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Marine Biology

, 166:55 | Cite as

Testing the importance of predation refuge vs. food quality in determining the use of macroalgal hosts by a generalist marine mesograzer

  • Glauco B. O. MachadoEmail author
  • Ana P. Ferreira
  • Fosca P. P. Leite
Original paper

Abstract

Bottom-up (e.g. resource quality) and top-down (e.g. predation) factors have strong effects on the fitness and distribution of small herbivores. Herein, we investigated how food quality and refuge offered by macroalgal hosts influence the distribution of a mesograzer. We used the herbivorous amphipod Cymadusa filosa and seasonally evaluated its association with the macroalgal hosts Sargassum filipendula, Padina gymnospora, and Dichotomaria marginata on a subtropical rocky shore from the Brazilian southeastern coast. Feeding experiments were conducted to test the food value of hosts, while predation experiments in the field and laboratory were performed to investigate the refuge value of the macroalgae. Cymadusa occurred on Padina in a density greater than that observed on Dichotomaria and Sargassum, while Dichotomaria harbored more amphipods than Sargassum. Adults of Cymadusa showed a higher consumption of Padina and Sargassum in both choice and no-choice feeding experiments and juveniles had greater growth and reproductive potential when feeding on such macroalgae. In the predation experiment in the field, Padina was a better refuge for Cymadusa than Sargassum. However, no difference in refuge value among hosts was observed in the laboratory assays. The distribution of Cymadusa was explained by a balance between food and refuge values of hosts, with higher abundances being observed in the high-quality food alga that provides refuge against predators (e.g. Padina), while fewer individuals occurred in other high-quality food that was less suitable as refuge (e.g. Sargassum). Therefore, predation may be more of a determinant for distribution of that mesograzer than resource quality.

Notes

Acknowledgements

We thank Aline Neufeld and Silvana Siqueira for assistance with field and laboratory work. We thank Marília Bueno, Pedro Bergamo, Edson Vieira and Bruno Rodrigues da Silva for their valuable comments. We are very grateful to the reviewers for their valuable comments and suggestions. This work was financially supported by the São Paulo Research Foundation (FAPESP) Grant to GBO Machado (No. 2013/17629-9).

