Biol. Rev. (2009), , pp. 203–223. doi:10.1111/j.1469 ...poboyca/documentos/documento… · predation or herbivory of seeds and seedlings had a signifi-cant impact on tree recruitment

Biol. Rev. (2009), 84, pp. 203–223. 203doi: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

1Meredith College, Department of Biological Sciences, 3800 Hillsborough Street, Raleigh, North Carolina 27607, USA2U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Boulevard, Lafayette, Louisiana, 70506, USA3Department of Botany, La Trobe University, Bundoora, Victoria 3086, Australia4Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Victoria 3800, Australia5University of Redlands, Department of Environmental Studies, 1200 East Colton Avenue, P.O. Box 3080, Redlands, California 92373, USA6U.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 ...................................................................................................................................... 204II. 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 � 2009 Journal compilation � 2009 Cambridge Philosophical Society. No claim to original US government works

Cambridge Philosophical Society

BIOLOGICALREVIEWS

(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 ....................................................................................................................................... 219VII. Acknowledgements ............................................................................................................................ 219VIII. References ......................................................................................................................................... 219

I. INTRODUCTION

Limitations on plant recruitment have been a popularavenue for ecological research (see Munzbergova & Herben,2005 and Hermy & Verheyen, 2007 for recent reviews),particularly in the tropical literature. Limited dispersal(Hubbell et al., 1999), seed availability (e.g. Norden et al.,2007) and low microsite availability (e.g. de Steven &Wright,2002; Doust, Erskine & Lamb, 2006) are all known tominimize the number of successfully recruited individuals intropical tree populations. Focusing on microsite limitationalone, abiotic factors such as light (e.g. Kyereh, Swaine &Thompson, 1999; Uriarte et al., 2005), desiccation (e.g.Veenendall et al., 1996), fire (Janzen, 1985), salinity and saltspray (Ceron et al., 2002) and soil characteristics (Swaine,1996) all have been found to limit tropical tree recruitment.In an examination of the literature, a large percentage (14out of 27) of studies found that abiotic conditions at themicrosite lower growth rates and the probability of survival(Lindquist, 2003). Of the same studies, ten also found thatpredation or herbivory of seeds and seedlings had a signifi-cant impact on tree recruitment. However, studies havemostly focused on insect and mammal seed predators (seeJanzen, 1971 for insects; Silman, Terborgh &Kiltie, 2003 formammals) and herbivores (see Coley & Barone, 1996 fora review).Here we focus on defining the mechanisms by which

a poorly exposed group of seed predators and herbivores,the land crabs, affect recruitment of tree species in tropicalcoastal forests. Prior to the early 1990s, the impact of landcrabs on plant communities was not well known (Wolcott,1988). Since the publication of Biology of the Land Crabs(Burggren & McMahon, 1988), investigators have advancedour understanding of the ecological role of land crabs intropical coastal ecosystems through a combination ofdescriptive and manipulative experiments. Our review isthe first to synthesise the findings made by these land crabstudies over the last 20 years.We define land crabs following Hartnoll (1988). Land

crabs are crabs which are able to remain active outsideof water for an extended period of time because of

physiological, morphological, ecological and behaviouraladaptation to terrestrial environments. For example, landcrabs minimise water loss by inhabiting damp, deepburrows, being active at night or in high humidity andthrough the evolutionary development of lungs, in additionto gills, for gas exchange (McMahon & Burggren, 1988).Land crabs vary in their level of terrestrial adaptation, evenwithin one family. Discoplax (Cardisoma) species requireregular immersion in water whereas Gecarcinus and Gecarcoi-dea species can obtain water from food, dew, or soil sub-strata through absorption (Gecarcinidae; Hartnoll, 1988).Land crabs include one family of hermit crabs, Coenobi-tidae (Coenobita and Birgus), which are terrestrial as adultsbut like the majority of land crabs are planktonic as lar-vae. Mangrove land crabs in the families Grapsidae(Neosarmatium and Goniopsis) and Ocypodidae (Ucides) burrowat or above the high tide line and are generally active out ofwater during low tide or by climbing vegetation (Hartnoll,1988). Land crab species which burrow and forage abovehigh tide or on the beach dunes are restricted to tropicaland subtropical ecosystems because cold temperatures limittheir ability to survive while inactive in burrows and theirforaging activity above ground (Wolcott, 1988). In thisreview we focus on land crab species which inhabit tropicalecosystems because the majority of research on the impactof crabs on forest recruitment has focused on these habitats.

Land crabs are found in tropical coastal ecosystemsaround the world. Information on the role of abiotic factorsin controlling plant growth in these systems is abundant. Weargue that in addition to environmental gradients, coastalecosystems share a biotic factor, land crabs, which can haveas much, or more, of an effect on plant recruitment. Studiesthat focus on the environmental gradients of coastal systemsminimise, by often ignoring, the important role of landcrabs. Through excavation of burrows (Guti�errez et al.,2006), collection of leaf litter in burrows (O’Dowd & Lake,1989; Sherman, 2003) and predation of seeds and seedlings(e.g. Smith, 1987c; Cannicci et al., 2008), land crabsdetermine the quantity, and sometimes the quality (species),of tropical coastal forest recruitment. The relative effects ofthese local abiotic and biotic factors on forest recruitment in

Erin S. Lindquist and others204


relation to larger scale factors can be represented by a groupof nested filters (Fig. 1). Ecological filters, such as crabpredation on seeds or seedlings (a local biotic condition) andsoil salinity (a local abiotic condition), cause mortality ofrecruits as individuals pass from one life stage to another. Bycausing differential species mortality by selecting particularspecies’ traits, ecological filters can impact the speciescomposition of communities (see Statzner, Dol�edec &Hugueny, 2004 for a review).

To contrast the role of land crabs against abiotic factorsin forest ecosystems, we selected three tropical coastalecosystems: mangroves, island maritime forests and main-land coastal terrestrial forests. These systems vary greatly inthe strength of their environmental gradients (Table 1). Forexample, mainland coastal terrestrial forests experienceseasonal droughts and floods but do not have significant

salinity gradients (Lindquist & Carroll, 2004). Conversely,salinity and water depth can dominate tree establishmentin mangroves, but drought and rain-induced flooding bythemselves are seldom important to plant recruitmentexcept for their linkages to salinity and propagule dispersal(Sousa et al., 2007). These ecosystems also differ in theprevalence and diversity of land crabs. Land crabs representa significant proportion of the faunal biomass in all threeecosystems (Table 2), but their densities are highest in islandand mainland maritime forests and they are most speciosein mangroves. Tree species richness varies among theseecosystems with mangroves having the fewest species, islandmaritime forests intermediate and mainland coastal terres-trial forests the most.

While considering these variations in the tree andcrab assemblages (Table 2) and environmental gradients(Table 1), we review here how the positive and negativeimpacts of crabs on tree recruitment are shared across threetypes of tropical coastal ecosystems. In order to highlightthese similarities, we present our findings in a systematicorder: (1) crab predation of seeds, propagules or fruits; (2)crab predation of seedlings; (3) spatial variation in crabpredation; (4) temporal variation in crab predation, and (5)crab predation, or filter, interactions with other factorsinfluencing forest structure and composition. By highlight-ing one shared, limiting factor in these ecosystems, we hopeto encourage other investigators to find commonality intheir studies investigating limitations in plant recruitmentand their effects on the structure and composition of forestecosystems.

Pool of species

Pool of species

Climate

Landscape

Local abiotic conditions

Local biotic conditions

A

Climate

Landscape

Local biotic conditions

Local abiotic conditions

B

Fig. 1. Schematic diagram of the effects of ecological filters onrecruitment of species (after Poff, 1997). The presence andabundance of species (represented by black lines) is determinedby their ability to pass through multiple filters (represented byovals). Filters are placed in a hierarchy based on the ability tolimit recruitment; the upper filters (i.e. climate and landscape)limit recruitment more than the lower filters (i.e. local abioticand biotic conditions). Any species that lacks traits which wouldallow it to pass through an upper filter will not be available topass through the lower filters. Previous tropical coastal forestliterature has argued that the upper diagram (A) is mostrepresentative of tree recruitment limitation. We argue thatwhere crabs are present, the lower scheme (B) is morerepresentative; crabs, as biotic filters, may limit tree recruit-ment as much or more than local abiotic conditions.

Table 1. Ecosystem comparison of coastal gradients amongmangrove, island maritime and mainland coastal terrestrialforests. ‘]’ signifies that the factor varies (direction nonspecific)relative to the coastal gradient (distance from shore or tide) ina particular system, ‘‘o’’ signifies that the factor does not varywith the gradient and ‘‘na’’ signifies not yet investigated insystem or data are inconclusive.

Factor for comparison, relativeto distance from shore or tide Mangrove Island Mainland

Physical environmentSalinity ] o oFlooding ] o oSoil texture, type, nutrientavailability

] ] ]

Light, canopy cover ] ] ]Forest structure and compositionTree density (juvenilesand adults)

o o ]

Tree size-class distribution ] o ]Tree species distribution ] ] ]

Crab assemblageDensity ] o ]Species distribution ] o ]Temporal activity na o ]Seed or propagule predation ],o o ], oSeedling predation ] o ], oLitter removal ] o ]

Land crabs and tropical forest recruitment 205


Table

2.Comparisonofthreetropicalcoastalecosystem

s(m

angroves,islandmaritimeforestsandmainlandcoastalterrestrialforests)for:(I)trophicassem

blages

including

trees,crabsandnaturalenem

iesofcrabs;(II)ecologicaleffectsontree

recruitmentincludingseedsorpropagule

predation,seedlingpredation,litter

removalandsoil

manipulation;(III)spatialvariationofcrabpredationrelative

tothetidal/coastallocationandcanopycover;and(IV)temporalvariationofcrabpredationrelative

totime

ofday,seasonandyear.

