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Land Crabs As Key Drivers in Tropical Coastal Forest Recruitment

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Land Crabs As Key Drivers in Tropical Coastal Forest Recruitment BIOLOGICAL Cambridge REVIEWS Philosophical Society Biol. Rev. (2009), 84, pp. 203–223. 203 doi:10.1111/j.1469-185X.2008.00070.x Land crabs as key drivers in tropical coastal forest recruitment Erin Stewart Lindquist1*, Ken W. Krauss2, Peter T. Green3, Dennis J. O’Dowd4, Peter M. Sherman5, and Thomas J. Smith, III6 1 Meredith College, Department of Biological Sciences, 3800 Hillsborough Street, Raleigh, North Carolina 27607, USA 2 U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Boulevard, Lafayette, Louisiana, 70506, USA 3 Department of Botany, La Trobe University, Bundoora, Victoria 3086, Australia 4 Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Victoria 3800, Australia 5 University of Redlands, Department of Environmental Studies, 1200 East Colton Avenue, P.O. Box 3080, Redlands, California 92373, USA 6 U.S. Geological Survey, Florida Integrated Science Center, 600 Fourth Street, South, St. Petersburg, Florida, 33701, USA (Received 17 October 2008; revised 11 November 2008; accepted 19 November 2008) ABSTRACT Plant populations are regulated by a diverse assortment of abiotic and biotic factors that influence seed dispersal and viability, and seedling establishment and growth at the microsite. Rarely does one animal guild exert as significant an influence on different plant assemblages as land crabs. We review three tropical coastal ecosystems– mangroves, island maritime forests, and mainland coastal terrestrial forests–where land crabs directly influence forest composition by limiting tree establishment and recruitment. Land crabs differentially prey on seeds, propagules and seedlings along nutrient, chemical and physical environmental gradients. In all of these ecosystems, but especially mangroves, abiotic gradients are well studied, strong and influence plant species distributions. However, we suggest that crab predation has primacy over many of these environmental factors by acting as the first limiting factor of tropical tree recruitment to drive the potential structural and compositional organisation of coastal forests. We show that the influence of crabs varies relative to tidal gradient, shoreline distance, canopy position, time, season, tree species and fruiting periodicity. Crabs also facilitate forest growth and development through such activities as excavation of burrows, creation of soil mounds, aeration of soils, removal of leaf litter into burrows and creation of carbon-rich soil microhabitats. For all three systems, land crabs influence the distribution, density and size-class structure of tree populations. Indeed, crabs are among the major drivers of tree recruitment in tropical coastal forest ecosystems, and their conservation should be included in management plans of these forests. Key words: biotic control, ecological filter, environmental gradient, environmental engineer, mangrove, island maritime forest, predation, seed, seedling, terrestrial mainland forest, tree. CONTENTS I. Introduction ...................................................................................................................................... 204 II. Mangroves ......................................................................................................................................... 208 (1) Propagule predation ................................................................................................................... 208 (2) Seedling predation ...................................................................................................................... 209 (3) Spatial variation .......................................................................................................................... 209 (4) Temporal variation ..................................................................................................................... 211 (5) Crab filter interactions ................................................................................................................ 211 III. Island maritime forests ...................................................................................................................... 211 * Address for correspondence: Tel: 01 919 760 8754; Fax: 01 919 760-8761; E-mail: [email protected] Biological Reviews 84 (2009) 203–223 Ó 2009 Journal compilation Ó 2009 Cambridge Philosophical Society. No claim to original US government works 204 Erin S. Lindquist and others (1) Fruit and seed predation ............................................................................................................ 212 (2) Seedling predation ...................................................................................................................... 212 (3) Spatial variation .......................................................................................................................... 212 (4) Temporal variation ..................................................................................................................... 213 (5) Crab filter interactions ................................................................................................................ 214 IV. Mainland coastal terrestrial forests ................................................................................................... 214 (1) Seed predation ............................................................................................................................ 214 (2) Seedling predation ...................................................................................................................... 216 (3) Spatial variation .......................................................................................................................... 216 (4) Temporal variation ..................................................................................................................... 216 (5) Crab filter interactions ................................................................................................................ 217 V. Implications ....................................................................................................................................... 217 (1) Implications across ecosystems ................................................................................................... 217 (2) Conservation implications .......................................................................................................... 218 VI. Conclusions ....................................................................................................................................... 219 VII. Acknowledgements ............................................................................................................................ 219 VIII. References ......................................................................................................................................... 219 I. INTRODUCTION physiological, morphological, ecological and behavioural adaptation to terrestrial environments. For example, land Limitations on plant recruitment have been a popular crabs minimise water loss by inhabiting damp, deep avenue for ecological research (see Mu¨nzbergova´ & Herben, burrows, being active at night or in high humidity and 2005 and Hermy & Verheyen, 2007 for recent reviews), through the evolutionary development of lungs, in addition particularly in the tropical literature. Limited dispersal to gills, for gas exchange (McMahon & Burggren, 1988). (Hubbell et al., 1999), seed availability (e.g. Norden et al., Land crabs vary in their level of terrestrial adaptation, even 2007) and low microsite availability (e.g. de Steven & Wright, within one family. Discoplax (Cardisoma) species require 2002; Doust, Erskine & Lamb, 2006) are all known to regular immersion in water whereas Gecarcinus and Gecarcoi- minimize the number of successfully recruited individuals in dea species can obtain water from food, dew, or soil sub- tropical tree populations. Focusing on microsite limitation strata through absorption (Gecarcinidae; Hartnoll, 1988). alone, abiotic factors such as light (e.g. Kyereh, Swaine & Land crabs include one family of hermit crabs, Coenobi- Thompson, 1999; Uriarte et al., 2005), desiccation (e.g. tidae (Coenobita and Birgus), which are terrestrial as adults Veenendall et al., 1996), fire (Janzen, 1985), salinity and salt but like the majority of land crabs are planktonic as lar- spray (Ceron et al., 2002) and soil characteristics (Swaine, vae. Mangrove land crabs in the families Grapsidae 1996) all have been found to limit tropical tree recruitment. (Neosarmatium and Goniopsis) and Ocypodidae (Ucides) burrow In an examination of the literature, a large percentage (14 at or above the high tide line and are generally active out of out of 27) of studies found that abiotic conditions at the water during low tide or by climbing vegetation (Hartnoll, microsite lower growth rates and the probability of survival 1988). Land crab species which burrow and forage above (Lindquist, 2003). Of the same studies, ten also found that high tide or on the beach dunes are restricted to tropical predation or herbivory of seeds and seedlings had a signifi- and subtropical ecosystems because cold temperatures limit cant impact on tree recruitment. However, studies have their ability to survive while inactive in burrows and their mostly focused on insect and mammal seed predators (see foraging activity above ground (Wolcott, 1988). In this Janzen, 1971 for
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