish Soc 113:1–32CrossRefGoogle Scholar
- Bisson PA, Sullivan K, Nielsen JL (1988) Channel hydraulics, habitat use, and body form of juvenile coho salmon, steelhead, and cutthroat trout in streams. Trans Am Fish Soc 117:262–273CrossRefGoogle Scholar
- Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, CambridgeGoogle Scholar
- Bookstein FL (1996a) Combining the tools of geometric morphometrics. In: Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE (eds) Advances in morphometrics. Plenum Press, New York, pp 131–151Google Scholar
- Bookstein FL (1996b) Standard formula for the uniform shape component in landmark data. In: Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE (eds) Advances in morphometrics. Plenum Press, New York, pp 131–151Google Scholar
- Breder CM Jr (1926) The locomotion of fishes. Zoologica 4:159–291Google Scholar
- Coburn MM, Cavender TM (1993) Interrelationships of North American cyprinid fishes. In: Mayden RL (ed) Systematics, historical ecology and North American freshwater fishes, vol i-xxvi, 1-969. Stanford University Press, Stanford, pp 328–373Google Scholar
- Dewitt TJ, Sih A, Hucko JA (1999) Trait compensation and cospecialization in a freshwater snail: size, shape and antipredator behaviour. Anim Behav 58:397–407PubMedCrossRefGoogle Scholar
- Douglas ME, Matthews WJ (1992) Does morphology predict ecology? Hypothesis testing within a freshwater stream fish assemblage. Oikos 65:213–224CrossRefGoogle Scholar
- Dunham JB, Vinyard GL (1997) Relationships between body mass, population density, and the self-thinning rule in stream-living salmonids. Can J Fish Aquat Sci 54:1025–1030CrossRefGoogle Scholar
- Emerson SB (1978) Allometry and jumping in frogs: helping the twain meet. Evolution 32:551–564CrossRefGoogle Scholar
- Facey DE, Grossman GD (1990) The metabolic cost of maintaining position for four North American stream fishes: effects of season and velocity. Physiol Zool 63:757–776Google Scholar
- Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
- Fraser NHC, Metcalfe NB (1997) The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic salmon. Funct Ecol 11:385–391CrossRefGoogle Scholar
- Freeman MC, Grossman GD (1992a) A field test for competitive interactions among foraging stream fishes. Copeia 1992:898–902CrossRefGoogle Scholar
- Freeman MC, Grossman GD (1992b) Group foraging by a stream minnow: shoals or aggregations? Anim Behav 44:393–403CrossRefGoogle Scholar
- Fulton CJ, Bellwood DR, Wainwright PC (2001) The relationship between swimming ability and habitat use in wrasses (Labridae). Mar Biol 139:25–33CrossRefGoogle Scholar
- Galis F (1993) Morphological constraints on behavior through ontogeny. The importance of developmental constraints. Mar Behav Physiol 23:119–135CrossRefGoogle Scholar
- Grant JWA, Noakes DLG, Jonas KM (1989) Spatial distribution of defence and foraging in young-of-the-year brook charr, Salvelinus fontinalis. J Anim Ecol 58:773–784CrossRefGoogle Scholar
- Grossman GD, Freeman MC (1987) Microhabitat use in a stream fish assemblage. J Zool 212:151–176CrossRefGoogle Scholar
- Grossman GD, Rincón PA, Farr MD, Ratajczak RE Jr (2002) A new optimal foraging model predicts habitat use by drift-feeding stream minnows. Ecol Freshw Fish 11:2–10CrossRefGoogle Scholar
- Harvey PH, Pagel M (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
- Hawkins DK, Quinn TP (1996) Critical swimming velocity and associated morphology of juvenile coastal cutthroat trout (Oncorhynchus clarki clarki), steelhead trout (Oncorhynchus mykiss), and their hybrids. Can J Fish Aquat Sci 53:1487–1496CrossRefGoogle Scholar