Mangroves

Islands

Mainland

I.Trophic

assemblages:

Treespeciesrichness

d1-7

speciesin

Neotropics

(Chapman,1976)

d3-5

tree

speciesonEnew

etakAtoll,

MarshallIslands(Louda&

Zedler,1985)

d600-700tree

speciesin

Corcovado,Costa

Rica(Q

uesadaetal.,1997)

d18-21speciesin

Indo-

South-Pacific(Duke,2006)

dApprox.50canopytree

species

onChristmasIsland,IndianOcean

(Green

etal.,1997)

d60-150tree

and250

plantspeciesin

CaboBlanco,CostaRica

(Lindquist,2003;Camacho-C�espedes

&Lindquist,2007)

Crabdensities

1dGrapsidcrabsalong

MurrayRiver,NEAustralia:

0-2

m-2(0.77crabsper

trap

night)(Frusher

etal.,1994)

dGecarcoidea

natalisonChristmasIsland:

0.2-2.5

crabsm

-2(G

reen

etal.,1997)

dGecarcinuslateralisatLaMancha,Mexico:

0.5-1.0

crabsm

-2(Kellm

an&

Delfosse,1993)

dXanthid

crabsin

Rookery

Bay,FLUSA:0.3

–4m

-2

(4.17crabsper

trapnight)

(McIvor&

Smith,1995)

dGecarcinusplanatus

onClippertonAtoll:6.0

crabsm

-2(Ehrhardt&

Niaussat,1970),

andupto

0.8

m-2onSocorroIsland,

Mexcio(Jim

�enez

etal.,1994;Perez-C

hi,

2005).

dGecarcinusquadratusin

Corcovado,Costa

Rica:0–2.5

crabsm

-2(Sherman,2002)

dGecarcinusquadratusin

CaboBlanco,Costa

Rica:0.8

–3.3

crabsm

-2(Lindquist&

Carroll,2004)

dCardisomaguanhumiin

SE

FloridaUSA:1.85per

m-2

(Herreid

&Gifford,1963)

dGecarcinusruricolaonSanAndresand

ProvidenciaIslands:0.08-0.21crabs

m-2(H

artnolletal.,2006)

dGecarcinuslateralisin

Veracruz,

Mexico:0.5

crabsm

-2(Capistran-Barradasetal.,2003)

dUca

annulipesin

EastAfrica:

10-175per

m-2(Skovetal.,

2002)

dCardisomaguanhumiin

South

Florida:

1.8

crabsm

-2(G

ifford,1962)

dNeosarmatiummeinertiin

East

Africa:;5per

m-2

(Skovetal.,2002)

dCardisomaguanhumionAndrosIsland

(Bahamas):1.0

crabsm

-2(Lutz

&Austin,1983)

dCardisomacarnifex

onAldabra

(Indian

Ocean):0.4

crabsm

-2(Alexander,1979)

andIfaluk(CarolineIs.):1.2

crabsm

-2

(Bates&

Abbott,1958)

Naturalenemies

ofcrabs

dHerons,ibis,raccoons,humans

(Diele

etal.,2005)

dIntraguildpredation(Birguslatroon

Gecarcoidea

natalis)onChristmasIsland

(Hicks

etal.,1990)

dRaccoons,coatis,cats,foxes,birdsofprey,

heronsin

CostaRica(Sherman2002;

Lindquist&

Carroll,2004)

dIntroducedpigsandratsonGecarcinus

planatus

onClippertonAtoll(Pitman

etal.,2005)

dFlightlessrailsonlandhermitcrabson

Aldabra

(Alexander,1979).

dEndem

icbirdsincludingyellow

crowned

nightheronNyctanassaviolacea

gravirostrison

Socorro(P�erez-C

hi,2005)

II.Ecologicaleffects

ontreerecruitment:

%seedorpropagule

predation(removal)

d0-100%

propagule

predation

dependentonspeciesandlocation

(Smith,1987c;

Smithetal.,1989)

d0-100%

destroyedbyhermitcrabs(Coenobita

perlatus)onEnew

etakAtoll,MarshallIslands

(Louda&

Zedler,1985)

d40%

removedin

CaboBlanco,Costa

Rica(Lindquist&

Carroll,2004)



d54.3%

propagule

predation

(Allen

etal.,2003)

d>80%

handledand47%

destroyedby

Gecarcoidea

natalisonChristmasIsland(0-94%

byseed

species;Green

etal.,1997)

Seedlingpredation

dNodamageto

seedlings

(Siddiqi,1995)

dGecarcoidea

natalisgrazedon25seedling

species;seedlingdensity

was20-fold

higher,

andseedlingrichnesswasfive-fold

higher

incrabexclosuresthanin

unfenced

controlplots(O

’Dowd&

Lake,1990;

Green

etal.,1997)

dSeedlingdensity

increased144%

incrabexclosures(Sherman,2002)

dCotyledonsremovedfrom

Avicenniaseedlings

(Smith,1987b)

d74-100%

seedlingremovaloutsideof

exclosures(Lindquist&

Carroll,2004)

Litterremoval

dLitterremovalandburialbycrabs

isim

portantin

nutrientcycling

(Robertson,1986)

dGecarcoidea

natalisprocesses

39-87%

ofannual

leaflitterfallonChristmasIsland

(Green

etal.,1999b)

d;Five-fold

higher

litter

massin

crab

exclosuresthanin

open

plots

(Kellm

an&

Delfosse,

1993)

dInfluence

oflitter

removalon

propagule

establishmenthas

notbeenstudied.

d5.6

times

higher

leaflitter

accumulationin

crabexclosuresthanin

controls

(Sherman,2003)

Soil

manipulation

dElevate

soils5-15cm

(Minchinton,2001)

dGecarcoidea

natalisrelocatesleaflitter

onand

into

burrows;meanturnovertime

ofburrow

>4.4

years

(O’D

owd&

Lake,

1989;Green,2004)

dCrabburrowsnutrient-andcarbon-rich;

plantrootdensities

higher

around

burrow

microsites(Sherman,2006)

dSoilsulphide&

ammonium

levelsare

lowered

bycrab

burrowing(Smithetal.,1991)

III.Spatialvariationofcrabpredationrelativeto:

Locationrelativeto

tide/coastline

dDependentonspeciesof

propagule

(Osborne&

Smith,1990)

dNovariationrelative

tocoastallowlandand

inlandplateauforest(G

reen

etal.,2008)

dHigher

incoastalzone(0-100m

from

coast)thanin

inlandzone(>100m

from

coast)(Lindquist&

Carroll,2004)

dHigher

inlower

intertidal

(Sousa

&Mitchell,1999)

dNodifferencesrelative

totidalposition(Clarke&

Myerscough,1993;Allen

etal.,2003)

dDensity

ofGecarcinusplanatus

highatlow

and

highaltitude,

andlow

atmid-altitudes,

onSocorroIsland(Perez-C

hi,2005)

Canopycover

dHigher

inunderstorey;

lower

inlargegaps

(Osborne&

Smith,1990;

Clarke&

Kerrigan,2002;

Clarke,

2004)

dNodifference

incrabdensities

andseedling

predationin

shaded

understoreyandin

lightgaps(G

reen

etal.,1997)

dNodifference

inseed

andseedlingremoval

bycrabsbetweengapsandunderstorey

sites(Lindquist&

Carroll,2004)

dNochangerelative

togap

size

orunderstorey(Sousa

&Mitchell,1999;Allen

etal.,

2003;Krauss

&Allen,2003)

dLower

crabdensities

insparsecanopy

cover(effectonseed/seedlingpredation

unknown;Jim�enez

etal.,1994)

IV.Temporalvariationofcrabpredationrelativeto:

Tim

eofday

dCrabactivitydetermined

more

bystageoftidethantimeofday

(Frusher

etal.,1994)

dGecarcoidea

natalisisdiurnalonChristmas

Island;activityispositively

correlatedwith

relative

humidity(G

reen,1997)

dGecarcinusquadratusprimarily

nocturnal

(Sherman,2002;Lindquist&

Carroll,2004)



II. MANGROVES

Crabs influence many aspects of mangrove communitydynamics by facilitating the conversion of organic nitrogento ammonia (Alongi, Boto & Robertson, 1992), promotingdecomposition of organic matter (Robertson & Daniel, 1989;Micheli,Gherardi &Vannini, 1991; Lee, 1998), grazing on leafmaterial (Onuf, Teal & Valiela, 1977; Beever, Simberloff &King, 1979), aerating anoxic soils through burrowing (Smithet al., 1991) and altering soil microtopography by creatingmounds (Warren & Underwood, 1986; Minchinton, 2001). Inaddition, predation of propagules and seeds by crabs can beextremely important in controlling recruitment (Smith, 1987c;Allen, Krauss & Hauff, 2003).

