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Sex- and habitat-specific movement of an omnivorous semi-terrestrial crab controls habitat connectivity and subsidies: a multi-parameter approach

Abstract

Distinct habitats are often linked through fluxes of matter and migration of organisms. In particular, intertidal ecotones are prone to being influenced from both the marine and the terrestrial realms, but whether or not small-scale migration for feeding, sheltering or reproducing is detectable may depend on the parameter studied. Within the ecotone of an upper saltmarsh in the United States, we investigated the sex-specific movement of the semi-terrestrial crab Armases cinereum using an approach of determining multiple measures of across-ecotone migration. To this end, we determined food preference, digestive abilities (enzyme activities), bacterial hindgut communities (genetic fingerprint), and the trophic position of Armases and potential food sources (stable isotopes) of males versus females of different sub-habitats, namely high saltmarsh and coastal forest. Daily observations showed that Armases moved frequently between high-intertidal (saltmarsh) and terrestrial (forest) habitats. Males were encountered more often in the forest habitat, whilst gravid females tended to be more abundant in the marsh habitat but moved more frequently. Food preference was driven by both sex and habitat. The needlerush Juncus was preferred over three other high-marsh detrital food sources, and the periwinkle Littoraria was the preferred prey of male (but not female) crabs from the forest habitats; both male and female crabs from marsh habitat preferred the fiddler crab Uca over three other prey items. In the field, the major food sources were clearly vegetal, but males have a higher trophic position than females. In contrast to food preference, isotope data excluded Uca and Littoraria as major food sources, except for males from the forest, and suggested that Armases consumes a mix of C4 and C3 plants along with animal prey. Digestive enzyme activities differed significantly between sexes and habitats and were higher in females and in marsh crabs. The bacterial hindgut community differed significantly between sexes, but habitat effects were greater than sex effects. By combining multiple measures of feeding ecology, we demonstrate that Armases exhibits sex-specific habitat choice and food preference. By using both coastal forest and saltmarsh habitats, but feeding predominantly in the latter, they possibly act as a key biotic vector of spatial subsidies across habitat borders. The degree of contributing to fluxes of matter, nutrients and energy, however, depends on their sex, indicating that changes in population structure would likely have profound effects on ecosystem connectivity and functioning.

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References

  • Alderson B, Mazumder D, Saintilan N, Zimmerman K, Mulry P (2013) Application of isotope mixing models to discriminate dietary sources over small-scale patches in saltmarsh. Mar Ecol Progr Ser 487:113–122

    Article  Google Scholar 

  • Anger K (1995) The conquest of freshwater and land by marine crabs: adaptations in life-history patterns and larval bioenergetics. J Exp Mar Biol Ecol 193:119–145

    Article  Google Scholar 

  • Barbier EB, Hacker SD, Kennedy C, Koch E, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193

    Article  Google Scholar 

  • Breed GA, Jonsen ID, Myers RA, Bowen WD, Leonard ML (2006) Sex-specific, seasonal foraging tactics of adult grey seals (Halichoerus grypus) revealed by state-space analysis. Ecology 90:3209–3221

    Article  Google Scholar 

  • Brittain RA, Schimmelmann A, Parkhurst DF, Craft CB (2012) Habitat use by coastal birds inferred from stable carbon and nitrogen isotopes. Estuar Coasts 35:633–645

    CAS  Article  Google Scholar 

  • Buck TL, Breed GA, Pennings SC, Chase ME, Zimmer M, Carefoot TH (2003) Diet choice in an omnivorous saltmarsh crab: different food types, body size and habitat complexity. J Exp Mar Biol Ecol 292:103–116

    Article  Google Scholar 

  • Cai W-J (2011) Estuarine and coastal ocean carbon paradox: CO2 sinks or sites of terrestrial carbon incineration? Annu Rev Mar Sci 3:123–145

    Article  Google Scholar 

  • Créach V, Schricke MT, Bertru G, Mariotti A (1997) Stable isotopes and gut analyses to determine feeding relationships in saltmarsh macroconsumers. Estuar Coast Shelf Sci 44(5):599–611

