Habitat and food selection by herbivorous amphipods associated with macroalgal beds on the southeast coast of Brazil

Tavares, Mauro Rezende; Grande, Henrique; Jacobucci, Giuliano Buzá

Abstract

The factors that influence the selection of marine macrophytes by meso-herbivores are complex, and may include the nutritional quality of algae, the value of the habitat as a shelter, and the availability of algae in the environment. Here we investigated the existence of differential use of Sargassum filipendula C. Agardh, 1824 (Phaeophyta) and Galaxaura stupocaulon Kjellman, 1900 (Rhodophyta) as habitats and feeding resources by species of Hyalidae and Ampithoidae, in laboratory manipulation experiments and in an algal bed on the northern coast of the state of São Paulo, Brazil. In the field, 19 fronds were collected from each alga and the associated amphipods were identified and counted. To evaluate food preference and habitat selection by amphipods, we conducted laboratory experiments using containers containing fragments of algae and individuals of Cymadusa filosa Savigny, 1816 or Hyale nigra (Haswell, 1879). In natural conditions, the density of C. filosa was significantly higher on G. stupocaulon, while in the feeding and habitat preference experiment we found a higher density on S. filipendula. The densities of H. nigra did not differ between the algae in both experiments, probably as a result of the variety of food items in its diet, and its high mobility and wide distribution on different substrates. The different results for C. filosa suggest that the pattern of feeding and habitat selection can be affected by external characteristics of the algae; probably, refuge from predation is an important selective force acting on the use of algae by these animals.

