J. Zool., Lond. (2000) 250, 141±160 # 2000 The Zoological Society of London Printed in the United Kingdom

A reconstruction of the invasion of land by Jamaican crabs (Grapsidae: Sesarminae)

Rudolf Diesel 1,2*, Christoph D. Schubart 2,3 and Martina Schuh 2 1 Max-Planck-Institut fuÈr Verhaltensphysiologie, Postfach 1564, D-82305 Seewiesen, Germany 2 Lehrstuhl fuÈr Verhaltensforschung, UniversitaÈt Bielefeld, Postfach 100131, D-33501 Bielefeld, Germany 3 Department of Biology and Laboratory for Crustacean Research, University of Southwestern Louisiana, Lafayette, LA 70504-2451, U.S.A. (Accepted 3 April 1999)

Abstract Several decapod groups independently colonized freshwater and terrestrial habitats and became independent from the sea. These invasions were accompanied by analogous reproductive and developmental traits such as large eggs and an abbreviated, lecithotrophic development. Here, we present the ®rst empirical study on the evolution of reproductive and developmental traits that accompany the invasion of land by crabs. As crucial steps in the colonization, we identify the transitions of the larval nursery, ®rst, from the marine plankton into landlocked-brackish nurseries and, second, into fresh water. During these invasions, the early life-cycle stages were facing new ecological conditions and selective agents. We test hypotheses on the evolution of egg size and the mode of development in relation to the larval ecology of recent species and draw conclusions on their evolutionary past. As a model we focus on the genus Sesarma, that colonized Jamaica relatively recently and comprises species with a larval development in marine, brackish and freshwater habitats. In addition, we compare representatives of the crab genera Armases, Sesarma and Uca that invaded brackish-nursery habitats independently. The analysis reveals that in each genus the transition from marine to brackish nurseries resulted in fewer and larger eggs, an abbreviated development and higher endotrophic potential of larvae, and a wider tolerance to physicochemical stress (salinity). Size at metamorphosis, however, did not change in brackish species, suggesting that it is constrained. Within the Sesarma-lineage, egg size increases considerably from marine to freshwater species. The duration of embryonic development, the size and endotrophic potential of larvae are positively correlated, but the duration of the larval phase is negatively correlated with egg size. Hypotheses suggesting that large eggs evolved as a response to limited food or intense predation are inadequate to explain the initial egg-size increase in brackish species. We suggest that the speci®c abiotic environment of the brackish nurseries ultimately selected for increased egg size. These particular larval nurseries of brackish species of Armases, Sesarma and Uca are nutrient rich but ephemeral habitats with unfavourable physicochemical conditions, which strongly favour a swift larval phase and possibly large body size and higher salinity-stress resistance of larvae. The reason for the further and substantial increase in egg size in freshwater species remains unknown. The `food-limitation' hypothesis derived from laboratory experiments, however, is inadequate to explain this increase. Our results support general life-history hypotheses (`safe harbour' hypothesis) that predict the evolution of large eggs if post- embryonic stages face high risk of mortality, but not the predicted positive relationship between egg size and instantaneous egg stage mortality. On the contrary, we ®nd a negative relationship, suggesting that larger eggs are a `safer harbour' than smaller eggs. We outline a scenario for the invasion of land by crabs and propose a two-step model: as a ®rst step, an instant shift of the larval development from offshore into landlocked-brackish nurseries, and, as a second step, from there into freshwater nurseries.

Key words: Brachyura, terrestrial invasion, ecology, life history, egg size

INTRODUCTION one on land is an important issue in evolutionary biology (Labandeira & Beall, 1990; Little, 1990; Selden The transition of animals from a marine existence to & Edwards, 1990; Schubart & Diesel, 1999). Questions commonly asked are: when did colonization take place, which route was taken, and what adaptations were *All correspondence to: R. Diesel. E-mail: [email protected] involved? Arthropods had already colonized land in the 142 R. Diesel, C. D. Schubart and M. Schuh