    Article  Google Scholar 

  • Currin CA, Newell SY, Paerl HW (1995) The role of standing dead Spartina alterniflora and benthic microalgae in saltmarsh food webs—considerations based on multiple stable isotope analysis. Mar Ecol Prog Ser 121:99–116

    Article  Google Scholar 

  • Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31–47

    Article  Google Scholar 

  • Dìaz-Tenorio LM, García-Carreno FL, Navarrete del Toro MA (2006) Characterization and comparison of digestive proteinases of the Cortez swimming crab, Callinectes bellicosus, and the arched swimming crab, Callinectes arcuatus. Invertebr Biol 125:125–135

    Article  Google Scholar 

  • Dittmer J, Lesobre J, Raimond R, Zimmer M, Bouchon D (2012) Influence of changing plant food sources on the gut microbiota of saltmarsh detritivores. Microb Ecol 64:814–825

    PubMed  Article  Google Scholar 

  • Doi H, Matsumasa M, Toya T, Satoh N, Mizota C, Maki Y, Kikuchi E (2005) Spatial shifts in food sources for macrozoobenthos in an estuarine ecosystem: carbon and nitrogen stable isotope analyses. Estuar Coast Shelf Sci 64:316–322

    Article  Google Scholar 

  • Ewers C, Beiersdorf A, Wieski K, Pennings SC, Zimmer M (2012) Predator/prey-interactions promote decomposition of low-quality detritus. Wetlands 32:931–938

    Article  Google Scholar 

  • Fantle MS, Dittel AI, Schwalm SM, Epifanio CE, Fogel ML (1999) A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120:416–426

    Article  Google Scholar 

  • Frenkel D (2004) Introduction to Monte Carlo Methods. In: Attig N, Binder K, Grubmüller H, Kremer K (eds) Computational soft matter: from synthetic polymers to proteins. John von Neumann Institute for Computing, Jülich, pp 23–59

    Google Scholar 

  • Garcia EA, Bertness MD, Alberti J, Silliman BR (2011) Crab regulation of cross-ecosystem resource transfer by marine foraging fire ants. Oecologia 166:1111–1119

    PubMed  Article  Google Scholar 

  • Giddins RL, Lucas JS, Neilson MJ, Richards GN (1986) Feeding ecology of the mangrove crab Neosarmatium smithi (Crustacea: Decapoda: Sesarmidae). Mar Ecol Prog Ser 33:147–155

    Article  Google Scholar 

  • Gratton CJ, Vander Zanden MJ (2009) Flux of aquatic insect productivity to land: comparison of lentic and lotic ecosystems. Ecology 90:2689–2699

    PubMed  Article  Google Scholar 

  • Gratton CJ, Donaldson J, Vander Zanden MJ (2008) Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11:764–774

    Article  Google Scholar 

  • Guest MA, Connolly RM, Loneragan NR (2004) Carbon movement and assimilation by invertebrates in estuarine habitat at a scale of metres. Mar Ecol Prog Ser 278:27–34

    CAS  Article  Google Scholar 

  • Haines EB (1976a) Relation between the stable carbon isotope composition of fiddler crabs, plants and soils in a saltmarsh. Limnol Oceanogr 21:880–883

    Article  Google Scholar 

  • Haines EB (1976b) Stable carbon isotope ratios in the biota, soils and tidal water of a Georgia saltmarsh. Estuar Coast Mar Sci 4:609–616

    CAS  Article  Google Scholar 

  • Haines EB, Montague CL (1979) Food sources of estuarine invertebrates analyzed using 13C/12C ratios. Ecology 60:48–56

    Article  Google Scholar 

  • He X (2003) A continuous spectrophotometric assay for the determination of diamondback moth esterase activity. Arch Insect Biochem Physiol 54:68–76

    CAS  PubMed  Article  Google Scholar 

  • Helfer V, Broquet T, Fumagalli L (2012) Sex-specific estimates of dispersal show female philopatry and male dispersal in a promiscuous amphibian, the alpine salamander (Salamandra atra). Mol Ecol 21:4706–4720