Amphipods; food choice; habitat choice; predation refuge

Arrontes, J. 1990. Diet, food preference and digestive efficiency in intertidal isopods inhabiting macroalgae. Journal of Experimental Marine Biology and Ecology, 139: 231-249.
Arrontes, J. 1999. On the evolution of interactions between marine mesoherbivores and algae. Botanica Marina, 42: 137-155.
Brawley, S.H. 1992. Mesoherbivores. p. 235-263. In: John, D.M.; Hawkins, S.J. and Price J.H. (eds), Plant-animal Interactions in the Marine Benthos. Systematics Associations Special, Vol. 46. New York, Oxford University Press.
Brawley, S.H. and Adey, W.H. 1981. The effects of micrograzers on algal community structure in a coral reef microcosm. Marine Biology, 61: 167-178.
Conlan, K.E. 1982. Revision of the gammaridean amphipod family Ampithoidae using numerical analytical methods. Canadian Journal of Zoology, 60: 2015-2027.
Cruz-Rivera, E. and Hay, M.E. 2001. The effects of diet mixing on consumer fitness: macroalgae, epiphytes, and animal matter as food for marine amphipods. Oecologia, 123: 252-264.
Duffy, J.E. and Hay, M.E. 1991. Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology, 72: 1286-1298.
Duffy, J.E. and Hay, M.E. 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecological Monographs, 70: 237-26.
Duffy, J.E.; Macdonald, K.S.; Rhode, J.M. and Parker, J.D. 2001. Grazer diversity, functional redundancy and productivity in seagrass beds: an experimental test. Ecology, 82: 2417-2434.
Hay, M.E. 1992. The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. p. 93-118. In: V.J. Paul (ed), Ecological Roles of Marine Natural Products. New York, Academic Press.
Hay, M.E.; Duffy, J.E. and Fenical, W. 1990. Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing. Ecology, 71: 733-743.
Hay, M.E.; Duffy, J.; Pfister C.A. and Fenical, W. 1987. Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology, 68: 1567-1580.
Hay, M.E.; Pawlik, J.R.; Duffy, J.E. and Fenical, W. 1989. Seaweed-herbivore-predator interactions: host-plant specialization reduces predation on small herbivores. Oecologia, 81: 418-427.
Hughes, R.N. 1980. Optimal foraging theory in the marine context. Oceanography and Marine Biology: An Annual Review, 18: 423-481.
Iribarne, O. 1996. Habitat structure, population abundance and the opportunity for selection on body weight in the amphipod Eogammarus oclairi Marine Biology, 127: 143-150.
Isaksson, I.; Pihl, L. and Montfrans, J. 1994. Eutrophication-related changes in macrovegetation and foraging of young cod (Gadus morhua L.): a mesocosm experiment. Journal of Experimental Marine Biology and Ecology, 177: 203-217.
Jacobucci, G.B. and Leite, F.P.P. 2002. Distribuição vertical e flutuação sazonal da macrofauna vágil associada a Sargassum cymosum C. Agardh, na praia do Lázaro, Ubatuba, São Paulo, Brasil. Revista Brasileira de Zoologia, 19(1): 87-100.
Jacobucci, G.B.; Tanaka, M.O. and Leite, F.P.P. 2009. Temporal variation of amphipod assemblages associated with Sargassum filipendula (Phaeophyta) and its epiphytes in a subtropical shore. Aquatic Ecology, 43: 1031-1040.
Jernakoff, P.; Brearley, A. and Nielsen, J. 1996. Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceagraphy and Marine Biology: An Annual Review, 34: 109-162.
Jormalainen, V.; Honkanen, T. and Heikkila, N. 2001. Feeding preferences and performance of a marine isopod on seaweeds hosts: cost of habitat specialization. Marine Ecology Progress Series, 220:219-230.
Klumpp, D.W.; Salita-Espinosa, J.T. and Fortes, M.D. 1992. The role of epiphytic periphiton and macroinvertebrate grazer in the trophic flux of a tropical seagrass community. Aquatic Botany, 43: 327-349.
Leite, F.P.P.; Güth, A.Z. and Jacobucci, G.B. 2000. Temporal comparison of gammaridean amphipods of Sargassum cymosum on two rocky shores in southeastern Brazil. Nauplius, 8(2): 227-236.
Lubchenco, J. and Gaines, S.D. 1981. A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annual Review of Ecology and Systematics, 12: 405-437.
Masunari, S. and L. Forneris. 1981. O ecossistema fital - uma revisão. p. 149-172. In: Seminários de Biologia Marinha. Academia Brasileira de Ciências, Rio de Janeiro.
Mattila, J. 1992. The effect of habitat complexity on predation efficiency of perch (Perca fluviatilis L.) and ruffe (Gymnocephalus cernutus) (L.). Journal of Experimental Marine Biology and Ecology, 157: 55-67.
Mattingly, H.T. and Butler, M.J. 1994. Laboratory predation on the Trinidadian guppy: implications for the size-selective predation hypothesis and guppy life history evolution. Oikos, 69: 54-64.
Nelson, W.G. 1979. An analysis of structural pattern in an eelgrass (Zostera marina L.) amphipod community. Journal of Experimental Marine Biology and Ecology, 39: 231- 264.
Nicotri, M.E. 1980. Factors involved in herbivore food preference. Journal of Experimental Marine Biology and Ecology, 42: 13-26.
Norton, T.A. and Benson, M.R. 1983. Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology, 75: 169-177.
Pereira, P.H.C. and Jacobucci, G.B. 2008. Diet and feeding behavior of Malacoctenus delalandii (Perciformes: Labrisomidae). Biota Neotropica, 8(3): 141-149.
Perreira, R.C. and Yoneshigue-Valentin, Y. 1999. The role of polyphenols from the tropical brown alga Sargassum furcutum on the feeding by amphipod herbivores. Botanica Marina, 42: 441-448.
Ruffo, S. 1998. The Amphipoda of the Mediterranean. Mémoires de l'Institut Océanographique, 13:1-959.
Serejo, C.S. 2004. Cladistic revision of talitroidean amphipods (Crustacea, Gammaridea), with a proposal of a new classification. Zoologica Scripta, 33: 551-586.
Stoner, A.W. 1980. Perception and choice of substratum by epifaunal amphipods associated with seagrasses. Marine Ecology Progress Series, 3: 105-111.
Széchy, M.T.M. and Paula, E.J. 2000. Padrões estruturais quantitativos em bancos de Sargassum (Phaeophyta, Fucales) do litoral dos estados do Rio de Janeiro e São Paulo, Brasil. Revista Brasileira de Botânica, 23(2): 121-132.
Szlávecz, K. 1985. The effect of microhabitats on the leaf litter decomposition and on the distribution of soil animals. Holarctic Ecology, 8: 33-38.
Tararam, A.S.; Wakabara, Y. and Mesquita, H.S.L. 1985. Feeding habits of Hyale media (Dana, 1853) (Crustacea-Amphipoda). Boletim do Instituto Oceanográfico, 33: 193-199.
Taylor, R.B. and Cole, R.G. 1994. Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Marine Ecology Progress Series, 115: 271-282.
Thomas, J.D. 1993. Biological monitoring and tropical biodiversity in marine environments: a critique with recommendations, and comments on the use of amphipods as bioindicators. Jornal of Natural History, 27: 795-806.
Van Montfrans, J.; Orth, R.J. and Vay, S.A. 1982. Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquatic Botany, 14: 75-89.
Wakabara, Y.; Flynn, M. and Tararam, A.S. 1996. Ingestion and selection of suprabenthic crustaceans by small-sized fishes in a lower saltmarsh system. Revista Brasileira de Oceanografia, 44: 89-103.