Late Palaeozoic and with the hexapods and arachnids Guldberg & Pearse, 1995), but these may be of little became the most successful and diverse animal group on relevance for life histories of land-living organisms earth. Interestingly, with more than 50 000 described (Strathmann, 1990). species, the Crustacea is one of the largest arthropod With the transition onto land, the larval stage taxa, but the only one with predominantly marine apparently became the most risky life stage. The `safe species. Some decapods ± particularly brachyuran crabs harbour' hypothesis (Shine, 1978) proposes that organ- ± are recent colonizers of land, and are still undergoing isms should spend more time in safe than in risky life important modi®cations for life on land (see Labandeira stages (Williams, 1966). For example, if mortality rates & Beall, 1990). With few exceptions, decapods reach the are lower in eggs than in larvae, then large eggs, highest diversity on land in the tropics and subtropics, extended embryonic and abbreviated juvenile periods with new species still being described. A literature are expected. Sargent, Taylor & Gross (1987) noted that survey revealed that at least 20 of 112 decapod families large eggs become large larvae (or juveniles) with lower have representatives that are true freshwater or mortality and faster growth rates and thus, selection on terrestrial species, i.e. their entire life cycle takes place larvae may often favour large size. Hence, the same life on land. history pattern may evolve even if eggs have higher Two major routes in the colonization of terrestrial mortality rates than larvae, if the enhanced survival of habitats have been suggested (see Little, 1990): (1) the large larvae more than compensates for losses during `direct' route via the marine intertidal and littoral- the egg stage. marginal marine habitats; (2) the `indirect' route via Here we address two questions: (1) what route was fresh water and subsequently into terrestrial habitats. taken during the colonization of land; (2) how and why Little (1990) implied that both routes might have did the relevant life-history traits in freshwater and included transient stages in mangrove swamps and terrestrial crabs evolve? Our hypothesis is that in species brackish-water habitats such as estuaries and coastal with aquatic larvae the colonization of freshwater lagoons. habitats has occurred via an ancestor with larval Much research has focused on the adaptations of development in coastal brackish-water habitats (for crabs that live in terrestrial habitats (summarized in de®nition see below). This transitory ancestor must Bliss, 1968; Powers & Bliss, 1983; Burggren & have had acquired reproductive and developmental McMahon, 1988; Mantel, 1992). Most of these studies adaptations which provided the preconditions for the investigated the physiological and behavioural adapta- subsequent colonization of freshwater or terrestrial tions of adults of crab genera (such as Gecarcinus, habitats (see also Schuh & Diesel, 1995b,c). Cardisoma,andUca) that do not present truly fresh- The larval stage is crucial because it will allow the water or terrestrial lines and depend on the sea for transition. Our approach is to study the ecology and larval development. Truly freshwater and terrestrial reproductive and developmental traits of closely related decapods share the following important features: (1) a species with larval development in the sea, in coastal life cycle entirely emancipated from the sea; (2) the brackish-waters, and in fresh water. As model, we use production of relatively few but large yolk-rich eggs; (3) three lineages and genera of crabs occurring in the an abbreviated and lecithotrophic larval development or neotropics: the grapsids Sesarma and Armases (sub- a direct development (see Rabalais & Gore, 1985). family Sesarminae), and the ocypodid Uca. Each genus Hence, one important key to the invasion of land by contains one `transitory' species (S. curacaoense, crabs is the evolution of reproductive and develop- A. miersii, and U. subcylindrica) that independently mental traits that accompany independence from the evolved a development in coastal brackish-water marine plankton. habitats, for example supratidal rock pools (Schuh & It has been suggested that large egg size and the high Diesel, 1995a). These are the only transitory brachyuran endotrophic potential of larvae (the ability to thrive on species presently known in the world, and their larval yolk reserves) of freshwater decapods is an adaptation habitats are described only from the north coast of to food limitation in fresh water (Soh, 1969; Jamaica (Schuh & Diesel, 1995a,b) and from the McConaugha, 1985; Rabalais & Cameron, 1985; Raba- western Gulf of Mexico between Copano Bay (Texas) lais, 1991; Anger, 1995a,b). However, the production of and Tampico (Mexico) (Thurman, 1984; Rabalais & large yolk-rich eggs has also been attributed to high Cameron, 1985). All species studied here require water predation, risk of desiccation, lack of predation, recruit- for larval development. ment ability, reduced dispersal from parental habitat, The Caribbean Sesarma-group is the only brachyuran temporariness of nursery habitats and physicochemical group known to comprise species with `ancestral' factors (see Rabalais & Gore, 1985; Hoegh-Guldberg & marine-planktonic, `transitory' coastal-brackish-water, Pearse, 1995; Schuh & Diesel, 1995a; Strathmann, and freshwater larval development. On Jamaica, this 1995). In addition, a large body of theoretical and group colonized land during the Pliocene (Schubart, empirical studies has been concerned with life-history Diesel & Hedges, 1998) and underwent an extensive strategies of marine invertebrates considering variations adaptive radiation in freshwater and terrestrial habitats in egg size, fecundity, developmental mode, and (Hartnoll, 1964a,b, 1971; Abele & Means, 1977; larval and post-larval stages (e.g. Thorson, 1950; Schubart et al., 1997; Reimer, Schubart & Diesel, 1998; Vance, 1973a,b; Strathmann, 1978, 1985, 1995; Hoegh- Schubart, Reimer & Diesel, 1998). Invasion of land by crabs 143

Table 1. Adult and larval habitat and distribution of American species of the subfamily Sesarminae, including a complete list of the presently known Jamaican endemites

