Marine Biology

, 164:215 | Cite as

Habitat-dependent niche partitioning between colour morphs of the algal-dwelling shrimp Hippolyte obliquimanus

  • Rafael C. Duarte
  • Augusto A. V. Flores
  • Catarina Vinagre
  • Miguel C. Leal
Original paper


Trait-based differences among individuals are common and particularly important for polymorphic species in which alternative morphs exploit the same habitat types but occupy different trophic niches. The shrimp Hippolyte obliquimanus inhabits shallow-water vegetated habitats, particularly the seasonal and physically complex brown alga Sargassum furcatum and the less-structured but temporally stable red weed Galaxaura marginata. Two main colour morphs can be found in these habitats: homogeneous colour-changing shrimp that are able to match to their background and show little mobility, and transparent shrimp with coloured stripes, which cannot match their background, show lower habitat fidelity and are more evenly distributed between algal habitats. We used carbon and nitrogen stable isotopes and Bayesian mixing models to test whether morph-specific patterns of habitat use observed for H. obliquimanus living in Sargassum and Galaxaura meadows also influence trophic niche segregation. We observed morph-specific trophic differences that varied with habitat, with narrower niche space and lower niche overlap between morphs in Galaxaura meadows, and broader niche space and higher niche overlap between morphs in Sargassum habitat. Niche segregation between morphs occurred only in Galaxaura, where available resources are presumably less abundant than in Sargassum and the strength of competition between morphs is higher. Resource availability and habitat stability are likely driving dietary niche segregation between shrimp morphs, which can ultimately affect population dynamics and community composition in a spatially heterogeneous and seasonal habitat.



We are grateful to Maria Fernanda Morrison for her help on sample processing and to Inês Carvalho for preparation of stable isotope analyses. We thank Márcio Araújo and two anonymous referees for helpful comments on the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


This study was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP (2012/17003-0), which granted a PhD fellowship to RCD. This is a contribution of the Research Centre for Marine Biodiversity of the University of São Paulo (NP‐Biomar/USP).

Ethical approval

All sampling and experimental procedures used in this study comply with the current laws of Brazilian legislation.