Of the 70 distinct mangrove species or hybrids in the world(Duke, Ball & Ellison, 1998), an individual mangrove forestcommonly has one to seven species in the Neotropics(Chapman, 1976) but as many as 18 to 21 species in thetropics of Malaysia and Australia (Watson, 1928; Ball, 1998;Duke, 2006). Also, mangroves often occur as visibly distinctbands in many locales and there is strong evidence thatpredator guilds exert pressure on mangrove recruitment(Smith et al., 1989). Accordingly, environmental stress hasdirect effects on the distribution of both mangroves (Krausset al., 2008) and crabs (Frusher, Giddins & Smith, 1994); attimes both must cope with low oxygen levels, high tem-perature and desiccation (Hogarth, 1999). As the distributionof crabs changes along these environmental gradients, crabscan exert a differential influence on mangrove seed ger-mination or propagule growth initiation through directconsumption, damage or burial (Smith, 1987a,b).

The dominant members of the crab fauna in mangrovesbelong to the families Gecarcinidae, Grapsidae and Ocypo-didae. The grapsid crabs are the primary consumers ofpropagules in the Indo-West-Pacific region. In the easternPacific, Atlantic andCaribbean the gecarcinids (e.g.Cardisomaspp.) and Ocypodids (e.g. Ucides spp.) are more importantthan the grapsids (Twilley et al., 1997; Diele, Koch & Saint-Paul, 2005).

(1) Propagule predation

Among studies conducted globally, crabs destroyed 54.3%(^ 31% S.D.) of seeds or propagules falling to the man-grove forest floor (Allen et al., 2003). Much research at-tention has been given to this influence, with general trendssuggesting that predation is related variously to the chemi-cal composition of propagules (McKee, 1995; Smith, 1987c;Allen et al., 2003), related negatively to propagule density(Sousa & Mitchell, 1999; Krauss & Allen, 2003; but seeSmith, 1988), and unrelated to whether predation occurs insmall canopy gaps or under a forest canopy (Sousa &Mitchell, 1999; Krauss & Allen, 2003; Allen et al., 2003;Clarke, 2004; but see Osborne & Smith, 1990). Central tomany predation studies are tests of what has become knownas the dominance-predation hypothesis (Smith, 1987c). Thishypothesis suggests that selective predation by crabs pre-vents preferred tree species from establishing and becomingdominant at particular points along the tidal gradient.T

able

2.(cont.)

Mangroves

Islands

Mainland

dPlasticityin

dielactivityin

Gecarcinusplanatus

onSocorroIsland(Jim

enez

etal.,1994;

P�erez-C

hi,2005)andG.lalandiionJarak

Island,Malaysia

(Audy,1950)

dGecarcinuslateralisprimarily

diurnal

(Kellm

an&

Delfosse,

1993;Capistran-

Barradasetal.,2003)

Season

dIncreasedwithavailabilityof

propagules(Robertson,1986)

dIncreasedin

wet

seasonwhen

humidityis

highandseed/seedlingavailabilityishigh

(Green

etal.,1997)

dIncreasedin

wet

seasonwhen

humidity/

rainfallishighandseed/seedling

availabilityishigh(Capistran-Barradas

etal.,2003;Sherman,2003;Lindquist&

Carroll,2004)

Supra-annual

dCrababundancescanvary

annually(Conde&

Diaz,

1989),buttheim

pact

on

propagule

predationand

seedlingestablishmentis

unknown

dAnnualperiodicityin

crabdensities

may

allow

pulses

oftree

recruitmentin

low

crabyears

(Green

etal.,1997,2008)

dAnnualperiodicityin

crabdensities

may

allow

pulses

oftree

recruitmentin

low

crabyears

(Sherman,2002;Lindquist&

Carroll,2004)

1See

Green

(1997)foranadditionalreview

ofgecarcinid

landcrabdensities

inislandandmainlandcoastalforests.



Several papers fail to support this hypothesis conclusively(c.f., McKee, 1995; McGuinness, 1997; Sousa & Mitchell,1999; Clarke & Kerrigan, 2002), however many do notfollow the fate of propagules through to establishment. Forexample, predation of Xylocarpus granatum seeds did notdiffer under forests with different overstorey compositions,but establishment, measured after 161 days, was greaterin forests with X. granatum in the overstorey (Allen et al.,2003). This result leaves the possibility of either differen-tial consumption of seeds among habitats, or differentialenvironmental factors as possible explanations for thespatial distributions of tree species. In all, studies haveindicated a large range of strategies among crabs, fromalmost completely non-selective feeding by Neosarmatiummeinerti (Dahdouh-Guebas et al., 1997) to strongly selectiveassociations whereby crabs only consume propagules frommangrove species foreign to a particular site (Clarke &Kerrigan, 2002).

Some mangroves with small propagules and highnutritive quality (e.g. Avicennia spp.) are heavily consumedby crabs. For these species, propagules are often excludedcompletely from some intertidal zones (Smith et al., 1989).Other studies have also reported strong susceptibility ofAvicennia spp., and other small-seeded species, to crabpredation (McKee, 1995; Sousa & Mitchell, 1999; Clarke &Kerrigan, 2002). It is likely that the dominance-predationmodel may apply strongest to mangrove species that arehighly palatable and easily killed, and, hence, in specieswhere crab diet selectivity is most intense.

(2) Seedling predation

Few studies have assessed the effects that partial crab pre-dation, or herbivory in the case of seedlings, has on thesurvival of mangrove seedlings. It is common to assume that50% consumption of the vegetative portion of propagules orthe loss of a plumule equates to mortality (see Smith, 1987cfor propagules; but see Allen et al., 2003 for seeds).However, insect herbivory studies offer some insight intothe resiliency of seedlings to attack on propagules and loss ofbiomass. Insect herbivory is widespread on mangrovepropagules both before and after dispersal (Robertson,Giddens & Smith, 1990; Farnsworth & Ellison, 1997;Minchinton, 2006), and can have varying effects on thegrowth of seedlings. For example, insects reduced growth inAvicennia germinans slightly, but either had no effect onindividual seedlings of Laguncularia racemosa or completelystalled the growth of individual plants (Sousa, Kennedy &Mitchell, 2003a; Sousa, Quek & Mitchell, 2003b). Height orbiomass increments for seedlings of Avicennia marina,Bruguiera exaristata, Xylocarpus australasicus and Xylocarpusgranatum were reduced by insect damage, but survival wasaffected only in the latter two species (Robertson et al.,1990). Generally, survival and establishment are affectedless often than growth for seedlings with herbivore-damagedpropagules, though determining limits of sublethal tissuedamage is difficult and can vary widely by species (Sousaet al., 2003a). Minchinton (2006) reported that pre-dispersalherbivory by insect larvae on A. marina propagules did not

prevent establishment; it did, however, have negative effectson establishment with increasing dispersal distance and thuscould limit long-distance supply of propagules. In somecases, the annual cycle of insects into and out of seedlingscommonly results in mortality, as reported for the beetleCoccotrypes rhizophorae on Rhizophora mangle in Panama (Sousaet al., 2003b) and in Florida, USA (Devlin, 2004). What ismore certain, however, is that cotyledon consumption byany vector reduces energy reserves needed for optimalinitial growth of mangrove seedlings (Minchinton & Dalby-Ball, 2001; Sousa et al., 2003a).

The mechanisms of attack by insects versus crabs, how-ever, are very different. Many insects bore small holes intothe propagule (i.e. viviparous seedlings that germinate onthe parent tree prior to dispersal) to remove internal por-tions of the seedling not associated with water-conductingxylem tissue. Crabs, on the other hand, typically removelarge outer portions of the propagule to get to the inner,more palatable portions. Yet, the effect of both insect andcrab herbivores can be similar for seed-producing man-grove species. Both herbivores are responsible for killingXylocarpus granatum seeds in experimental studies (Robertsonet al., 1990; Allen et al., 2003), presumably to benefit fromthe 50% increase in crude protein, 105% increase in crudefat, 23% increase in total carbohydrates, and 22% decreasein crude fibre content of cotyledon material versus entire X.granatum seed (Allen et al., 2003). On the other hand,mangroves that produce propagules may have much lessdifficulty than seed producers in ameliorating mortalityfrom crab damage once seedlings are established. Forexample, crabs did not cause damage to mangrove seedlingsplanted in Bangladesh, in which only six out of 336propagule seedlings died outside of crab exclosures while 11died within exclosures (Siddiqi, 1995).