- Hernandez LP (2000) Intraspecific scaling of feeding mechanics in an ontogenetic series of zebrafish, Danio rerio. J Exp Biol 203:3033–3043PubMedGoogle Scholar
- Hill J, Grossman GD (1993) An energetic model of microhabitat use for rainbow trout and rosyside dace. Ecology 74:685–698CrossRefGoogle Scholar
- Hughes NF, Dill LM (1990) Position choice by drift-feeding salmonids: model and test for arctic grayling (Thymallus arcticus) in subarctic mountain streams, Interior Alaska. Can J Fish Aquat Sci 47:2039–2048CrossRefGoogle Scholar
- Hughes NF, Kelly LH (1996) A hydrodynamic model for estimating the energetic cost of swimming maneuvers from a description of their geometry and dynamics. Can J Fish Aquat Sci 53:2484–2493CrossRefGoogle Scholar
- James RS, Cole NJ, Davies MLF, Johnston IA (1998) Scaling of intrinsic contractile properties and myofibrillar protein composition of fast muscle in the fish Myoxocephalus scorpius. J Exp Biol 201:901–912PubMedGoogle Scholar
- Jenkins RE, Burkhead NM (1994) Freshwater fishes of Virginia. American Fisheries Society, BethesdaGoogle Scholar
- Kolok AS (1999) Interindividual variation in the prolonged locomotor performance of ectothermic vertebrates: a comparison of fish and herpetofaunal methodologies and a brief review of the recent fish literature. Can J Fish Aquat Sci 56:700–710CrossRefGoogle Scholar
- Lack D (1947) Darwin’s finches. Cambridge University Press, CambridgeGoogle Scholar
- Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667CrossRefGoogle Scholar
- Matthews WJ (1998) Patterns in freshwater fish ecology. Chapman and Hall, LondonGoogle Scholar
- McLaughlin RL (1994) Morphological and behavioural differences among recently-emerged brook charr, Salvelinus fontinalis, foraging in slow- vs. fast-running water. Environ Biol Fish 39:289–300CrossRefGoogle Scholar
- McLaughlin RL, Kramer DL (1991) The association between amount of red muscle and mobility in fishes: a statistical evaluation. Environ Biol Fish 30:369–378CrossRefGoogle Scholar
- McLaughlin RL, Noakes DLG (1998) Going against the flow: an examination of the propulsive movements made by young brook trout in streams. Can J Fish Aquat Sci 55:853–860CrossRefGoogle Scholar
- McMahon TA (1973) Size and shape in biology. Science 179:1201–1204PubMedCrossRefGoogle Scholar
- Menhinick EF (1991) The freshwater fishes of North Carolina. North Carolina Wildlife Resources Commission, RaleighGoogle Scholar
- Mettee MF, O’Neil PE, Pierson JM (1996) Fishes of Alabama and the Mobile basin. Oxmoor House, BirminghamGoogle Scholar
- Miles DB, Ricklefs RE, Travis J (1987) Concordance of ecomorphological relationships in three assemblages of passerine birds. Am Nat 129:347–364CrossRefGoogle Scholar
- Monteiro LR (1999) Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol 48:192–199PubMedCrossRefGoogle Scholar
- Monteiro LR, Bordin B, Furtado dos Reis S (2000) Shape distances, shape spaces and the comparison of morphometric methods. Trends Ecol Evol 15:217–220PubMedCrossRefGoogle Scholar
- Myers RH (1990) Classical and modern regression with applications. Duxbury Press, BelmontGoogle Scholar
- Nakano S, Fausch KD, Kitano S (1999) Flexible niche partitioning via a foraging mode shift: a proposed mechanism for coexistence in stream-dwelling charrs. J Anim Ecol 68:1079–1092CrossRefGoogle Scholar
- Nicieza AG (1995) Morphological variation between geographically disjunct populations of Atlantic salmon: the effects of ontogeny and habitat shift. Funct Ecol 9:448–456CrossRefGoogle Scholar