    CAS  PubMed  Article  Google Scholar 

  • Henry HAL, Jefferies RL (2009) Opportunistic herbivores, migratory connectivity, and catastrophic shifts in Arctic coastal systems. In: Silliman BR, Grosholz ED, Bertness MD (eds) Human impacts on saltmarshes: a global perspective. University of California Press, Berkeley, pp 85–102

    Google Scholar 

  • Ho C-K, Pennings SC (2008) Consequences of omnivory for trophic interactions on a saltmarsh shrub. Ecology 89(6):1714–1722

    PubMed  Article  Google Scholar 

  • Hoekman D, Dreyer J, Jackson R, Townsend P, Gratton CJ (2011) Lake to land subsidies: experimental addition of aquatic insects increases terrestrial arthropod densities. Ecology 92:2063–2072

    PubMed  Article  Google Scholar 

  • Johnston DJ, Freeman J (2005) Dietary preference and digestive enzyme activities as indicators of trophic resource utilization by six species of crab. Biol Bull 208:36–46

    CAS  PubMed  Article  Google Scholar 

  • Johnston DJ, Yellowlees D (1998) Relationship between dietary preference and digestive enzyme complement of the slipper lobster, Thenus orientalis (Decapoda: Scyllaridae). J Crustac Biol 18:656–665

    Article  Google Scholar 

  • Jones RF, Baltz DM, Allen RL (2002) Patterns of resource use by fishes and macroinvertebrates in Barataria Bay, Louisiana. Mar Ecol Prog Ser 237:271–289

    Article  Google Scholar 

  • Kanaya G, Takagi S, Nobata E, Kikuchi E (2007) Spatial dietary shift of macrozoobenthos in a brackish lagoon revealed by carbon and nitrogen stable isotope ratios. Mar Ecol Prog Ser 345:117–127

    CAS  Article  Google Scholar 

  • Kasai A, Horie H, Sakamoto W (2004) Selection of food sources by Ruditapes philippinarum and Mactra veneriformis (Bivalva: Mollusca) determined from stable isotope analysis. Fish Sci 70:11–20

    CAS  Article  Google Scholar 

  • Kneib RT (1997) The role of tidal marshes in the ecology of estuarine nekton. Oceanogr Mar Biol Annu Rev 35:163–220

    Google Scholar 

  • Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437(7060):880–883

    CAS  PubMed  Article  Google Scholar 

  • Krest JM, Moore WS, Gardner LR, Morris JT (2000) Marsh nutrient export supplied by groundwater discharge: evidence from radium measurements. Glob Biogeochem Cycles 14:167–176

    CAS  Article  Google Scholar 

  • Kurata K, Minami H, Kikuchi E (2001) Stable isotope analysis of food sources for salt marsh snails. Mar Ecol Prog Ser 223:167–177

    Article  Google Scholar 

  • Kyomo J (1992) Variations in the feeding habits of males and females of the crab Sesarma intermedia. Mar Ecol Prog Ser 83:151–155

    Article  Google Scholar 

  • Lachnit T, Bümel M, Imhoff JF, Wahl M (2009) Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat Biol 5:181–186

    Google Scholar 

  • Lee SY (1998) Ecological role of grapsid crabs in mangrove ecosystems: a review. Mar Freshw Res 49:335–343

    Article  Google Scholar 

  • Lewis TL, Mews M, Jelinski DE, Zimmer M (2007) Detrital subsidy to the supratidal zone provides feeding habitat for intertidal crabs. Estuar Coast 30:451–458

    Article  Google Scholar 

  • Loreau M, Naeem S, Inchausti S (2002) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford

    Google Scholar 

  • Lundberg J, Moberg F (2003) Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6:87–98

    Article  Google Scholar 

  • Marczak LB, Ho C-K, Wieski K, Vu H, Denno RF, Pennings SC (2011) Latitudinal variation in top-down and bottom-up control of a saltmarsh food web. Ecology 92:276–281

    CAS  PubMed  Article  Google Scholar 

  • Mattila JM, Zimmer M, Vesakoski O, Jormalainen V (2014) Habitat-specific gut microbiota of the marine herbivore Idotea balthica (Isopoda). J Exp Mar Biol Ecol 455:22–28