(3) Spatial variation

Spatial variation in predation on propagules and seeds hasfocused on two principal topics, intertidal location (e.g.upper, middle, and lower intertidal; Fig. 2A) and canopyposition (i.e. gap versus understorey). Predation can varyconsiderably with spatial shifts in intertidal position as thedegree of tidal inundation affects exposure time of seeds andpropagules on the soil surface (Osborne & Smith, 1990) andinfluences the abundance of crab predators. Because speciescomposition often changes at different intertidal locations,many tests of the dominance-predation hypothesis de-scribed above are also tests for predation differences amongintertidal location. Panamanian mangroves, for example,have greater propagule predation in lower intertidallocations than in upper or middle intertidal locations(Sousa & Mitchell, 1999). In that same study, larger crabs,such as Ucides cordatus and Goniopsis cruentata, were bettersuited to propagule grazing and were common in lowerintertidal locations; detritivore species predominated inmid-to-upper intertidal locations. Crab predators removedmore Bruguiera gymnorrhiza propagules in low than in middleintertidal locations on a Pacific island (Krauss & Allen,2003; Fig. 2B), more Aegiceras corniculatum propagules in high



than in low intertidal locations in Australia (Osborne &Smith, 1990) and more Avicennia germinans propagules ina salt marsh zone than mangrove zone in Louisiana, USA(Patterson, McKee & Mendelssohn, 1997). Several studiesindicate variable patterns of loss by species with intertidallocation (Smith, 1987c, 1988; Dahdouh-Guebas et al., 1998;Clarke & Kerrigan, 2002) and some show no differences inpredation by intertidal location (Clarke & Myerscough,1993; Allen et al., 2003; Fig. 2B).By canopy position, predation was higher in understorey

locations than in canopy gaps for Avicennia marina and lessin large canopy gaps (> 600 m2) than in small canopy gaps(< 300 m2) (Osborne & Smith, 1990). Interestingly, thesepatterns mimic herbivory by the beetle Coccotrypes rhizophoraein Panama (Sousa et al., 2003b); large gaps appear to serveas refugia for propagules from predation by crabs andherbivory by insects. Both Clarke & Kerrigan (2002) andClarke (2004) found additional support for the gap refugiahypothesis relative to crab predation in that morepropagules were killed by crabs under forest canopies thanin large light gaps. Mechanistically, larger gaps have greaterirradiance which, in turn, increases the temperature of thesoil (Smith, 1987c). Some experiments, on the other hand,

indicate no differences in rates of predation by canopy po-sition (Sousa & Mitchell, 1999; Allen et al., 2003; Krauss &Allen, 2003; Fig. 2B). The reasons for this result are unclearat present and warrant further research.

Crabs can also alter the spatial distribution and growthpotential of mangroves. By serving as ecosystem engineers(see Jones, Lawton & Shachak, 1994), crabs can havea profound effect on soil microtopography. Elevationchange in most mangrove forests is minimal and bestmeasured in centimeters or tenths of meters along the entireintertidal range (Macnae, 1969b; Thom, 1982; Woodroffe,1992). Some species of crabs create large mounds whileexcavating burrows. These mounds can range in area from0.5 to 1.0 m2 (Minchinton, 2001). Atop these mounds, thesoil elevation can be as much as 5-15 cm or more higherthan surrounding soil and facilitate the establishment ofmangrove species better adapted to lower frequencies oftidal inundation, reduced flood durations and higher soiloxygen status. Similarly, the mud lobster (Thalassina anomala)can alter soil elevations by as much as 1-2 m (Macnae,1969a). Mangrove species richness is observably greater ontop of such mounds in Palau and Papua New Guinea (K.W.Krauss and T.J. Smith III, personal observations). In Papua

Fig. 2. (A) Cross section of the intertidal distribution for dominant species studied in Micronesia (after Tomlinson, 1986), and (B)predation of Bruguiera gymnorrhiza and Xylocarpus granatum across this gradient in one Micronesian mangrove forest (data after Krauss& Allen, 2003; Allen et al., 2003). Predation for B. gymnorrhiza propagules was reduced in the middle intertidal where the speciesmaintains dominance in the overstorey. Trends were not significant for Xylocarpus granatum, even though X. granatum is a dominantcomponent of the upper intertidal overstorey. No differences were apparent for comparisons of understorey (shaded bars) versus gap(open bars) locations within intertidal zone. Predation assessments followed by the same letter among intertidal zone for eachspecies are not significantly different at P ¼ 0.05. Values are means ^ 1 S.E. (N ¼ 18, % out of 12 propagules in each plot).



New Guinea, as many as 250 T. anomala mounds can befound per hectare, each having a mean size of 15 m2 andcomprising greater than 20% of total mangrove area (T.J.Smith III, unpublished observations). In addition, crab-freemangrove zones have higher soil sulphide and ammoniumlevels, which have also been associated with reducedmangrove growth (Smith et al., 1991). In fact, Minchinton(2001) argues that on sites where crabs are removed bya disturbance (e.g. oil spill), the site will have higher mangroveestablishment and growth rates once those crabs recolonise.

(4) Temporal variation

Timing of propagule production was important on a coralcay in Belize, where most propagule consumption by crabswas evident at the beginning of major periods of propagulefall and dispersal (McKee, 1995). Though mangroves aretropical and often produce seeds or propagules in somecapacity throughout the year (Williams, Bunt & Duke, 1981;Twilley et al., 1997), there are often periods of time withmajor inputs. This was the case for propagule predationstudies conducted in Panama (Sousa & Mitchell, 1999),Micronesia (Krauss & Allen, 2003) and Africa (Dahdouh-Guebas et al., 1998), in which quantifying absolute rates ofpropagule loss to crabs may have been affected by theavailability of large quantities of propagules on the ground.Studies are often designed to correspond to these peaks,however, because we also expect crabs to have life-historystrategies that take advantage of seasonal peaks inpropagule production. Robertson (1986) observed thatcrabs decreased their consumption of fallen leaves aspropagules became available; the crabs were eating thepropagules during this time of year and not the leaves.Smith (1988), however, found that propagule density did notaffect predation in at least one Australian system. Singlepropagules, and propagules in piles of 10 or 100, of bothAvicennia marina and Bruguiera sexangula, were equally likely tobe consumed, regardless of predator density (Smith, 1988).

(5) Crab filter interactions

Interactive effects among canopy position, intertidal lo-cation and predator guilds are common in mangroves. Forexample, the relative importance of predation on prop-agules under the forest canopy versus in a gap was significantfor Aegiceras corniculatum in the lower intertidal zone only, andnot in the upper intertidal zone (Osborne & Smith, 1990).Propagule decay and predation by both crabs and snailshad a greater effect on recruitment of Avicennia germinansonto Spartina alterniflora marshes than recruitment intoAvicennia zones (Patterson et al., 1997).

An even more complex interaction involves alterationsof soil conditions by vegetation, which in turn can affectdensities and foraging activities of crabs. Canopy cover andlarge root densities facilitate mangrove species recruitmentby altering the physico-chemical status of the soil (Gleason,Ewel & Hue, 2003). This alteration, in turn, is moreconducive to crab colonisation (Minchinton, 2001). Al-though mangrove species establishment and growth are

enhanced by the more favourable soil conditions in theforest and by re-working of soils by crabs, crabs can alsoserve as a detriment to the establishment of mangrovespecies through predation. Once an insect component isadded, the relationship becomes even more complex.Insect-related mortality, which is also related to soilconditions and light, can be as high as 72% under a forestcanopy versus 10% in a gap (Sousa et al., 2003b). In situationswhere propagule densities are really high, insects may bemore effective predators than crabs (Robertson et al., 1990).

III. ISLAND MARITIME FORESTS

Land crabs are vital inhabitants of tropical oceanic islands(Ehrhardt & Niaussat, 1970; Alexander, 1979; Hicks,Rumpff & Yorkston, 1990; Jim�enez et al., 1994; Ashmole &Ashmole, 2000). Their abundances commonly exceedone crab per m2 and 1000 kg ha-1 (Green, 1997). Theirbiomass on some islands exceeds the total biomass ofanimals reported in tropical rain forests in Costa Rica (115kg ha-1; Odum et al., 1970) and the central Amazon (210 kgha-1; Fittkau & Klinge, 1973). Reasons proffered for thisdominance include ecological release in the absence ofnatural enemies and competitors, high reproductive poten-tial and the ability to survive on a low-quality diet (Green,1997). Omnivory, combined with a low metabolic rate, maybe the key to the success of land crabs in island maritimeforests (Green, O’Dowd & Lake, 1997). Land crabs straddlethree trophic levels and are free of many of themorphological and anatomical constraints that limit dietbreadth of most consumers (Yodzis, 1984).

Anecdotes that mention that land crabs eat seeds, fruitsand seedlings on islands are rife (Bourne, 1886; Guppy,1890; Borradaile, 1901; English, 1913; Howard, 1950;Degener & Gillaspy, 1955; Niering, 1956; Alexander, 1979).The influence of land crabs in insular plant dynamics hasbeen quantified only recently and in just three islandecosystems (Fanning Island – Lee, 1985, 1988; EnewetakAtoll – Louda & Zedler, 1985; Christmas Island, IndianOcean – O’Dowd & Lake, 1989, 1990, 1991; Green et al.,1997; Green, O’Dowd & Lake, 2008). Land crabs influenceinsular plant community membership in two fundamentalways. They shape the probability of colonisation from thepool of immigrants arriving at an island (Ridley, 1930;Louda & Zedler, 1985), or they mould communitymembership throughout succession (Alexander, 1979).Guppy (1906) attributed the early failure of Caesalpiniabonduc (a common drift seed) to establish on Anak Krakatauto the activities of land crabs. These crabs may assisttransport of sea-dispersed propagules from the shore to theinterior of islands (Ridley, 1930; Howard, 1950), but there islittle information on how land crabs influence the course ofprimary succession on islands, even in a well-studied systemlike Krakatau (Thornton, 1995). Given the superabundanceof land crabs on many islands, it is not surprising thatthey can consume a large fraction of seeds and seedlings(Louda & Zedler, 1985; Lee, 1988; O’Dowd & Lake, 1990,1991), affecting seedling recruitment (Green et al., 1997).