  1. Ahnesjö J, Forsman A (2006) Differential habitat selection by pygmy grasshopper color morphs; interactive effects of temperature and predator avoidance. Evol Ecol 20:235–257. doi: 10.1007/s10682-006-6178-8 CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x Google Scholar
  3. Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958. doi: 10.1111/j.1461-0248.2011.01662.x CrossRefGoogle Scholar
  4. Bearhop S, Adams CE, Waldron S et al (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012. doi: 10.1111/j.0021-8790.2004.00861.x CrossRefGoogle Scholar
  5. Bessa F, Baeta A, Marques JC (2014) Niche segregation amongst sympatric species at exposed sandy shores with contrasting wrack availabilities illustrated by stable isotopic analysis. Ecol Ind 36:694–702. doi: 10.1016/j.ecolind.2013.09.026 CrossRefGoogle Scholar
  6. Bolnick DI (2001) Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature 410:463–466. doi: 10.1038/35068555 CrossRefGoogle Scholar
  7. Bolnick DI, Svanbäck R, Fordyce JA et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. doi: 10.1086/343878 CrossRefGoogle Scholar
  8. Bolnick DI, Amarasekare P, Araújo MS, Bürger R et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192CrossRefGoogle Scholar
  9. Booth CL (1990) Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40:125–163. doi: 10.1111/j.1095-8312.1990.tb01973.x CrossRefGoogle Scholar
  10. Bourke P, Magnan P, Rodríguez M, Rodriguez MA (1997) Individual variations in habitat use and morphology in brook charr. J Fish Biol 51:783–794. doi: 10.1111/j.1095-8649.1997.tb01999.x CrossRefGoogle Scholar
  11. Caro T, Sherratt TN, Stevens M (2016) The ecology of multiple colour defences. Evol Ecol 30:797–809. doi: 10.1007/s10682-016-9854-3 CrossRefGoogle Scholar
  12. Correa SB, Winemiller KO (2014) Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest. Ecology 95:210–224. doi: 10.1890/13-0393.1 CrossRefGoogle Scholar
  13. Duarte RC, Flores AAV (2017) Morph-specific habitat and sex distribution in the caridean shrimp Hippolyte obliquimanus. J Mar Biol Assoc UK 97:235–242. doi: 10.1017/S0025315416000230 Google Scholar
  14. Duarte RC, Stevens M, Flores AAV (2016) Shape, colour plasticity, and habitat use indicate morph-specific camouflage strategies in a marine shrimp. BMC Evol Biol 16:218. doi: 10.1186/s12862-016-0796-8 CrossRefGoogle Scholar
  15. Forsman A, Ahnesjö J, Caesar S, Karlsson M (2008) A model of ecological and evolutionary consequences of color polymorphism. Ecology 89:34–40. doi: 10.1890/07-0572.1 CrossRefGoogle Scholar
  16. Fry B (1999) Using stable isotopes to monitor watershed influences on aquatic trophodynamics. Can J Fish Aquat Sci 56:2167–2171. doi: 10.1139/f99-152 CrossRefGoogle Scholar
  17. Godoy EAS, Coutinho R (2002) Can artificial beds of plastic mimics compensate for seasonal absence of natural beds of Sargassum furcatum? ICES J Mar Sci 59:111–115. doi: 10.1006/jmsc.2002.1220 CrossRefGoogle Scholar
  18. González-Solís J, Oro D, Jover L et al (1997) Trophic niche width and overlap of two sympatric gulls in the southwestern Mediterranean. Oecologia 112:75–80. doi: 10.1007/s004420050285 CrossRefGoogle Scholar
  19. Hall M, Bell S (1988) Response of small motile epifauna to complexity of epiphytic algae on seagrass blades. J Mar Res 46:613–630. doi: 10.1357/002224088785113531 CrossRefGoogle Scholar
  20. Herder F, Pfaender J, Schliewen UK (2008) Adaptive sympatric speciation of polychromatic “roundfin” sailfin silverside fish in Lake Matano (Sulawesi). Evolut (N Y) 62:2178–2195. doi: 10.1111/j.1558-5646.2008.00447.x Google Scholar
  21. Howard R (1984) The trophic ecology of caridean shrimps in an eelgrass community. Aquat Bot 18:155–174. doi: 10.1016/0304-3770(84)90085-8 CrossRefGoogle Scholar
  22. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. doi: 10.1111/j.1365-2656.2011.01806.x CrossRefGoogle Scholar
  23. Jacobucci GB, Leite FPP (2014) The role of epiphytic algae and different species of Sargassum in the distribution and feeding of herbivorous amphipods. Lat Am J Aquat Res 42:353–363. doi: 10.3856/vol42-issue2-fulltext-6 CrossRefGoogle Scholar