Publication Dates

Publication in this collection
27 Jan 2015
Date of issue
June 2013

History

Received
15 Dec 2012
Accepted
07 May 2013

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] Arrontes, J. 1990. Diet, food preference and digestive efficiency in intertidal isopods inhabiting macroalgae. Journal of Experimental Marine Biology and Ecology, 139: 231-249.

[2] Arrontes, J. 1999. On the evolution of interactions between marine mesoherbivores and algae. Botanica Marina, 42: 137-155.

[3] Brawley, S.H. 1992. Mesoherbivores. p. 235-263. In: John, D.M.; Hawkins, S.J. and Price J.H. (eds), Plant-animal Interactions in the Marine Benthos. Systematics Associations Special, Vol. 46. New York, Oxford University Press.

[4] Brawley, S.H. and Adey, W.H. 1981. The effects of micrograzers on algal community structure in a coral reef microcosm. Marine Biology, 61: 167-178.

[5] Conlan, K.E. 1982. Revision of the gammaridean amphipod family Ampithoidae using numerical analytical methods. Canadian Journal of Zoology, 60: 2015-2027.

[6] Cruz-Rivera, E. and Hay, M.E. 2001. The effects of diet mixing on consumer fitness: macroalgae, epiphytes, and animal matter as food for marine amphipods. Oecologia, 123: 252-264.

[7] Duffy, J.E. and Hay, M.E. 1991. Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology, 72: 1286-1298.

[8] Duffy, J.E. and Hay, M.E. 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecological Monographs, 70: 237-26.

[9] Duffy, J.E.; Macdonald, K.S.; Rhode, J.M. and Parker, J.D. 2001. Grazer diversity, functional redundancy and productivity in seagrass beds: an experimental test. Ecology, 82: 2417-2434.

[10] Hay, M.E. 1992. The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. p. 93-118. In: V.J. Paul (ed), Ecological Roles of Marine Natural Products. New York, Academic Press.

[11] Hay, M.E.; Duffy, J.E. and Fenical, W. 1990. Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing. Ecology, 71: 733-743.

[12] Hay, M.E.; Duffy, J.; Pfister C.A. and Fenical, W. 1987. Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology, 68: 1567-1580.

[13] Hay, M.E.; Pawlik, J.R.; Duffy, J.E. and Fenical, W. 1989. Seaweed-herbivore-predator interactions: host-plant specialization reduces predation on small herbivores. Oecologia, 81: 418-427.

[14] Hughes, R.N. 1980. Optimal foraging theory in the marine context. Oceanography and Marine Biology: An Annual Review, 18: 423-481.

[15] Iribarne, O. 1996. Habitat structure, population abundance and the opportunity for selection on body weight in the amphipod Eogammarus oclairi Marine Biology, 127: 143-150.

[16] Isaksson, I.; Pihl, L. and Montfrans, J. 1994. Eutrophication-related changes in macrovegetation and foraging of young cod (Gadus morhua L.): a mesocosm experiment. Journal of Experimental Marine Biology and Ecology, 177: 203-217.

[17] Jacobucci, G.B. and Leite, F.P.P. 2002. Distribuição vertical e flutuação sazonal da macrofauna vágil associada a Sargassum cymosum C. Agardh, na praia do Lázaro, Ubatuba, São Paulo, Brasil. Revista Brasileira de Zoologia, 19(1): 87-100.

[18] Jacobucci, G.B.; Tanaka, M.O. and Leite, F.P.P. 2009. Temporal variation of amphipod assemblages associated with Sargassum filipendula (Phaeophyta) and its epiphytes in a subtropical shore. Aquatic Ecology, 43: 1031-1040.

[19] Jernakoff, P.; Brearley, A. and Nielsen, J. 1996. Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceagraphy and Marine Biology: An Annual Review, 34: 109-162.