(1) Fruit and seed predation

In all cases where fruit and seed selection have beenexamined on islands, land crabs, including hermit andgecarcinid crabs, displayed a catholic but choosy diet. Landcrabs selectively remove fruits and seeds in controlledexperiments (Louda & Zedler, 1985; Lee, 1988; O’Dowd &Lake, 1991; Green et al., 1997) but this does not necessarilyindicate differential fate of seeds. Seeds may be removed butnot eaten, and thus have the potential to germinate aftercrab removal. However, seed fate experiments with the redland crab Gecarcoidea natalis in artificial burrows showeddifferential predation on seeds of 10 species (Green et al.,1997). Seed predation varied from 0 to 94% over severaldays. Physical protection and chemical deterrence wereboth likely to be important determinants of seed fate. Toughendocarps afforded complete protection to the seeds of twotree species. For the other eight species, variation in seedfate was probably related to both physical protection andchemical deterrence (O’Dowd & Lake, 1991). Seeds ofsome species are too small for land crabs to handle and theirsurvival probabilities on the forest floor remain unaffected.On Christmas Island, these species form a persistentseedbank whose abundance and relative species composi-tion is unaffected by even high densities of land crabs(Green et al., 1999a). These crabs did not inhibit theformation of a seedbank of 17,000 seeds m-2 of Muntingiacalabura, a tiny-seeded roadside weed. For larger seeds thatland crabs can handle, the vast majority are completelydestroyed and consumed (Green et al., 1997). However, landcrabs may be effective dispersal agents for seeds of a fewspecies with tough endocarps or chemical deterrents. Forexample, on Christmas Island, the seeds and seedlings ofInocarpus fagifer are positively associated with burrowentrances (O’Dowd & Lake, 1991), consistent withobservations by Ridley (1930) who commonly saw a dozenor more seedlings growing around burrow entrances. OnFanning Island, Lee (1985) found that seedlings of Pandanustectorius were, on average, further away from adults thanundispersed seeds. She attributed this dispersion pattern toseed dispersal by Cardisoma carnifex, but other factors such asseed predation by insects or limiting environmentalconditions near adults could be important, but were notaddressed in her study.


Strong evidence indicates that land crabs selectively con-sume seedlings in transplant experiments using cagedcontrols (O’Dowd & Lake, 1990; Green et al., 1997).Seedlings with higher nitrogen levels, fibre content andconcentrations of total phenols experienced higher survivor-ship, suggesting that selection of seedlings by G. natalis isdetermined by both structural and chemical attributes ofseedlings (O’Dowd & Lake, 1990). Green et al. (1997)showed significant differences in seedling survival for 12 ofthe 16 species examined. Seedlings are vulnerable to landcrab herbivory from germination to such a size where stemsare too woody or leaves are out of reach. This is certain tovary among species but has never been quantified.

These studies show that land crabs have a direct,differential effect on the survival of both the seed and youngseedling stages (Table 2). They may also act indirectlythrough their manipulation of leaf litter that is demonstrablyimportant to seedling recruitment (Molofsky & Augspurger,1992; Benitez-Malvido & Kossmann-Ferraz, 1999; Table 2).Red crabs consume a large fraction of the annual litter andseed input on Christmas Island, affecting litter cover andbiomass (O’Dowd & Lake, 1989; Green, O’Dowd & Lake,1999b). Their combined direct and indirect effect is bestdemonstrated through their exclusion from 25 m2 plotsfollowed by long-term (three or six years) monitoring ofseedling recruitment. In the absence of G. natalis, not only didseedling density and species richness increase approximately20-fold and fivefold (Fig. 3A,B), respectively, but also therewas a strong shift in seedling species composition. A sparseassemblage of only 1-3 species, largely unpalatable to G.natalis, populated the unfenced control plots in both coastallowland and upland plateau forest. These tree species alsooccurred on the exclusion plots, but an additional 10 to 12highly palatable species were found only in these exclusionplots. These initial differences have persisted for seven yearsand some of the earliest seedling recruits have grown intosaplings, and a few to reproductive age (Green et al., 2008).The compositional shifts were qualitatively consistent withpredictions from the simple cafeteria and seedling transplantexperiments. In this island maritime system, the red landcrab regulates the dynamics of seedling recruitment in-dependently of gradients including forest type, understoreylight environment, elevation and distance from the sea.


Unlike mangrove and mainland coastal terrestrial forests,few quantitative data are available to evaluate spatialvariation in the strength of the effect of land crabs onseedling recruitment on islands. Nevertheless, crab densitiesvary within and between islands (Jim�enez et al., 1994; Greenet al., 1997; P�erez-Chi, 2005); therefore, the strength of theeffect may vary accordingly. Local patchiness in the densityof Gecarcinus planatus on Socorro Island is driven by habitatpatchiness; crab densities have been found to be lower inareas with sparse canopy cover (Jim�enez et al., 1994), orrocky substrata (P�erez-Chi, 2005). On Christmas Island,however, variation in land crab abundance is not related toedaphic factors or distance from the sea (P.T. Green,unpublished observations) and may be primarily a conse-quence of variation in migration routes of adults andemergence sites of juvenile crabs. Although the underlyingreasons for density variation remain obscure, patchiness incrab densities may generate patchiness in seedling recruit-ment. However, patchiness may have little functionalsignificance for seedling recruitment if the crab density isuniversally sufficient to limit seedling recruitment. Theprobability of recruitment for many species is effectively nilover the observed range of crab density on the island (0.2 –2.5 burrows m-2) and it is only when the density of landcrabs has been artificially lowered, either through experi-mental exclusion (Green et al., 1997) or local extirpation by



an alien invader (O’Dowd, Green & Lake, 2003), that theseplant species can recruit (Fig. 3A,B).


On islands, land crab densities can vary diurnally (Audy,1950; Page & Willason, 1982; Jim�enez et al., 1994; Green,1997; P�erez-Chi, 2005) and seasonally (Hicks, 1985;O’Dowd & Lake, 1990; Green, 1997; P�erez-Chi, 2005).The only time during which land crabs can affect seedlingrecruitment dynamics directly is the period between seeddispersal and the attainment of a ‘‘crab-proof ’’ seedlingsize. This period is variable among seedling species buttypically will vary from weeks to months. Diurnal variationin crab density is unlikely to affect the probability of seed-ling recruitment, but seasonal variation in crab densities

could produce an ‘‘escape’’ window for some seedlingspecies. Because land crabs are sensitive to changes inrelative humidity any recruitment window could only occurduring extended dry periods. However, these are the sameconditions that produce seedling stress and high mortality.On Christmas Island, there is no evidence that seedlingrecruitment probabilities increase during the dry season(Green et al., 1997).

A decline in land crab densities over years or decades,especially where they have been sustained at high densities,may dictate patterns of seedling recruitment and may be theonly way in which seedlings of some species recruit. Fewdata are available to address this hypothesis. On ChristmasIsland, red land crabs represent a widespread biotic filter toseedling recruitment (Fig. 3). Their experimental exclusionresulted in the recruitment of carpets of seedlings of a suite

Upland plateau

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Fig. 3. The effect of the red land crab Gecarcoidea natalis on seedling (A) abundance, (B) species richness and (C) species compositionin coastal lowland and upland plateau rainforest types on Christmas Island, Indian Ocean. Red crabs were excluded from 4 or 5 25m2 plots at coastal and inland sites for either three or six years, respectively (Green et al., 1997, 2008). Values in A and B aremean ^ 1 S.E. Open symbols are control plots and solid symbols are exclusion plots. Average crab density on paired control plotswas 2.0 and 0.8 crabs per m2 at lowland and upland sites, respectively. For A, seedling abundance was significantly greater inexclusion plots in both lowland (t ¼ 7.67, df ¼ 3, P ¼ 0.005) and upland (t ¼ 8.67, df ¼ 4, P < 0.001) sites. For B, seedling speciesrichness was significantly greater in exclusion plots in both lowland (t ¼ 8.72, df ¼ 3, P ¼ 0.003) and upland (t ¼ 8.57, df ¼ 4, P ¼0.001) sites. For the Non-Metric Multidimensional Scaling (nMDS) ordination of species composition in C, Global R and ANOSIMP were 0.73 and 0.067 at the lowland site, and 0.55 and 0.008 at the upland site, respectively. For the lowland site, only two of thefour control plots had seedlings. The red crab, irrespective of forest type, distance from the ocean, and elevation, has an over-ridinginfluence on the dynamics of seedling recruitment.



of canopy tree species, many of which never recruited onunfenced control plots (Green et al., 1997, 2008). These treespecies are especially palatable to red crabs and theexperiment predicted that they should be a minor compo-nent of the forest canopy, which should otherwise bedominated by those few species whose seeds and seedlingsare resistant to red crabs. In fact, palatable species dominatethe forest canopy on Christmas Island, completely at oddswith the prediction of the exclusion experiments and thedominance-predation hypothesis applied to mangroves.However, the mismatch between the composition of thecanopy and seedlings in the presence of red crabs could bethe result of a decline in red crab density or activity. Long-term recruitment failure of juveniles, epizootic events orcatastrophic disturbance could cause abrupt or gradualchanges in crab densities but no historical evidence existsfor their occurrence.