  24. Jacobucci GB, Tanaka MO, Leite FPP (2009) Factors influencing temporal variation of a Sargassum filipendula (Phaeophyta: Fucales) bed in a subtropical shore. J Mar Biol Assoc UK 89:315. doi: 10.1017/S0025315409002306 CrossRefGoogle Scholar
  25. Jormalainen V, Tuomi J (1989) Sexual differences in habitat selection and activity of the colour polymorphic isopod Idotea baltica. Anim Behav 38:576–585. doi: 10.1016/S0003-3472(89)80002-8 CrossRefGoogle Scholar
  26. Kadye WT, Chakona A, Jordaan MS (2016) Swimming with the giant: coexistence patterns of a new redfin minnow Pseudobarbus skeltoni from a global biodiversity hot spot. Ecol Evol 6:7141–7155. doi: 10.1002/ece3.2328 CrossRefGoogle Scholar
  27. Karpestam E, Forsman A (2011) Dietary differences among colour morphs of pygmy grasshoppers revealed by behavioural experiments and stable isotopes. Evol Ecol Res 13:461–477Google Scholar
  28. Komada T, Anderson MR, Dorfmeier CL (2008) Carbonate removal from coastal sediments for the determination of organic carbon and its isotopic signatures, δ13C and ∆14C: comparison of fumigation and direct acidification by hydrochloric acid. Limnol Oceanogr Methods 6:254–262. doi: 10.4319/lom.2008.6.254 CrossRefGoogle Scholar
  29. Kusche H, Elmer KR, Meyer A (2015) Sympatric ecological divergence associated with a color polymorphism. BMC Biol 13:82. doi: 10.1186/s12915-015-0192-7 CrossRefGoogle Scholar
  30. Lattanzio MS, Miles DB (2014) Ecological divergence among colour morphs mediated by changes in spatial network structure associated with disturbance. J Anim Ecol 83:1490–1500. doi: 10.1111/1365-2656.12252 CrossRefGoogle Scholar
  31. Lattanzio MS, Miles DB (2016) Trophic niche divergence among colour morphs that exhibit alternative mating tactics. R Soc Open Sci 3:150531. doi: 10.1098/rsos.150531 CrossRefGoogle Scholar
  32. Leite F, Turra A (2003) Temporal variation in Sargassum biomass, Hypnea epiphytism and associated fauna. Braz Arch Biol Technol 46:665–671. doi: 10.1590/S1516-89132003000400021 CrossRefGoogle Scholar
  33. MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385. doi: 10.1086/282505 CrossRefGoogle Scholar
  34. Maerz JC, Myers EM, Adams DC (2006) Trophic polymorphism in a terrestrial salamander. Evol Ecol Res 8:23–35Google Scholar
  35. Martin-Smith KM (1993) Abundance of mobile epifauna: the role of habitat complexity and predation by fishes. J Exp Mar Biol Ecol 174:243–260. doi: 10.1016/0022-0981(93)90020-O CrossRefGoogle Scholar
  36. May RM (1973) On relationships among various types of population models. Am Nat 107:46–57. doi: 10.2307/2459565 CrossRefGoogle Scholar
  37. Merilaita S, Jormalainen V (1997) Evolution of sex differences in microhabitat choice and colour polymorphism in Idotea baltica. Anim Behav 54:769–778. doi: 10.1006/anbe.1996.0490 CrossRefGoogle Scholar
  38. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140. doi: 10.1016/0016-7037(84)90204-7 CrossRefGoogle Scholar
  39. Muschick M, Indermaur A, Salzburger W (2012) Convergent evolution within an adaptive radiation of cichlid fishes. Curr Biol 22:2362–2368. doi: 10.1016/j.cub.2012.10.048 CrossRefGoogle Scholar
  40. Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83. doi: 10.1146/annurev.ento.43.1.63 CrossRefGoogle Scholar
  41. Parnell A (2016) Simmr: a stable isotope mixing model. Accessed 19 Nov 2016
  42. Parnell AC, Phillips DL, Bearhop S et al (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399. doi: 10.1002/env.2221 Google Scholar
  43. Phillips DL (2012) Converting isotope values to diet composition: the use of mixing models. J Mammal 93:342–352. doi: 10.1644/11-MAMM-S-158.1 CrossRefGoogle Scholar
  44. Phillips DL, Inger R, Bearhop S et al (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 835:823–835. doi: 10.1139/cjz-2014-0127 CrossRefGoogle Scholar
  45. Pianka ER (1981) Competition and niche theory. Theor Ecol 8:167–196. doi: 10.1002/jlac.1993199301120 Google Scholar
  46. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. doi: 10.2307/3071875 CrossRefGoogle Scholar
  47. Power M, O’Connell MF, Dempson JB (2005) Ecological segregation within and among Arctic char morphotypes in Gander Lake, Newfoundland. Environ Biol Fishes 73:263–274. doi: 10.1007/s10641-005-2137-4 CrossRefGoogle Scholar