- Norberg U (1994) Wing design, flight performance and habitat use in bats. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology, vol i-viii, 1-367. University of Chicago Press, Chicago, pp 205–239Google Scholar
- Outten LM (1957) A study of the life history of the cyprinid fish Notropis coccogenis. J Elisha Mitchell Sci Soc 73:68–84Google Scholar
- Outten LM (1974) Additional comparative studies of Cyprinid fishes in the Southeast. J Elisha Mitchell Sci Soc 93:101–102Google Scholar
- Peters RH (1983) The ecological implications of body size. Cambridge University Press, CambridgeGoogle Scholar
- Petterson LB, Brönmark C (1999) Energetic consequences of an inducible morphological defence in crucian carp. Oecologia 121:12–18CrossRefGoogle Scholar
- Reisen WK (1972) The influence of organic drift on the food habits and life history of the yellowfin shiner, Notropis lutipinnis, (Jordan and Brayton). Am Midl Nat 88:376–383CrossRefGoogle Scholar
- Richard BA, Wainwright PC (1995) Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): I. Kinematics of prey capture. J Exp Biol 198:419–433PubMedGoogle Scholar
- Ricklefs RE, Miles DB (1994) Ecological and evolutionary inferences from morphology: an ecological perspective. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology, vol i-viii, 1–367. University of Chicago Press, Chicago, pp 13–41Google Scholar
- Rincón PA, Grossman GD (2001) Intraspecific aggression in rosyside dace, a drift-feeding stream cyprinid. J Fish Biol 59:968–986CrossRefGoogle Scholar
- Rincón PA, Lobón-Cerviá J (2002) Non-linear self-thinning in a stream-resident population of brown trout (Salmo trutta). Ecology 83:1808–1816CrossRefGoogle Scholar
- Robinson BW, Wilson DS, Margosian AS (2000) A pluralistic analysis of character displacement in pumpkinseed sunfish (Lepomis gibbosus). Ecology 81:2799–2812CrossRefGoogle Scholar
- Rohlf FJ (1991) Relative warp analysis and an example of its application to mosquito wings. In: Marcus LF, Bello E, Garcia-Valdecasas A (eds) Contributions to morphometrics Museo Nacional de Ciencias Naturales, Madrid, pp 131–159Google Scholar
- Rohlf FJ. TpsRegr, Version 1.26. [1.26] (2000) Stony Brook, New York, Department of Ecology and Evolution, State University of New York at Stony BrookGoogle Scholar
- Rohlf FJ. TpsDig, Version 1.30. [1.30] (2001) Stony Brook, New York, Department of Ecology and Evolution, State University of New York at Stony BrookGoogle Scholar
- Rohlf FJ. TpsSpline, Version 1.19. [1.19] (2002) Stony Brook, New York, Department of Ecology and Evolution, State University of New York at Stony BrookGoogle Scholar
- Rohlf FJ, Marcus LF (1993) A revolution in morphometrics. Trends Ecol Evol 8:129–132CrossRefGoogle Scholar
- Rohlf FJ, Slice DE (1990) Extension of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59CrossRefGoogle Scholar
- Schaefer JF, Lutterschmidt WI, Hill LG (1999) Physiological performance and stream microhabitat use by the centrarchids Lepomis megalotis and Lepomis macrochirus. Environ Biol Fish 54:303–312CrossRefGoogle Scholar
- Scheiner SM (1993) MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, vol i-xiv, 1-445. Chapman & Hall, New York, pp 94–112Google Scholar
- Schmidt-Nielsen K (1984) Scaling: why is animal size so important? Cambridge University Press, CambridgeGoogle Scholar
- Sidell BD, Moerland TS (1989) Effects of temperature on muscular function and locomotory performance in teleost fish. Adv Comput Environ Physiol 5:116–156Google Scholar