Land crabs are susceptible to a wide range of verte-brate predators (Wolcott, 1988), but on islands theirsuperabundance suggests that they have few naturalenemies or competitors that can regulate populationabundance (Table 2). Native ants compete for food withland hermit crabs in the Bahamas (Morrison, 2002), butthere is no evidence that these interactions restrict crabdistribution and abundance, and thus the spatial gradient orpatchiness of their effect on plant recruitment. However,novel interactions between crabs and invasive alienpredators and competitors make these ecosystems vulner-able to rapid state shifts. If crab densities are severelyreduced by an introduced species, these island maritimeforests have no other similar dominant seed and seedlingpredator. Plant recruitment, therefore, could be releasedfrom the natural crab filter (Denslow, 2003). On ChristmasIsland, an invasive alien crazy ant (Anoplolepis gracilipes) hascaused a rapid state change in the rainforest seedlingcommunity driven by its extirpation of the native red landcrab across the island (O’Dowd et al., 2003). Thisintroduced ant is also a predator of land crabs in theSeychelles (Feare, 1999; Gerlach, 2004) and South Pacificislands (Lester & Tavite, 2004).

IV. MAINLAND COASTAL TERRESTRIALFORESTS

Mainland coastal terrestrial forests possess higher diversityof trees and other woody plants than mangroves and mostisland communities (Table 2). On the Osa Peninsula ofCosta Rica for example, over 2100 species of plants fromover 185 families have been documented with an estimated600 to 700 tree species (Quesada et al., 1997). In markedcomparison to these mainland coastal terrestrial forests, theisland maritime forest community of Christmas Islandcontains approximately 50 canopy tree species (Green et al.,1997; Table 2). Forest stand structures, however, are com-

parable in terms of tree density (approximately 400 stems/ha), basal area (approximately 50 m2/ha) and height(approximately 45 m) (Green et al., 1997; Lindquist &Carroll, 2004). Even with a larger pool of tree species,mainland coastal terrestrial forests show distinct zonation inthe distribution, density and size structure of tree speciesrelative to distance from shore similar to that found inmangrove ecosystems (Sherman, 2002; Lindquist & Carroll,2004; Table 1; Fig. 4A,B).

Land crab populations in mainland coastal terrestrialforests are less speciose than those of mangroves, yetmaintain similar densities to those on islands and inmangroves (Table 2). In two Costa Rican mainland coastalterrestrial forests (Corcovado National Park, Osa Peninsula,Sherman, 2002; Cabo Blanco Absolute Nature Reserve,Nicoya Peninsula, Lindquist & Carroll, 2004), Gecarcinusquadratus (Harlequin land crab, Gecarcinidae) densitiesdecrease with increased distance from the coastline. InCorcovado, the crab zone extends from the shore toapproximately 600 m inland at which point the substrateshifts from sandy loam to clay and burrowing activity ceasescompletely (Sherman, 2002). Within the crab zone, adultpopulation densities are patchy ranging from 0 to 2.5 m-2

with the highest burrow densities adjacent to buttressingroots of large trees. The crab zone of G. quadratus in CaboBlanco is similar but extends 7800 m inland with averagedensities ranging from 3.3 crabs m-2 in the coastal crabzone (>100 m from coastline) to 0.76 crabs m-2 in the inlandcrab zone (150-350 m from coastline) (Lindquist & Carroll,2004; Fig. 4C). In Caribbean coastal forests of Veracruz,Mexico, Gecarcinus lateralis (sometimes considered synony-mous with G. quadratus) maintains mean densities of 0.5crabs m-2 (Capistran-Barradas, Defeo & Moreno-Casasola,2003). In addition to G. quadratus (and its Caribbeancounterpart G. lateralis; Hartnoll, 1988), two other species ofcrab inhabit Costa Rica’s Pacific coastline: a terrestrialhermit crab, Coenobita compressus (Coenobitidae), foundwithin 100 m of the shoreline, and a second Gecarcinidland crab, Cardisoma crassum, found in frequently floodedclays bordering rivers within a few hundred meters of thecoastline.

All of these terrestrial crabs found in neotropicalmainland coastal forests forage principally on plantmaterial, including leaf litter (Kellman & Delfosse, 1993;Sherman, 2003), seeds (Garcia-Franco, Rico-Gray & Zayas,1991; Lindquist & Carroll, 2004; Capistran-Barradas &Moreno-Casasola, 2006) and seedlings (Delfosse, 1990;Garcia-Franco et al., 1991; Thacker, 1996, 1998; Sherman,2002; Lindquist & Carroll, 2004). In the two mainlandcoastal terrestrial forests studied by the authors (Sherman,2002, 2003; Lindquist & Carroll, 2004), predation by landcrabs affects seed and seedling survival differential to thecoastal gradient and correlates with shifts in the foreststructure and species composition in the crab zone.

(1) Seed predation

In mainland coastal terrestrial forests, land crabs are knownto be significant seed predators providing a mechanism bywhich crabs may limit the establishment of plant species



(Table 2). By collecting seeds and carrying them to theirunderground burrows (;1 m in depth) for consumption,land crabs prevent seeds from establishing through activepredation or removal to depths inhospitable for seedlinggrowth (Lindquist & Carroll, 2004). In one seed transplantexperiment in Cabo Blanco, over 40% of non-protectedseeds were removed by land crabs within five days of theirtransplantation; however, removal of seeds transplanted intothe crab exclosures was only 15% (Lindquist & Carroll,2004). Seed removal in crab exclosures was most likelycaused by a combination of seed predators includingmammals (agoutis, coatis, raccoons, skunks, squirrels, deer,and opposums) and birds that walked, climbed, or flew over

the 0.3 m tall exclosure. The crab zone in Cabo Blanco isdeficient in terrestrial mice and rats, most likely due tocompetitive exclusion by the land crabs (R. Timm &D. McClearn, unpublished observations). Seed removal inthe transplantation experiments did not differ among awind-dispersed species, Terminalia oblonga, and two animal-dispersed species, Anacardium excelsum (Anacardiaceae)and Enterolobium cyclocarpum (Mimosoideae). By contrast,Capistran-Barradas & Moreno-Casasola (2006) documen-ted species preference by foraging G. lateralis among 10species of fruits and seeds that varied in size and nutritionalcontent. Crabs were found to remove species with large fruitsor small seeds at lower rates than other seed types. T. Lee &

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0Coastal InlandInland

Fig. 4. (A) Tree density was higher (t ¼ -7.79, P < 0.0001) in the inland zone (1700 ^ 860 trees ha-1, N ¼ 36) than in the coastalzone (510 ^ 350 trees ha-1, N ¼ 36) in a mainland terrestrial coastal forest in Cabo Blanco, Costa Rica (after Lindquist & Carroll,2004). (B) Tree species richness (total in 0.28 ha sampled) was also higher in the inland zones (S ¼ 59) than coastal zones (S ¼ 18).(C) Densities of the land crab, Gecarcinus quadratus, were on average fourfold higher (t ¼ 6.3, P < 0.0001) in the coastal zone (0-100 mfrom coast, 3.0 ^ 1.4 crabs m-2, N ¼ 22) than in the inland zone (150-350 m from coast, 0.76 ^ 0.78 crabs m-2, N ¼ 24). Incoastal habitats where crab densities are higher, tree densities and species richness were lower. In the inland zone, tree density andspecies richness increased by almost the same magnitude (3.4 times and 3.5 times greater respectively) that crab density decreases(4.0 times less). (D) In experimental transplantations of seeds (N ¼ 36, 46 days) and (E) seedlings (N ¼ 25-47, 31 days), seed (X2¼28.3, P < 0.001) and seedling (X2¼ 7.85, P < 0.01) survivorships were higher in the inland zone where crab density is lower. Alsonote that seed and seedling survivorships were higher where crabs were excluded (dark bars) than where crabs were present(‘‘control’’, open bars).



P.M. Sherman (unpublished observations) also report G.quadratus preferences for certain fleshy fruits such as Simabacedron (Simaroubaceae). Neither of these studies investigatedthe connection of crab predation specificity with treedistributions relative to the coastal gradient.