  48. R Development Core Team (2016) R: a language and environment for statistical computing. Accessed 22 Oct 2015
  49. Ricklefs RE, Nealen P (1998) Lineage-dependent rates of evolutionary diversification: analysis of bivariate ellipses. Funct Ecol 12:871–885. doi: 10.1046/j.1365-2435.1998.00263.x CrossRefGoogle Scholar
  50. Rossi F, Olabarria C, Incera M, Garrido J (2010) The trophic significance of the invasive seaweed Sargassum muticum in sandy beaches. J Sea Res 63:52–61. doi: 10.1016/j.seares.2009.09.005 CrossRefGoogle Scholar
  51. Roughgarden J (1974) Niche width: biogeographic patterns among Anolis lizard populations. Am Nat 108:429–442. doi: 10.1086/282924 CrossRefGoogle Scholar
  52. Russo AR (1990) The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194:1–12. doi: 10.1007/BF00012107 CrossRefGoogle Scholar
  53. Ruxton G, Sherratt T, Speed M (2004) Avoiding attack. Oxford University Press, OxfordCrossRefGoogle Scholar
  54. Sebastiano S, Antonio R, Fabrizio O et al (2012) Different season, different strategies: feeding ecology of two syntopic forest-dwelling salamanders. Acta Oecol 43:42–50. doi: 10.1016/j.actao.2012.05.001 CrossRefGoogle Scholar
  55. Silva LS, Miranda LB, Castro Filho BM (2005) Numerical study of circulation and thermohaline structure in the São Sebastião channel. Rev Braz Geofish 23:407–425. doi: 10.1590/S0102-261X2005000400005 Google Scholar
  56. Soberon J, Nakamura M (2009) Niches and distributional areas. Concepts, methods, and assumptions. Proc Natl Acad Sci USA 106:19644–19650CrossRefGoogle Scholar
  57. Stevens M, Lown AE, Wood LE (2014) Camouflage and individual variation in shore crabs (Carcinus maenas) from different habitats. PLoS One 9:1–31. doi: 10.1371/journal.pone.0115586 Google Scholar
  58. Strong DR (1982) Harmonious coexistence of hispine beetles on Heliconia in experimental and natural communities. Ecology 63:1039–1049. doi: 10.2307/1937243 CrossRefGoogle Scholar
  59. Stuart-Fox D, Moussalli A (2009) Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philos Trans R Soc Lond B Biol Sci 364:463–470. doi: 10.1098/rstb.2008.0254 CrossRefGoogle Scholar
  60. Svanbäck R, Bolnick DI (2005) Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evol Ecol Res 7:993–1012Google Scholar
  61. Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc B Biol Sci 274:839–844. doi: 10.1098/rspb.2006.0198 CrossRefGoogle Scholar
  62. Svanbäck R, Eklöv P (2002) Effects of habitat and food resources on morphology and ontogenetic growth trajectories in perch. Oecologia 131:61–70. doi: 10.1007/s00442-001-0861-9 CrossRefGoogle Scholar
  63. Tinker MT, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Natl Acad Sci USA 105:560–565. doi: 10.1073/pnas.0709263105 CrossRefGoogle Scholar
  64. Todd P, Briers R, Ladle R, Middleton F (2006) Phenotype-environment matching in the shore crab (Carcinus maenas). Mar Biol 148:1357–1367. doi: 10.1007/s00227-005-0159-2 CrossRefGoogle Scholar
  65. Zalewski M, Dudek-Godeau D, Tiunov AV et al (2015) Wing morphology is linked to stable isotope composition of nitrogen and carbon in ground beetles (Coleoptera: Carabidae). Eur J Entomol 112:810–817. doi: 10.14411/eje.2015.072 Google Scholar
  66. Zupo V, Nelson W (1999) Factors influencing the association patterns of Hippolyte zostericola and Palaemonetes intermedius (Decapoda: Natantia) with seagrasses of the Indian River Lagoon, Florida. Mar Biol 134:181–190. doi: 10.1007/s002270050536 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Centro de Biologia MarinhaUniversidade de São PauloSão SebastiãoBrazil
  2. 2.Programa de Pós-Graduação em Biologia Comparada, Faculdade de Filosofia, Ciências e Letras de Ribeirão PretoUniversidade de São PauloRibeirão PretoBrazil
  3. 3.MARE - Marine and Environmental Sciences Centre, Faculdade de Ciências da Universidade de LisboaLisbonPortugal
  4. 4.Department of Fish Ecology and Evolution, Center for Ecology, Evolution and BiogeochemistryEawag: Swiss Federal Institute of Aquatic Science and TechnologyKastanienbaumSwitzerland

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