Funding

This study was financially supported by the São Paulo Research Foundation (FAPESP) Grant to GBO Machado (No. 2013/17629-9).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  1. Appadoo C, Myers AA (2004) Reproductive bionomics and life history traits of three gammaridean amphipods, Cymadusa filosa Savigny, Ampithoe laxipodus Appadoo and Myers and Mallacoota schellenbergi Ledoyer from the tropical Indian Ocean (Mauritius). Acta Oecol 26:227–238.  https://doi.org/10.1016/j.actao.2004.06.002 CrossRefGoogle Scholar
  2. Barnard JL (1965) Marine amphipoda of atolls in Micronesia. Proc US Natl Mus 117:459–551CrossRefGoogle Scholar
  3. Beermann J, Boos K, Gutow L, Boersma M, Peralta AC (2018) Combined effects of predator cues and competition define habitat choice and food consumption of amphipod mesograzers. Oecologia 186:645–654.  https://doi.org/10.1007/s00442-017-4056-4 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bell TM, Sotka EE (2012) Local adaptation in adult feeding preference and juvenile performance on the generalist herbivore Idotea balthica. Oecologia 170:383–393.  https://doi.org/10.1007/s00442-012-2302-3 CrossRefPubMedGoogle Scholar
  5. Berthelsen AK, Taylor RB (2014) Arthropod mesograzers reduce epiphytic overgrowth of subtidal coralline turf. Mar Ecol Prog Ser 515:123–132.  https://doi.org/10.3354/meps11025 CrossRefGoogle Scholar
  6. Boström C, Mattila J (1999) The relative importance of food and shelter for seagrass-associated invertebrates: a latitudinal comparison of habitat choice by isopod grazers. Oecologia 120:162–170.  https://doi.org/10.1007/s004420050 CrossRefPubMedGoogle Scholar
  7. Bruno JF, O’Connor MI (2005) Cascading effects of predator diversity and omnivory in a marine food web. Ecol Lett 8:1048–1056.  https://doi.org/10.1111/j.1461-0248.2005.00808.x CrossRefGoogle Scholar
  8. Bueno M, Dias GM, Leite FPP (2017) The importance of shore height and host identity for amphipod assemblages. Mar Biol Res 13:870–877.  https://doi.org/10.1080/17451000.2017.1306650 CrossRefGoogle Scholar
  9. Byrnes J, Stachowicz JJ, Hultgren KM, Hughes AR, Olyarnik SV, Thornbert CS (2006) Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecol Lett 9:61–71.  https://doi.org/10.1111/j.1461-0248.2005.00842.x CrossRefPubMedGoogle Scholar
  10. Cook K, Vanderklift MA, Poore AGB (2011) Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Mar Ecol Prog Ser 442:263–269.  https://doi.org/10.3354/meps09446 CrossRefGoogle Scholar
  11. Coull BC, Wells JBJ (1983) Refuges from fish predation: experiments with phytal meiofauna from the New Zealand rocky intertidal. Ecology 64:1599–1609.  https://doi.org/10.2307/1937513 CrossRefGoogle Scholar
  12. Cronin G, Hay ME (1996) Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 105:361–368.  https://doi.org/10.1007/BF00328739 CrossRefPubMedGoogle Scholar
  13. Cruz-Rivera E, Hay ME (2000) The effects of diet mixing on consumer fitness: macroalgae, epiphytes, and animal matter as food for marine amphipods. Oecologia 123:252–264.  https://doi.org/10.1007/s004420051012 CrossRefPubMedGoogle Scholar
  14. Cruz-Rivera E, Hay ME (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar Ecol Prog Ser 218:249–266.  https://doi.org/10.3354/meps218249 CrossRefGoogle Scholar
  15. Damman H (1987) Leaf quality and enemy avoidance by the larvae of a pyralid moth. Ecology 68:88–97.  https://doi.org/10.2307/1938808 CrossRefGoogle Scholar
  16. Denno RF, Gratton C, Döbel H, Finke DL (2003) Predation risk affects relative strength of top-down and bottom-up impacts on insect herbivores. Ecology 84:1032–1044.  https://doi.org/10.1890/0012-9658(2003)084%5b1032:PRARSO%5d2.0.CO;2 CrossRefGoogle Scholar
  17. Douglass JG, Duffy JE, Bruno JF (2008) Herbivore and predator diversity interactively affect ecosystem properties in an experimental marine community. Ecol Lett 11:598–608.  https://doi.org/10.1111/j.1461-0248.2008.01175.x CrossRefPubMedGoogle Scholar