- Slice DE. Morpheus et al.: software for morphometric research. Revision 01-30-98 (1998) Stony Brook, New York, Department of Ecology and Evolution, State University of New YorkGoogle Scholar
- StatSoft I. STATISTICA (data analysis software system), version 6. http://www.statsoft.com (2001) Tulsa, StatSoft, Inc
- Svanbäck R, Eklöv P (2002) Effects of habitat and food resources on morphology and ontogenetic growth trajectories in perch. Oecologia 131:61–70CrossRefGoogle Scholar
- Taylor EB (1988) Water temperature and velocity as determinants of microhabitats of juvenile chinook and coho salmon in a laboratory stream channel. Trans Am Fish Soc 117:22–28CrossRefGoogle Scholar
- Taylor EB, Foote CJ (1991) Critical swimming velocities of juvenile sockeye salmon and kokanee, the anadromous and non-anadromous forms of Oncorhynchus nerka (Walbaum). J Fish Biol 38:407–419CrossRefGoogle Scholar
- Taylor EB, McPhail JD (1985a) Variation in body morphology among British Columbia populations of coho salmon, Oncorhynchus kisutch. Can J Fish Aquat Sci 42:2020–2028Google Scholar
- Taylor EB, McPhail JD (1985b) Variation in burst and prolonged swimming performance among British Columbia populations of coho salmon, Oncorhynchus kisutch. Can J Fish Aquat Sci 42:2029–2033Google Scholar
- Taylor EB, McPhail JD (1986) Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus. Can J Zool 64:416–420CrossRefGoogle Scholar
- Thomas AE, Donahoo MJ (1977) Differences in swimming performance among strains of rainbow trout (Salmo gairdneri). J Fish Res Board Can 34:304–306Google Scholar
- Tyler JA (1993) Effects of water velocity, group size, and prey arrival rate on the capture efficiency of stream-drift by Rhinichthys atratulus. Can J Fish Aquat Sci 50:1055–1061CrossRefGoogle Scholar
- Tyler JA, Gilliam JF (1995) Ideal free distributions of stream fish: a model and test with minnows, Rhinichthys atratulus. Ecology 76:580–592CrossRefGoogle Scholar
- Vogel S (1994) Life in moving fluids. Princeton University Press, PrincetonGoogle Scholar
- Wainwright PC (1994) Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology, vol i-viii, 1-367. University of Chicago Press, Chicago, pp 42–59Google Scholar
- Wainwright PC, Reilly SM (1994) Ecological morphology: integrative organismal biology. University of Chicago Press, ChicagoGoogle Scholar
- Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50CrossRefGoogle Scholar
- Webb PW (1983) Speed, acceleration and manoeuverability of two teleost fishes. J Exp Biol 102:115–122:115–1222Google Scholar
- Webb PW (1984a) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120Google Scholar
- Webb PW (1984b) Form and function in fish swimming. Sci Am 251:58–68CrossRefGoogle Scholar
- Webb PW (1991) Composition and mechanics of routine swimming of rainbow trout, Oncorhynchus mykiss. Can J Fish Aquat Sci 48:583–590CrossRefGoogle Scholar
- Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:394–425CrossRefGoogle Scholar
- Wilzbach MA, Cummins KW (1986) Influence of habitat manipulations on interactions between cutthroat trout and invertebrate drift. Ecology 67:898–911CrossRefGoogle Scholar
- Winans GA (1984) Multivariate morphometric variability in Pacific salmon: technical demonstration. Can J Fish Aquat Sci 41:1150–1159CrossRefGoogle Scholar
- Wood BM, Bain MB (1995) Morphology and microhabitat use in stream fish. Can J Fish Aquat Sci 52:1487–1498CrossRefGoogle Scholar
- Zar JH (1996) Biostatistical analysis. Prentice Hall, New JerseyGoogle Scholar