In both mainland forests on the Pacific coast in Costa Rica(Corcovado, Sherman, 2002; Cabo Blanco, Lindquist &Carroll, 2004), strong experimental evidence shows thatcrab predation of seedlings decreases tree seedling survivor-ship. In Corcovado, after two years of experimental crabexclusion, average seedling densities within five protectiveexclosures increased 144% over baseline values whileaverage control densities decreased for seedlings 3 to 25cm tall. Preference tests conducted in the crab zonerevealed a fivefold ratio of predatory removal rates forseedling species only found in the crabless zone versus thosealso found in the crab zone. These findings suggest thatthose seedling species surviving in the crab zone are thosethat are, for some reason, undesirable to crabs (i.e. similar tothe assumptions of the dominance-predation hypothesis formangrove communities, see above). As a second control tothis study, seedling species collected from the crabless andcrab zones were transplanted into the crab zone andprotected from crab predation. Both groups of seedlingssurvived similarly well over six months with 83% and 70%survival of the crabless zone and crab zone seedlings,respectively. Such findings indicate that crabs are selectivein their seedling consumption and cause differentialsurvivorship of tree species propagules, and as a resultaffect adult tree diversity and distributions in Corcovado’scoastal forest (Sherman, 2002).In two transplantation studies in Cabo Blanco for 120

days in 2001 and 40 days in 2002, seedling mortality washigher in unprotected treatments (74% or 100%, respect-ively) than in exclosures (35% or 52%, respectively;Lindquist & Carroll, 2004). As in the seed removalexperiments at the same site (see previous subsection), landcrabs did not demonstrate predation selectivity between twospecies of seedlings, E. cyclocarpum and Pachira quinata (58%or 49%, respectively). Experimentation with additionalseedling species should be conducted to substantiate thisinitial finding. However, the results suggest that shifts inforest species composition along the coastal gradient aredue to variation in crab predation pressure in space andtime, not only species preferences.Despite the reported differences in seedling selectivity in

Sherman (2002) and Lindquist & Carroll (2004), bothstudies found seedling predation by crabs to vary relative toseedling size and stage of establishment. Sherman (2002)reports that seedlings at the cotyledon stage (0 – 3 cm), andthose taller (26 - 50 cm), were unaffected by crab exclusion.Similarly, seedling predation by crabs did not limit survivalof older seedlings (8 months after germination; Lindquist &Carroll, 2004). From these findings, we propose that crabpredation is higher for younger seedlings because theyprovide a higher nutritive reward. Size refugia, hence, mayprotect seedlings from removal of the recruitment pool by

crabs in mainland coastal terrestrial forests, similar to whathas been found in mangroves (Sousa & Mitchell, 1999).


The magnitude of seed predation changes along a coastalgradient in terrestrial mainland forests (Table 1). In CaboBlanco, land crab densities and their removal rates of seedsand seedlings are lower inland than they are closer to thecoast (Lindquist & Carroll, 2004; Fig. 4C,D,E). In the sameseed and seedling transplantation experiments mentionedabove (Lindquist & Carroll, 2004), crab predation was higherfor seeds and seedlings in the coastal zone (higher G. quadratusdensities, C. compressus present) than in the inland zone (lowerG. quadratus densities, C. compressus absent). This gradient ofpredation pressure likely represents an important mechanismexplaining the documented paucity of seedlings, saplings andadult small-stemmed individuals and reduced tree diversity inthis forest’s most seaward zone. In addition, the three mostdominant trees of the seaward zone are wind-dispersedspecies (Calycophyllum candidissimum, Lonchocarpus felipei,P. quinata). Those species that disperse large numbers of smallseeds, such as wind-dispersed species, in any given fruitingepisode may have more seeds escape predation by crabs thanthose species with lower fecundity (sensu Janzen, 1969).

In contrast to one mangrove crab study (Osborne &Smith, 1990) and one mainland coastal forest study inMexico of G. lateralis (Capistran-Barradas & Moreno-Casasola, 2006) which found land crabs to avoid large lightgaps (> 300 m2 and < 15% vegetation cover, respectively),but similar to several other mangrove studies (Sousa &Mitchell, 1999; Krauss & Allen, 2003; Allen et al., 2003;Clarke, 2004), our mainland findings show no relation be-tween crab foraging activity and canopy cover (Lindquist &Carroll, 2004, P.M. Sherman, personal observations). Landcrabs removed seeds at similar rates in both gap (67-80%canopy cover) and non-gap (86-91% canopy cover) plots inthe dry season when crab activity would be most influencedby microclimatic shifts in evaporation rate (Lindquist &Carroll, 2004). The more homogenous predation pressurereported may be due to the more nocturnal foragingactivity of G. quadratus compared to other species (Table 2),or by less stressful environmental conditions for crabforaging in smaller mainland forest light gaps (Sousa &Mitchell, 1999).

In addition to the coastal gradient and canopy cover,increased crab densities in mainland coastal terrestrialforests have been associated with: (1) increase in treebuttress and root density (P.M. Sherman, personal obser-vations), (2) age of forest (Capistran-Barradas et al., 2003)and (3) increase in leaf litter (Capistran-Barradas et al.,2003). Further studies should assess how this spatialvariation in crab densities affects recruitment and sub-sequent coastal forest structure.


Land crabs have a distinct seasonality to their above-groundactivity (Table 2). Because land crabs receive their oxygen



through both air- (branchial chambers) and water- (gills)breathing systems, their foraging is limited by higherevaporation rates in the dry season of mainland coastalterrestrial forests (McMahon & Burggren, 1988). In CostaRica populations, crabs emerge from their burrows to mateduring the first rains of the wet season, and remain activethroughout the next eight to nine months until thebeginning of the dry season in early January. At this pointthey retreat to their burrow chambers that providea homeostatic moist environment year-round. During thedry season, during which crabs are relatively inactive aboveground (Capistran-Barradas et al., 2003; Sherman, 2003),the majority of tree species in seasonal tropical forestsdisperse their seeds. We have observed, however, nocturnalseed removal by crabs during the dry months (Lindquist &Carroll, 2004). Although seedling germination and estab-lishment typically occurs at the onset of the rains, thoseseedlings that can establish early in the dry season or late inthe wet season when crab activities decline may benefitfrom a temporal refuge from this predation pressure.

Land crab above-ground activity also varies over a 24 hperiod in mainland coastal terrestrial forests (Table 2).In both Cabo Blanco and Corcovado, Gecarcinus quadratusare primarily nocturnal. Their nocturnal foraging activitiesmay reflect sensitivity to the lower humidity and higherdaytime temperatures (Wolcott, 1988), and/or higher ratesof daytime predation. Although avian and mammalianpredators are active during both day (water, shore andriparian birds, birds of prey, grey foxes and coatis) and night(owls, opossums, raccoons, kinkajous, olingos and ocelots),nocturnal hours may provide crabs a greater opportunity toescape predation. By contrast, Gecarcinus lateralis in Mexicois more diurnal, foraging between 07:00 and 11:00h(Capistran-Barradas et al., 2003).

Similarly to island maritime forests, year-to-year period-icity (cf. Wolcott, 1988) in crab densities may providea recruitment window for tree species where seedlingsurvival will be higher, particularly for species excludedfrom the crab zone. The presence of adult trees of speciesthat are preferred by crabs as seeds or seedlings suggeststhat through some combination of spatial or temporalavoidance and predator satiation, plant individuals maysurvive crab predation and recruit successfully. A species-by-species analysis of trees, in regards to their palatability aspropagules and seedlings and their phenology of seed set, isa recommended avenue for further research.


Land crabs can have indirect positive effects on seedlingmicrosite conditions through leaf litter subterraneanaccumulation. Despite the propensity for land crabs toremove fruits, seeds and seedlings, they also forage on theabscised leaves that accumulate on the ground. InCorcovado during the wet season, the removal of leavescan result in broad expanses of forest floor (tens or hundredsof m2) completely or nearly devoid of accumulated litter(Sherman, 2003). Experimental exclosures accumulatedmore leaf litter over the two-year period (5.6 times) than did

control plots, and developed a thick humus and fungalhyphae layers. By collecting, hoarding and breaking downleaf litter in the burrow chambers (collections of up to 11.75g dry mass have been retrieved), much of the litter falling inthe crab zone decomposes below ground rather than at thesurface as it does in the crabless zone. This influence onorganic carbon stores and soil nutrient profiles can bemultiplied by the number of crabs burrowing in the forest.Plant growth follows these nutrient-rich microsites; increaseddensities of fine to very fine roots have been found in andaround burrow chambers relative to same-depth samplesfrom the crab zone that are unassociated with burrows(Sherman, 2006). Furthermore in crab exclosures, crab zoneseedlings survived better in bare soil plots, and crabless zoneseedlings survived better in litter plots. The presenceor absence of leaf-litter may act as an effect-modifier(Hosmer & Lemeshow, 1989) to the crab predation effect byenhancing the survival of seedlings (Sherman, 1997). Bymodifying the physical properties of the litter and soil layers,land crabs also act as ecosystem engineers facilitating plantgrowth (Machicote, Branch & Villarreal, 2004).

V. IMPLICATIONS

(1) Implications across ecosystems

By comparing the findings across three tropical coastalecosystems, we have found that land crabs play similarecological roles and thus have similar impacts on treerecruitment in the different habitats. In all three ecosystems,crabs remove seeds or propagules at rates significant toimpact plant establishment (Table 2). Although crabdamage to seedlings is minor in mangroves, crabs furtherlimit plant establishment through their preferential pre-dation of seedlings in island maritime and mainland coastalterrestrial forests (Table 2).

Crab predation of seeds, propagules and seedlings canvary in space and time, but not necessarily in the samedirection among the three ecosystems (Table 2). Findings inmangroves suggest that there is not always a change in crabpredation pressure along the intertidal gradient. There isalso no shift in crab predation pressure in island maritimeforests; island land crabs have a large, negative impact onseedling establishment throughout their range. In mainlandcoastal terrestrial forests, however, crab predation pressurehas been found to be higher closer to the coastline whereGecarcinus spp. densities are highest and the terrestrialhermit crab, Coenobita compressus, is present. Crab predationof seeds, propagules and seedlings has not been found tovary with canopy cover in mangroves and mainland coastalterrestrial forests (Table 2). Yet some mangrove studies haveobserved the opposite; propagule removal was higher underfull canopy than in large gaps. This discrepancy in thefindings may be an artifact of variable gap size used in thedifferent investigations and seasonality in data collections.Crabs are known to be less active outside their burrowsduring periods of low humidity and high sun intensity inorder to conserve water stores.