  18. Dubiaski-Silva J, Masunari S (1995) Ecologia populacional dos amphipoda (Crustacea) dos fitais de Caiobá, Matinhos, Paraná, Brasil. Rev Bras Zool 12:373–396.  https://doi.org/10.1590/S0101-81751995000200015 CrossRefGoogle Scholar
  19. Dubiaski-Silva J, Masunari S (2008) Natural diet of fish and crabs associated with the phytal community of Sargassum cymosum C. Agardh, 1820 (Phaeophyta, Fucales) at Ponta das Garoupas, Bombinhas, Santa Catarina State, Brazil. J Nat Hist 42:1907–1922.  https://doi.org/10.1080/00222930802126896 CrossRefGoogle Scholar
  20. Duffy JE (1990) Amphipods on seaweeds: partners or pests? Oecologia 83:267–276.  https://doi.org/10.1007/BF00317764 CrossRefPubMedGoogle Scholar
  21. Duffy JE, Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298.  https://doi.org/10.2307/1941102 CrossRefGoogle Scholar
  22. Duffy JE, Hay ME (1994) Herbivory resistance to seaweed chemical defense: the roles of mobility and predation risk. Ecology 75:1304–1319.  https://doi.org/10.2307/1937456 CrossRefGoogle Scholar
  23. Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263.  https://doi.org/10.1890/0012-9615(2000)070%5b0237:SIOGAO%5d2.0.CO;2 CrossRefGoogle Scholar
  24. Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005) Within-thallus variation in chemical and physical defences in two species of ecologically dominant brown macroalgae from the Antarctic Peninsula. J Exp Mar Biol Ecol 322:1–12.  https://doi.org/10.1016/j.jembe.2005.01.010 CrossRefGoogle Scholar
  25. Fox GA (2001) Failure-time analysis: studying times to events and rates at which events occur. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press Inc, New York, pp 235–266Google Scholar
  26. Gutow L, Long JD, Cerda O, Hinojosa IA, Rothäusler E, Tala F, Thiel M (2012) Herbivorous amphipods inhabit protective microhabitats within thalli of giant kelp Macrocystis pyrifera. Mar Biol 159:141–149.  https://doi.org/10.1007/s00227-011-1794-4 CrossRefGoogle Scholar
  27. Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145.  https://doi.org/10.1146/annurev.es.19.110188.000551 CrossRefGoogle Scholar
  28. Hay ME, Pawlik JR, Duffy JE, Fenical W (1989) Seaweed-herbivore-predator interactions: host-plant specialization reduces predation on small herbivores. Oecologia 81:418–427.  https://doi.org/10.1007/BF00377093 CrossRefPubMedGoogle Scholar
  29. Hay ME, Duffy JE, Fenical W (1990) Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant’s clothing. Ecology 71:733–743.  https://doi.org/10.2307/1940326 CrossRefGoogle Scholar
  30. Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE et al (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909.  https://doi.org/10.1073/pnas.0701918104 CrossRefPubMedGoogle Scholar
  31. Holmlund MB, Peterson CH, Hay ME (1990) Does algal morphology affect amphipod susceptibility to fish predation? J Exp Mar Biol Ecol 139:65–83.  https://doi.org/10.1016/0022-0981(90)90039-F CrossRefGoogle Scholar
  32. Jacobucci GB, Leite FPP (2006) Biologia populacional das espécies de Ampithoidae (Crustacea, Amphipoda) associadas a Sargassum filipendula (Phaeophyta, Fucales) na Praia da Fortaleza, Ubatuba, São Paulo, Brasil. Rev Bras Zool 23:1207–1216.  https://doi.org/10.1590/S0101-81752006000400031 CrossRefGoogle Scholar
  33. 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.  https://doi.org/10.3856/vol42-issue2-fulltext-6 CrossRefGoogle Scholar
  34. Jormalainen V, Honkanen T, Heikkilä N (2001) Feeding preferences and performance of a marine isopod seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220:219–230.  https://doi.org/10.3354/meps220219 CrossRefGoogle Scholar
  35. Karez R, Engelbert S, Sommer U (2000) ‘Co-consumption’ and ‘protective coating’: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer-epiphyte-host interactions. Mar Ecol Prog Ser 205:85–93.  https://doi.org/10.3354/meps205085 CrossRefGoogle Scholar
  36. Kraufvelin P, Salovius S (2004) Animal diversity in Baltic rocky shore macroalgae: can Cladophora glomerate compensate for lost Fucus vesiculosus? Estuar Coast Shelf S 61:369–378.  https://doi.org/10.1016/j.ecss.2004.06.006 CrossRefGoogle Scholar
