Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes

Coral Reefs - Tập 30 - Trang 415-428 - 2011
L. Schmitz1, P. C. Wainwright1,2
1Department of Evolution and Ecology, University of California, Davis, USA
2Center for Population Biology, University of California, Davis, USA

Tóm tắt

Zooplanktivory is one of the most distinct trophic niches in coral reef fishes, and a number of skull traits are widely recognized as being adaptations for feeding in midwater on small planktonic prey. Previous studies have concluded that zooplanktivores have larger eyes for sharper visual acuity, reduced mouth structures to match small prey sizes, and longer gill rakers to help retain captured prey. We tested these three traditional hypotheses plus two novel adaptive hypotheses in labrids, a clade of very diverse coral reef fishes that show multiple independent evolutionary origins of zooplanktivory. Using phylogenetic comparative methods with a data set from 21 species, we failed to find larger eyes in three independent transitions to zooplanktivory. Instead, an impression of large eyes may be caused by a size reduction of the anterior facial region. However, two zooplanktivores (Clepticus parrae and Halichoeres pictus) possess several features interpreted as adaptations to zooplankton feeding, namely large lens diameters relative to eye axial length, round pupil shape, and long gill rakers. The third zooplanktivore in our analysis, Cirrhilabrus solorensis, lacks all above features. It remains unclear whether Cirrhilabrus shows optical specializations for capturing planktonic prey. Our results support the prediction that increased visual acuity is adaptive for zooplanktivory, but in labrids increases in eye size are apparently not part of the evolutionary response.