Because low water availability limits land crab activityabove ground, island and mainland coastal terrestrialstudies have found that crabs are active primarily in therainy season when humidity is high (Table 2). To minimizefurther water loss, some mainland studies have found landcrabs to be nocturnal (Sherman, 2002; Lindquist & Carroll,2004). In mainland coastal terrestrial forests on theCaribbean coast of Mexico, however, Capistran-Barradaset al. (2003) observed Gecarcinus lateralis to be diurnal.Observations of land crabs in island communities also havefound crabs to be either diel or diurnal with variation intheir daily activity patterns due to variable humidity levels(Table 2). In all three ecosystems, crab activity is highestwhen the majority of seeds and propagules are dispersed,typically at the beginning of the rainy season in seasonalforests. By coinciding with the preferable period for seedlingestablishment, the recruitment limitation effect of crabs isamplified. Although the negative impact of land crabs onplant recruitment is universally significant among coastalecosystems, even the most palatable tree species have beenable to recruit to maintain their populations. Differentialpredation pressure relative to the tidal location or treespecies would allow variable recruitment in space. Lesspalatable species may dominate the areas with morepredation pressure (dominance-predation hypothesis), andmore palatable species may be more abundant where crabdensities are low. However, differential predation pressuredoes not explain the observed presence of palatable speciesin areas with high crab densities. We suggest that annualvariability in crab densities may provide windows forrecruitment of palatable species when crab densities are low(Table 2).In addition to predation of seeds and seedlings, crabs also

impact forest recruitment through the removal of leaf litterin all three ecosystems (Table 2). The removal of leaf littercan be detrimental to seedling establishment by minimisingsoil nutrient replenishment and erosion of topsoil. However,by collecting the litter in their subterranean burrows, andmaintaining their burrows through regular soil movement,crabs may facilitate seedling establishment through anincrease in soil nutrient and carbon levels (Table 2). Inmangroves, crab burrows may be high enough to serve asrefugia from tidal inundation.

(2) Conservation implications

In this review, we have argued that land crabs are a keydriver of seedling recruitment in mangrove, insular andcoastal forests. Although this illustrates their currentimportance, it is certain that they played a much largerrole in the past. At least two human-induced drivers ofglobal change – land transformation and overexploitation –have caused major declines in the distribution andabundance of land crabs by reducing the areal extent andquality of coastal ecosystems. Mangroves have declined inarea by 35% globally, which is more than tropicalrainforests and coral reefs (Valiela, Bowen & York, 2001).Loss of mangroves has caused declines in benthic bio-diversity, including land crabs (Ellison, 2008). Even selective

harvesting of mangrove tree species reduces populations offoliovorous and other sesarmid crabs (Emmerson & Ndenze,2007). Transformation of coastal forests in southern NorthAmerica has obliterated populations of Gecarcinus lateralis andCardisoma guanhumi (Wolcott, 1988). Habitat in many, if notmost insular ecosystems dominated by land crabs (Borradaile,1901), has been drastically reduced through land trans-formation including urbanization, conversion to agriculture,mining and war (e.g., Baine et al., 2006).

Recent and rapid changes in land crab densities onislands are also occurring against a historical background ofharvesting of land crabs by humans (Moul, 1954; Bates &Abbott, 1958; Niering, 1963; Lutz & Austin, 1983; Ashmole &Ashmole, 2000; Pain et al., 2000). Most land crabs are tastyand in many circumstances have formed an importantdietary component for local people (e.g. Foale, 1999),frequently to the point of overexploitation. On the island ofSaba in the lesser Antilles, the mountain land crab Gecarcinusruricola formed a primary component in Amerindian dietsover 3000 years ago, but is now endangered throughmodern day hunting (Hofman & Hoogland, 2003).Legislation has been enacted to protect G. ruricola (Baineet al., 2007). Local peoples have developed specialized trapsto catch gecarcinid crabs in both the Caribbean and thePhilippines (Maitland, 2002). The coconut or robber crab(Birgus latro) is so prized that numbers have been drasticallyreduced across its Indo-Pacific range (Lavery, Moritz &Fielder, 1996). In other situations, land crabs have beenhunted as a nuisance. On Ascension Island, bounties placedon Gecarcinus (Johngarthia) lagostoma in 1879 resulted inthe destruction of 80,000 individuals from croplands(Ashmole & Ashmole, 2000).

Where land crab abundance has been drasticallyreduced, it is almost certain that the contemporary structureand functioning of these forest communities has beenaltered from its original state. In mangrove systems twogenera, Cardisoma and Ucides, which have profound impactson nutrient cycling within the forest, are harvested forhuman food. By processing leaf litter these land crabs helpretain nutrients in the forest ecosystem. Ecological modelshave shown that nutrient retention increases forest pro-ductivity, which in turn provides a positive feedback to crabbiomass (Wolff, Koch & Issac, 2000; Koch & Wolff, 2002).There is evidence that subsistence fisheries may beoverharvesting these crabs in many locations. This couldlead to decreases in forest production which in turn couldresult in further reductions in crab populations, alterationsin sediment geochemistry, followed by shifts in mangrovetree species composition and dominance. The portunid,Scylla serrata, is an important species in the Indo-West-Pacificregion although it does not consume mangrove propagulesor seedlings. It does however prey on other crabs in theforests. Overharvest of Scylla serrata for human consumptionis likely to affect the influence of crabs on mangroveecosystems indirectly (Demopoulos et al., 2008). All threetropical ecosystems highlighted in this review are in declinedue to rapid coastal development for tourism and foreignresidences around the world (Valiela et al., 2001; Rivera-Monroy et al., 2004). Given that land crabs serve as keyplayers in these coastal ecosystems, we recommend that



their ecological role discussed in this review be included inforest conservation and management plans.

VI. CONCLUSIONS

(1) Current dogma suggests that biotic factors may be lessimportant in insular ecosystems than in mainland ecosys-tems (e.g. Elton, 1958; Carlquist, 1965; MacArthur, 1972;Janzen, 1973). This view might also be extended to coastalecosystems in general, like those reviewed here, wheresalinity and flood gradients are assumed to be the primeregulators of plant establishment. However, the ubiquity ofland crabs and their effect on plant recruitment in tropical,coastal forests is not consistent with this view.

(2) Where their role has been quantified, land crabs areconsistently found to be key determinants of seedlingrecruitment at large spatial and temporal scales on islandsand continental landscapes. In fact, the magnitude of theirimpact on seedling recruitment can be severalfold greaterthan for coastal rainforests with a diverse assemblage ofseed and seedling predators (Molofsky & Fisher, 1993;Terborgh & Wright, 1994; Terborgh et al., 2001). Crabsare influential in this manner for at least five reasons. First,land crabs exert strong and consistent biotic influencesacross two plant life-history stages: seed/fruit/propaguleand seedling. Second, the effect of abiotic environmentalgradients (e.g., elevation, rainfall, salinity) is not as direct asthat of crabs because abiotic factors may only decreasegrowth rates, and do not always extirpate certain species’recruitment pools (Fig. 1). Third, where land crab popula-tions are dense, they often exclude, or at least minimize,other seed and seedling predators as well as herbivores.Fourth, land crabs indirectly influence seedling recruitmentdynamics through the removal of the leaf litter layer andsubsequent manipulation of the soil nutrient profiles.Finally, land crabs prey on the earliest stages of plantrecruitment, and thus initially restrict the long-term impactthat environmental conditions can have on survival andgrowth of the seedling.

(3) Studies reviewed here provide evidence that land crabassemblages shape tree species recruitment in a dominantmanner in several tropical locales. Crabs directly limit thedistribution and density of trees along coastal gradients andfacilitate plant establishment through several direct andindirect mechanisms. Given that all three coastal ecosys-tems vary in the strength of their environmental gradients,we suggest that crabs do have primacy in many forests overother, better studied abiotic effects, such as desiccation,flooding and salinity (Fig. 1). Tree recruitment models forthese systems should incorporate both abiotic and bioticfactors affecting seed and seedling survivorship, butdetermine which factor(s) are the primary filters, and whichcause secondary mortality. Using our example of how onebiotic factor can transcend abiotic variation across differenttropical coastal ecosystems, we hope to encourage others toisolate any common factor(s) driving plant recruitment thatin turn will influence forest structure and composition inother ecosystems not discussed here.

VII. ACKNOWLEDGEMENTS

We would like to thank those contributors to a specialsession on this topic at the American Society of Limnologyand Oceanography (ASLO) Summer 2006 meeting inVictoria, B.C., Canada, including Wayne P. Sousa (UC-Berkeley, USA), Todd E. Minchinton (University ofWollongong, Australia), Jos�e L. Guti�errez (UniversidadNacional de Mar del Plata, Argentina), Kauoa M. Fraiola(University of Georgia, USA) and Alan P. Covich(University of Georgia, USA). James B. Grace, WayneP. Sousa and two anonymous referees provided excellentreviews of earlier versions of this manuscript.

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Biol. Rev. (2009), , pp. 203–223. doi:10.1111/j.1469 ...poboyca/documentos/documento… · predation or herbivory of seeds and seedlings had a signifi-cant impact on tree recruitment