  37. Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R, Pedersen MF (2006) Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199–209.  https://doi.org/10.1016/j.aquabot.2005.08.008 CrossRefGoogle Scholar
  38. Lasley-Rasher RS, Rasher DB, Marion ZH, Taylor RB, Hay ME (2011) Predation constrains host choice for a marine mesograzer. Mar Ecol Prog Ser 434:91–99.  https://doi.org/10.3354/meps09218 CrossRefGoogle Scholar
  39. Littler DS, Littler MM, Bucher KE, Norris JN (1989) Marine plants of the Caribbean. A field guide from Florida to Brazil. Smithsonian Institution Press, Washington, D.CGoogle Scholar
  40. Lockwood JR (1998) On the statistical analysis of multiple-choice feeding preference experiments. Oecologia 116:475–481.  https://doi.org/10.1007/s004420050612 CrossRefGoogle Scholar
  41. Machado GBO, Siqueira SGL, Leite FPP (2017) Abundance, performance, and feeding preference of herbivorous amphipods associated with a host alga-epiphyte system. J Exp Mar Biol Ecol 486:328–335.  https://doi.org/10.1016/j.jembe.2016.10.030 CrossRefGoogle Scholar
  42. Machado GBO, Leite FPP, Sotka EE (2018) Nutrition of marine mesograzers: integrating feeding behavior, nutrient intake and performance of an herbivorous amphipod. PeerJ 6:e5929.  https://doi.org/10.7717/peerj.5929 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Main KL (1985) The influence of prey identity and size on selection of prey by two marine fishes. J Exp Mar Biol Ecol 88:145–152.  https://doi.org/10.1016/0022-0981(85)90034-6 CrossRefGoogle Scholar
  44. Martínez-Crego B, Arteaga P, Tomas F, Santos R (2016) The role of seagrass traits in mediating Zostera noltei vulnerability to mesograzers. PLoS One 11:e0156848.  https://doi.org/10.1371/journal.pone.0156848 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Martin-Smith KM (1993) Abundance of mobile fauna: the role of habitat complexity and predation by fishes. J Exp Mar Biol Ecol 174:243–260.  https://doi.org/10.1016/0022-0981(93)90020-O CrossRefGoogle Scholar
  46. McDonald PS, Bingham BL (2010) Comparing macroalgal food and habitat choice in sympatric, tube-building amphipods, Ampithoe lacertosa and Peramphithoe humeralis. Mar Biol 157:1513–1524.  https://doi.org/10.1007/s00227-010-1425-5 CrossRefGoogle Scholar
  47. Nicotri ME (1980) Factors involved in herbivore food preference. J Exp Mar Biol Ecol 42:13–26.  https://doi.org/10.1016/0022-0981(80)90163-X CrossRefGoogle Scholar
  48. Paul V, Hay ME (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264CrossRefGoogle Scholar
  49. Pennings SC, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619.  https://doi.org/10.2307/1940014 CrossRefGoogle Scholar
  50. Pereira PHC, Jacobucci GB (2008) Dieta e comportamento alimentar de Malacoctenus delalandii. Biota Neotrop 8:141–149.  https://doi.org/10.1590/S1676-06032008000300014 CrossRefGoogle Scholar
  51. Pereira RC, Pinheiro MD, Teixeira VL, Gama BAP (2002) Feeding preferences of the endemic gastropod Astraea latispina in relation to chemical defenses of Brazilian tropical seaweeds. Braz J Biol 62:33–40.  https://doi.org/10.1590/s1519-69842002000100005 CrossRefPubMedGoogle Scholar
  52. Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86.  https://doi.org/10.1007/BF00789935 CrossRefPubMedGoogle Scholar
  53. Poore AGB (1994) Selective herbivory by amphipods inhabiting the brown alga Zonaria angustata. Mar Ecol Prog Ser 107:113–123.  https://doi.org/10.3354/meps107113 CrossRefGoogle Scholar
  54. Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464.  https://doi.org/10.1890/0012-9615(1999)069%5b0443:PPRAEO%5d2.0.CO;2 CrossRefGoogle Scholar
  55. Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the Family Ampithoidae. Evolution 62:21–38.  https://doi.org/10.1111/j.1558-5646.2007.00261.x CrossRefPubMedGoogle Scholar
  56. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V et al (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922.  https://doi.org/10.1111/j.1461-0248.2012.01804.x CrossRefPubMedGoogle Scholar