  • Mazumder D, Saintilan N, Williams RJ (2006) Trophic relationships between itinerant fish and crab larvae in a temperate Australian saltmarsh. Mar Freshw Res 57:193–199

    Article  Google Scholar 

  • McCann KS (2012) Food webs. Princeton University Press, Princeton

    Google Scholar 

  • McIvor CC, Odum WE (1988) Food, predation risk, and microhabitat selection in a marsh fish assemblage. Ecology 69:1341–1351

    Article  Google Scholar 

  • Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed Central  PubMed  Google Scholar 

  • Myers RT, Zak DR, White DC, Peacock A (2001) Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367

    CAS  Article  Google Scholar 

  • Nordhaus I (2004) Feeding ecology of the semi-terrestrial crab Ucides cordatus (Decapoda: Brachyura) in a mangrove forest in northern Brazil. PhD thesis. University of Bremen

  • Orr M, Zimmer M, Mews M, Jelinski DE (2005) Wrack deposition on different beach types: spatial and temporal variation in the pattern of subsidy. Ecology 86:1496–1507

    Article  Google Scholar 

  • Parsons KA, De la Cruz AA (1980) Energy flow and grazing behavior of conocephaline grasshoppers in a Juncus roemerianus marsh. Ecology 6:1045–1050

    Article  Google Scholar 

  • Pavasovic M, Richardson NA, Anderson AJ, Mann D, Mather PB (2004) Effect of pH, temperature and diet on digestive enzyme profiles in the mud crab, Scylla serrata. Aquaculture 242:641–654

    CAS  Article  Google Scholar 

  • Pennings SC, Carefoot TH, Siska EL, Chase ME, Page TA (1998) Feeding preferences of a generalist salt-marsh crab: relative importance of multiple plant traits. Ecology 79:1968–1979

    Article  Google Scholar 

  • Peterson BJ, Howarth RW (1987) Sulfur, carbon and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnol Oceanogr 32:1195–1213

    CAS  Article  Google Scholar 

  • Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86

    CAS  PubMed  Article  Google Scholar 

  • Platt SG, Elsey RM, Liu H, Rainwater TR, Nifong JC, Rosenblatt AE, Heithaus M, Mazzotti FJ (2013) Frugivory and seed dispersal by crocodilians: an overlooked form of saurochory? J Zool 291:87–99

    Google Scholar 

  • Plumley FG, Davis DE, McEnerney JT, Everest JW (1980) Effects of a photosynthesis inhibitor, atrazine, on the saltmarsh fiddler crab, Uca pugnax. Estuaries 3:217–223

    CAS  Article  Google Scholar 

  • Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316

    Article  Google Scholar 

  • Riera P, Richard P, Gremare A, Blanchard G (1996) Food source of intertidal nematodes in the Bay of Marennes-Oleron (France), as determined by dual stable isotope analysis. Mar Ecol Prog Ser 142:303–309

    CAS  Article  Google Scholar 

  • Rosenblatt AE, Heithaus MR, Mather ME, Matich P, Nifong JP, Ripple WJ, Silliman BR (2013) The roles of large predators in coastal ecosystems. Oceanography 26:156–167

    Article  Google Scholar 

  • Schofield JA, Hagerman AE, Harold A (1998) Loss of tannins and other phenolics from willow leaf litter. J Chem Ecol 24:1409–1421

    CAS  Article  Google Scholar 

  • Seiple W (1979) Distribution, habitat preferences and breeding periods in the crustaceans Sesarma cinereum and S. reticulatum (Brachyura: Decapoda: Grapsidae). Mar Biol 52:77–86

    Article  Google Scholar 

  • Seiple W, Salmon M (1987) Reproductive, growth and life-history contrasts between two species of grapsid crabs, Sesarma cinereum and S. reticulatum. Mar Biol 94:1–6

  • Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia saltmarsh. Ecology 82:2830–2845

    Article  Google Scholar 

  • Sullivan MJ, Moncreiff S (1990) Edaphic algae are important component of saltmarsh food-webs: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 62:149–159