[20] Jormalainen, V.; Honkanen, T. and Heikkila, N. 2001. Feeding preferences and performance of a marine isopod on seaweeds hosts: cost of habitat specialization. Marine Ecology Progress Series, 220:219-230.

[21] Klumpp, D.W.; Salita-Espinosa, J.T. and Fortes, M.D. 1992. The role of epiphytic periphiton and macroinvertebrate grazer in the trophic flux of a tropical seagrass community. Aquatic Botany, 43: 327-349.

[22] Leite, F.P.P.; Güth, A.Z. and Jacobucci, G.B. 2000. Temporal comparison of gammaridean amphipods of Sargassum cymosum on two rocky shores in southeastern Brazil. Nauplius, 8(2): 227-236.

[23] Lubchenco, J. and Gaines, S.D. 1981. A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annual Review of Ecology and Systematics, 12: 405-437.

[24] Masunari, S. and L. Forneris. 1981. O ecossistema fital - uma revisão. p. 149-172. In: Seminários de Biologia Marinha. Academia Brasileira de Ciências, Rio de Janeiro.

[25] Mattila, J. 1992. The effect of habitat complexity on predation efficiency of perch (Perca fluviatilis L.) and ruffe (Gymnocephalus cernutus) (L.). Journal of Experimental Marine Biology and Ecology, 157: 55-67.

[26] Mattingly, H.T. and Butler, M.J. 1994. Laboratory predation on the Trinidadian guppy: implications for the size-selective predation hypothesis and guppy life history evolution. Oikos, 69: 54-64.

[27] Nelson, W.G. 1979. An analysis of structural pattern in an eelgrass (Zostera marina L.) amphipod community. Journal of Experimental Marine Biology and Ecology, 39: 231- 264.

[28] Nicotri, M.E. 1980. Factors involved in herbivore food preference. Journal of Experimental Marine Biology and Ecology, 42: 13-26.

[29] Norton, T.A. and Benson, M.R. 1983. Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology, 75: 169-177.

[30] Pereira, P.H.C. and Jacobucci, G.B. 2008. Diet and feeding behavior of Malacoctenus delalandii (Perciformes: Labrisomidae). Biota Neotropica, 8(3): 141-149.

[31] Perreira, R.C. and Yoneshigue-Valentin, Y. 1999. The role of polyphenols from the tropical brown alga Sargassum furcutum on the feeding by amphipod herbivores. Botanica Marina, 42: 441-448.

[32] Ruffo, S. 1998. The Amphipoda of the Mediterranean. Mémoires de l'Institut Océanographique, 13:1-959.

[33] Serejo, C.S. 2004. Cladistic revision of talitroidean amphipods (Crustacea, Gammaridea), with a proposal of a new classification. Zoologica Scripta, 33: 551-586.

[34] Stoner, A.W. 1980. Perception and choice of substratum by epifaunal amphipods associated with seagrasses. Marine Ecology Progress Series, 3: 105-111.

[35] Széchy, M.T.M. and Paula, E.J. 2000. Padrões estruturais quantitativos em bancos de Sargassum (Phaeophyta, Fucales) do litoral dos estados do Rio de Janeiro e São Paulo, Brasil. Revista Brasileira de Botânica, 23(2): 121-132.

[36] Szlávecz, K. 1985. The effect of microhabitats on the leaf litter decomposition and on the distribution of soil animals. Holarctic Ecology, 8: 33-38.

[37] Tararam, A.S.; Wakabara, Y. and Mesquita, H.S.L. 1985. Feeding habits of Hyale media (Dana, 1853) (Crustacea-Amphipoda). Boletim do Instituto Oceanográfico, 33: 193-199.

[38] Taylor, R.B. and Cole, R.G. 1994. Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Marine Ecology Progress Series, 115: 271-282.

[39] Thomas, J.D. 1993. Biological monitoring and tropical biodiversity in marine environments: a critique with recommendations, and comments on the use of amphipods as bioindicators. Jornal of Natural History, 27: 795-806.

[40] Van Montfrans, J.; Orth, R.J. and Vay, S.A. 1982. Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquatic Botany, 14: 75-89.

[41] Wakabara, Y.; Flynn, M. and Tararam, A.S. 1996. Ingestion and selection of suprabenthic crustaceans by small-sized fishes in a lower saltmarsh system. Revista Brasileira de Oceanografia, 44: 89-103.

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Habitat and food selection by herbivorous amphipods associated with macroalgal beds on the southeast coast of Brazil

Abstract

Publication Dates

History