  57. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  58. Renaud PE, Hay ME, Schmitt TM (1990) Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing. Oecologia 82:217–226.  https://doi.org/10.1007/BF00323538 CrossRefPubMedGoogle Scholar
  59. Reynolds PL, Richardson JP, Duffy JE (2014) Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnol Oceanogr 59:1053–1064.  https://doi.org/10.4319/lo.2014.59.3.1053 CrossRefGoogle Scholar
  60. Russo A (1987) Role of habitat complexity in mediating predation by the gray damselfish Abudefduf sordidus on epiphytal amphipods. Mar Ecol Prog Ser 36:101–105CrossRefGoogle Scholar
  61. Sazima I (1986) Similarities in feeding behavior between some marine and freshwater fishes in two tropical communities. J Fish Biol 29:53–65.  https://doi.org/10.1111/j.1095-8649.1986.tb04926.x CrossRefGoogle Scholar
  62. Simons EB (1906) A morphological study of Sargassum filipendula. Bot Gaz 41:161–182.  https://doi.org/10.1086/328760 CrossRefGoogle Scholar
  63. Sotka EE (2007) Restricted host use by the herbivorous amphipod Peramphithoe tea is motivated by food quality and abiotic refuge. Mar Biol 151:1831–1838.  https://doi.org/10.1007/s00227-007-0612-5 CrossRefGoogle Scholar
  64. Széchy MTM, Paula EJ (2000) Padrões estruturais quantitativos de bancos de Sargassum (Phaeophyta, Fucales) do litoral dos estados do Rio de Janeiro e São Paulo, Brasil. Rev Bras Bot 23:121–132CrossRefGoogle Scholar
  65. Tanaka MO, Leite FPP (2003) Spatial scaling in the distribution of macrofauna associated with Sargassum stenophyllum (Mertens) Martius: analyses of faunal groups, gammarid life habits, and assemblage structure. J Exp Mar Biol Ecol 293:1–22.  https://doi.org/10.1016/S0022-0981(03)00233-8 CrossRefGoogle Scholar
  66. Tararam AS, Wakabara Y, Leite FPP (1986) Vertical distribution of amphipods living on algae of a Brazilian intertidal rocky shore. Crustaceana 51:183–187.  https://doi.org/10.1163/156854086X00665 CrossRefGoogle Scholar
  67. Tavares MR, Grande H, Jacobucci GB (2013) Habitat and food selection by herbivorous amphipods associated with macroalgal beds on the southeast coast of Brazil. Nauplius 21:9–15.  https://doi.org/10.1590/S0104-64972013000100002 CrossRefGoogle Scholar
  68. Taylor RB, Brown PJ (2006) Herbivory in the gammarid amphipod Aora typica: relationships between consumption rates, performance and abundance across ten seaweed species. Mar Biol 149:455–463.  https://doi.org/10.1007/s00227-006-0245-0 CrossRefGoogle Scholar
  69. Taylor RB, Cole RG (1994) Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar Ecol Prog Ser 115:271–282CrossRefGoogle Scholar
  70. Tomida L, Lee JT, Barreto RE (2012) Stomach fullness modulates prey size choice in the frillfin goby, Bathygobius soporator. Zoology 115:283–288.  https://doi.org/10.1016/j.zool.2012.04.004 CrossRefPubMedGoogle Scholar
  71. Van Alstyne KL, Paul VJ (1990) The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes. Oecologia 84:158–163.  https://doi.org/10.1007/BF00318266 CrossRefPubMedGoogle Scholar
  72. Vidal MC, Murphy SM (2018) Bottom-up vs. top-down effects on terrestrial insect herbivores: a meta-analysis. Ecol Lett 21:138–150.  https://doi.org/10.1111/ele.12874 CrossRefPubMedGoogle Scholar
  73. Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141:171–178.  https://doi.org/10.1007/s00442-004-1644-x CrossRefPubMedGoogle Scholar
  74. Wernberg T, Thomsen MS, Kotta J (2013) Complex plant-herbivore-predator interactions in a brackish water seaweed habitat. J Exp Mar Biol Ecol 449:51–56.  https://doi.org/10.1016/j.jembe.2013.08.014 CrossRefGoogle Scholar
  75. Zamzow JP, Amsler CD, McClintock JB, Baker BJ (2010) Habitat choice and predator avoidance by Antarctic amphipods: the roles of algal chemistry and morphology. Mar Ecol Prog Ser 400:155–163.  https://doi.org/10.3354/meps08399 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Programa de Pós-graduação em Ecologia, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil
  2. 2.Departamento de Biologia Animal, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil

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