    Article  Google Scholar 

  • Teal JM (1962) Energy flow in the saltmarsh ecosystem of Georgia. Ecology 43:614–624

    Article  Google Scholar 

  • Thaxter CB, Daunt F, Hamer KC, Watanuki Y, Harris MP, Grémillet D, Peters G, Wanless S (2009) Sex-specific food provisioning in a monomorphic seabird, the common guillemot Uria aalge: nest defence, foraging efficiency or parental effort? J Avian Biol 40:75–84

    Article  Google Scholar 

  • Treplin M, Pennings SC, Zimmer M (2013) Decomposition in a US saltmarsh is driven by dominant species not species complementarity. Wetlands 33:83–89

    Article  Google Scholar 

  • Valiela I, Teal JM (1974) Nutrient limitations in salt marsh vegetation. In: Reimold RJ, Queen WH (eds) Ecology of Halophytes. Academic Press, New York, pp. 547–563

  • Vander Zanden MJ, Gratton CJ (2011) Blowin’ in the wind: reciprocal airborne carbon fluxes between lakes and land. Can J Fish Aquat Sci 68:170–182

    CAS  Article  Google Scholar 

  • Wolf PJ, Shanholtzer SF, Reimold RJ (1975) Population estimates for Uca pugnax (Smith, 1870) on the Duplin estuary marsh, Georgia, USA (Decapoda Brachyura, Ocypodidae). Crustaceana 29:79–91

    Article  Google Scholar 

  • Zimmer M (2002) Nutrition in terrestrial isopods (Isopoda: Oniscidea): an evolutionary-ecological approach. Biol Rev 77:455–493

    PubMed  Article  Google Scholar 

  • Zimmer M (2005) Cellulases. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Kluwer, London, pp 249–254

    Chapter  Google Scholar 

  • Zimmer M, Pennings SC, Buck TL, Carefoot TH (2002) Species-specific patterns of litter processing by terrestrial isopods (Isopoda: Oniscidea) in high intertidal saltmarshes and coastal forests. Funct Ecol 16:596–607

    Article  Google Scholar 

  • Zimmer M, Pennings SC, Buck TL, Carefoot TH (2004) Saltmarsh litter and detritivores: a closer look at redundancy. Estuaries 27:753–769

    Article  Google Scholar 

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Acknowledgments

We thank Stuart Linton (Deakin University, Australia) for valuable discussion on digestive enzymes; Melissa Both, Mario Muscarella and Daniel Saucedo (UGAMI), and Stephanie Stratil and Tim Lachnit (GEOMAR, Kiel, Germany) for support and assistance in the field and the lab. We thank NSF (OCE06-20959) for funding. This work is contribution #1038 of the University of Georgia Marine Institute, and a contribution of the Georgia Coastal Ecosystems Long-Term Ecological Research program.

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Correspondence to Martin Zimmer.

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Communicated by Liliane Ruess.

Appendices

Appendix 1: Spatial distribution of individual male and female crabs

Spatial distribution of individual male and female crabs according to recapture-based migration patterns within the marsh–forest ecotone. Elipsoids reflect the individual range of recapture spots along the two axes parallel versus perpendicular to the coast line.

figure a

Appendix 2: Estimated proportional contribution of different food sources

Estimated proportional contribution of different food sources (J, Juncus; B, Borrichia; S, Spartina; Q, Quercus; M, Melampus; L, Littoraria; O, Orchestia; U, Uca; D, benthic diatoms) to the nutrition of male and female Armases from marsh versus forest habitat. Box plots represent minimum, 5, 25, 75 and 95 % percentiles, and maximum.

figure b

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Hübneṙ, L., Pennings, S.C. & Zimmer, M. Sex- and habitat-specific movement of an omnivorous semi-terrestrial crab controls habitat connectivity and subsidies: a multi-parameter approach. Oecologia 178, 999–1015 (2015). https://doi.org/10.1007/s00442-015-3271-0

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  • DOI: https://doi.org/10.1007/s00442-015-3271-0

Keywords

  • Saltmarsh
  • Coastal forest
  • Land crab
  • Sexual dimorphism
  • Spatial subsidy
  • Habitat connectivity
  • Motile link organism