Tài liệu tham khảo

Alfaro M, Brock CD, Banbury B, Wainwright PC (2009) Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evol Biol 9:255 Baensch HA, Debelius H (1994) Baensch marine atlas, volume 1. Microcosm, Shelburne Barel CDN (1982) Towards a constructional morphology of cichlid fishes. Neth J Zool 33:357–424 Baumgartner HA, Bell MA, Weiberg PH (1988) Body form differences between the Enos Lake species pair of threespine sticklebacks (Gasterosteus aculeatus complex). Can J Zool 66:467–474 Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more liable. Evolution 57:717–745 Collin SP, Pettigrew JD (1989) Quantitative comparison of the limits of visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behav Evol 34:184–192 Cooper WJ, Westneat MW (2009) Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. BMC Evol Biol 9:24 Cowman, Bellwood DR, van Herwerden L (2009) Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs. Mol Phylogenet Evol 52:621–631 Davis WP, Birdsong RS (1973) Coral reef fishes which forage in the water column. Helgol Wiss Meeresunters 24:292–306 Douglas RH, Hawryshyn CW (1990) Behavioral studies of fish vision: an analysis of visual capabilities. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 373–418 Drenner RW, Mummert JR, deNoyelles F Jr, Kettle D (1984) Selective particle ingestion by a filter-feeding fish and its impact on phytoplankton community structure. Limnol Oceanogr 29:941–948 Dullemeijer P, Barel CDN (1977) Functional morphology and evolution. In: Hecht M, Goody P, Hecht B (eds) Major patterns in vertebrate evolution. NATO Adv Study Inst Ser A 14, pp 83–117 Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15 Fernald RD (1990) The optical system of fishes. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 45–62 Fernald RD, Wright SE (1985) Growth of the visual system in the African cichlid fish, Haplochromis burtoni. Vision Res 25:163–170 Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa: their biology and evolution. Oliver and Boyd, Edinburgh Gerber RP, Marshall N (1974) Ingestion of detritus by the lagoon pelagic community at Eniwetok Atoll. Limnol Oceanogr 19:815–824 Goatley CHR, Bellwood D (2009) Morphological structure in a reef fish assemblage. Coral Reefs 28:449–457 Gomon MF (2001) Descriptions of two new species of Bodianus (Perciformes: Labridae) from Australasian waters. N Z J Zool 28:407–416 Gomon MF (2006) A revision of the labrid fish genus Bodianus with descriptions of eight new species. Rec Aust Mus Suppl 30:1–133 Hairston NG, Li KT, Easter SS (1982) Fish vision and the detection of planktonic prey. Science 218:1240–1242 Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131 Hart PJB, Gill AB (1994) Evolution of foraging behavior in the threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford Hobson ES (1991) Trophic relationships of fishes specialized to feed on zooplankters above coral reefs. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 69–95 Hobson ES, Chess JR (1976) Trophic interactions among fishes and zooplankters nearshore at Santa Catalina Island, California. Fish Bull 74:567–598 Hobson ES, Chess JR (1978) Trophic relationships among fishes and plankton in the lagoon at Enewetak Atoll, Marshall Islands. Fish Bull 76:133–153 Hughes A (1977) The topography of vision in mammals of contrasting life style: comparative optics and retinal organisation. In: Crescitelli F (ed) The visual system in vertebrates. Springer-Verlag, Berlin, Heidelberg, New York, pp 613–756 Hulsey CD, Mims MC, Streelman JT (2007) Do constructional constraints influence cichlid craniofacial diversification? Proc R Soc B 274:1867–1875 Hung GK, Ciuffreda KJ (2002) Models of the visual system. Springer, Berlin, Heidelberg, New York Ingram T, Shurin JB (2009) Trait-based assembly and phylogenetic structure in northeast Pacific rockfish assemblage. Ecology 90:2444–2453 Job SD, Bellwood DR (2000) Light sensitivity in larval fishes: implications for vertical zonation in the pelagic zone. Limnol Oceanogr 45:362–371 Johnsen S (2001) Hidden in plain sight: the ecology and physiology of organismal transparency. Biol Bull 201:301–318 Kassam DD, Adams DC, Ambali AJD, Yamaoka K (2003) Body shape variation in relation to resource partitioning within cichlid trophic guilds coexisting along the rocky shore of Lake Malawi. Anim Biol 53:59–70 Kazancioğlu E, Near TJ, Hanel R, Wainwright PC (2009) Influence of sexual selection and feeding functional morphology on diversification rate of parrotfishes (Scaridae). Proc R Soc, B 276:3439–3446 Kiltie RA (2000) Scaling of visual acuity with body size in mammals and birds. Funct Ecol 14:226–234 Kröger RHH, Fritsches KA, Warrant EJ (2009) Lens optical properties in the eyes of large marine predatory teleosts. J Comp Physiol A 195:175–182 Land MF (1981) Optics and vision in invertebrates. In: Land MF, Laughlin SB, Naessel DR, Strausfeld NJ, Waterman TH (eds) Comparative physiology and evolution of vision in invertebrates B: invertebrate visual centers and behavior I. Springer-Verlag, Berlin, Heidelberg, New York, pp 471–592 Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, Oxford Langeland A, Nøst T (1995) Gill raker structure and selective predation on zooplankton by particulate feeding fish. J Fish Biol 47:719–732 Langerhans RB, Layman CA, Langerhans AK, Dewitt TJ (2003) Habitat-associated morphological divergence in two Neotropical fish species. Biol J Linn Soc 80:689–698 Loew ER, McFarland WN (1990) The underwater visual environment. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 1–43 Lythgoe JN (1979) The ecology of vision. Clarendon Press, Oxford Magnuson JJ, Heitz JG (1971) Gill raker apparatus and food selectivity among mackerels, tunas, and dolphins. Fish Bull 69:361–370 Maindonald J, Braun WJ (2009) DAAG: data analysis and graphics data and functions. R package version 1.01. http://CRAN.R-project.org/package=DAAG Marshall NB (1979) Developments in deep-sea biology. Blandford Press, Poole, Dorset McPeek MA (1995) Testing hypotheses about evolutionary change on single branches of a phylogeny using evolutionary contrasts. Am Nat 145:686–703 McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can J Zool 62:1402–1408 Miller WH (1979) Intraocular filters. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates A: invertebrate photoreceptors. Springer-Verlag, Berlin, Heidelberg, New York, pp 69–143 Motta PJ (1988) Functional morphology of the feeding apparatus of ten species of Pacific butterflyfishes (Perciformes, Chaetodontidae): an ecomorphological approach. Environ Biol Fish 22:39–67 Mundy BC (2005) Checklist of the fishes of the Hawaiian Archipelago. Bishop Mus Bull Zool 6:1–704 Pankhurst NW (1989) The relationship of ocular morphology to feeding modes and activity periods in shallow marine teleosts from New Zealand. Environ Biol Fishes 26:201–211 Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290 Parenti P, Randall JE (2000) An annotated checklist of the species of the labroid fish families Labridae and Scaridae. Ichthyol Bull JLB Smith Inst Ichthyol 68:1–97 R Development Core Team (2010) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:655–847 Randall JE (1983) Caribbean reef fishes. TFH Publications, Neptune City, NJ Randall JE (2005) Reef and shore fishes of the South Pacific. University of Hawaii Press, Honolulu Randall JE, Lubbock R (1981) Labrid fishes of the genus Paracheilinus, with descriptions of three new species from the Philippines. Jpn J Ichthyol 28:19–30 Randall JE, Nagareda BH (2002) Cirrhilabrus bathyphilus, a new deep-dwelling labrid fish from the Coral Sea. Cybium 26:123–127 Revell LJ (2009) Size-correction and principal components for interspecific comparative studies. Evolution 63:3258–3268 Robinson BW, Parsons KJ (2002) Changing times, spaces and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Can J Fish Aquat Sci 59:1819–1833 Schluter D (1993) Adaptive radiation in sticklebacks: size, shape and habitat use efficiency. Ecology 74:699–709 Schmitz L (2009) Quantitative estimates of visual performance features in fossil birds. J Morph 270:759–773 Schmitz L, Motani R (2010) Morphological differences between the eyeballs of nocturnal and diurnal amniotes revisited from optical perspectives of visual environments. Vision Res 50:936–946 Siebeck UE, Marshall NJ (2007) Potential ultraviolet vision in pre-settlement larvae and settled reef fish—a comparison across 23 families. Vision Res 47:2337–2352 Sivak JG (1978) The functional significance of the aphakic space of the fish eye. Can J Zool 56:513–516 Sivak JG (1990) Optical variability in the fish lens. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 63–108 Strauss RE (1984) Allometry and functional feeding morphology in haplochromine cichlids. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. Univ Maine Press, ME, pp 217–230 Wainwright PC (1988) Morphology and ecology: the functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69:635–645 Wainwright PC, Bellwood DR (2002) Ecomorphology of feeding in coral reef fishes. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 33–55 Wainwright PC, Richard BA (1995) Predicting patterns of prey use from morphology of fishes. Env Biol Fish 44:97–113 Wainwright PC, Bellwood DR, Westneat MW (2002) Ecomorphology of locomotion in labrid fishes. Environ Biol Fish 65:47–62 Wainwright PC, Bellwood DR, Westneat MW, Grubich JR, Hoey AS (2004) A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biol J Linn Soc 82:1–25 Walls GL (1942) The vertebrate eye and its adaptive radiation. Hafner Pub Co, New York Warrant EJ (2004) Vision in the dimmest habitats on earth. J Comp Physiol A 190:765–789 Warrant EJ, Locket NA (2004) Vision in the dep sea. Biol Rev 79:671–712 Warton D, and translated to R by Ormerod J (2007). smatr: (standardised) major axis estimation and testing routines. R package version 2.1. http://web.maths.unsw.edu.au/~dwarton Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291 Weitkamp DE, Sullivan RD (1939) Fishes. The John Murray expedition 1933–1934. Sci Rep John Murray Exped 7:1–116 Westneat MW (1995) Feeding, function, and phylogeny: analysis of historical biomechanics in labrid fishes using comparative methods. Syst Biol 44:361–383 Westneat MW, Alfaro ME (2005) Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Mol Phylogenet Evol 36:370–390 Westneat MW, Alfaro ME, Wainwright PC, Bellwood DR, Grubich JR, Fessler J, Clements KD, Smith L (2005) Repeated convergence of skull biomechanics in coral reef fishes. Proc R Soc B 272:993–1000