Species Adult habitat Larval habitat Distributiona Sourceb

Armases cinereum (Bosc) Salt marshes Marine, estuary North-east America to Mexico 2, 4, 7, 14 A. ricordi (H. Milne Edwards) Upper mangal, dry habitats Marine Florida to Surinam (Jamaica) 1,2,5,13,16 A. roberti (H. Milne Edwards) Riverbanks, up to 10 km Marine West Indies (Jamaica) 2, 16 upstream A. miersii (Rathbun) Coastal, near brackish Brackish water, supratidal Florida, Jamaica 2, 17, 21 water pools (West Indies) ? Sesarma reticulatum (Say) Salt marshes and mangal Marine, estuary Massachusetts to eastern 2, 4, 14 Florida S. sp (nr. reticulatum) Edges of estuary, salt Marine (?) Florida to Mexico 20 marshes S. rectum Randall Edges of estuary and Marine (?) Trinidad, Guyana to Brazil 2, 10 mangal S. curacaoense DeMann Landward mangal Brackish water, mangal Florida to Brazil (Jamaica) 1, 2, 13, 18 S. bidentatum Benedict River banks, mountain Freshwater pools Eastern Jamaica 2, 11, 23 streams S. ayatum Schubart et al. River banks, mountain Freshwater pools Eastern Jamaica 23 streams S. windsor TuÈrkay & Diesel River banks Fresh water, burrows Western Jamaica 22, 23 S. fossarum Schubart, Diesel River banks, cave streams Fresh water, burrows Western Jamaica 15, 19 &TuÈrkay S. dolphinum Reimer, Schubart River banks, mountain Fresh water, burrows (?) Western Jamaica 19, 22 & Diesel streams S. verleyi Rathbun Cave systems Freshwater pools Western Jamaica 2, 11, 12, 23 S. cookei Hartnoll Rain forest ¯oor Fresh water (?) Eastern Jamaica 2, 3, 21, 23 S. jarvisi Rathbun Rain forest ¯oor Fresh water, snail shells Western Jamaica 2, 3, 9 Metopaulias depressus Rathbun Bromeliad leaf axils Fresh water, bromeliads Western Jamaica 8, 11 a Distribution after Abele, 1992, Chace & Hobbs, 1969, & Powers, 1977. b Data from: (1) Abele, 1973; (2) Abele, 1992; (3) Abele & Means, 1977; (4) Seiple, 1979; (5) Boschi, 1981; (7) Costlow, Bookhout & Monroe, 1960; (8) Diesel, 1989; (9) Diesel & Horst, 1995; (10) von Hagen (1975); (11) Hartnoll, 1964a; (12) Hartnoll, 1964b; (13) Hartnoll, 1965; (14) Sandifer, 1973; (15) Schubart, Reimer, Diesel & ToÁrkay, 1997; (16) Diesel & Schuh, 1998; (17) Schuh & Diesel, 1995a,c; (18) Schuh & Diesel, 1995b; (19) TuÈrkay & Diesel, 1994; (20) Zimmermann & Felder, 1991; (21) Hartnoll, 1971; (22) Reimer et al., 1998; (23) R. Diesel, pers. obs.; Schubart, Reimer & Diesel, 1998.

Today, Jamaica contains the highest species density see Williamson, 1982; Gore, 1985). We regard this of true land crabs with nine endemic species. Within this developmental pattern as ancestral. Taxa with fewer group an extraordinary degree of parental care and a larval stages than closely related ones have a derived, social organization evolved in the terrestrial bromeliad abbreviated development (cf. Gore, 1985; Rabalais & crab, Metopaulias depressus (see Diesel, 1989, 1992a,b, Gore, 1985); direct development is a particular type of 1997) and snail shell crab Sesarma jarvisi (see Diesel & extremely abbreviated development. Horst, 1995). We present here a new approach to the invasion of land by crabs and explain the evolution of egg size in Phylogenetic relationships relation to ecological factors during this transition. The present taxonomy of the Sesarminae requires revision. Our analysis is based on a phylogeny of the American Sesarminae using molecular (Schubart, Diesel GENERAL BIOLOGY OF THE SPECIES AND & Hedges, 1998) and morphological characters (Niem, DEFINITIONS 1996; J. Reimer, pers. comm.). A simpli®ed phylogenetic tree of the species concerned in this study is shown in Life cycle of brachyuran crabs Fig. 1a. Accordingly, Armases (former Sesarma sub- genus Holometopus, see Abele, 1992) and Sesarma In most brachyuran crabs the eggs are small and (former Sesarma subgenus Sesarma) are closely related larvae develop in the offshore plankton through nu- and sister taxa. Both lineages independently colonized merous larval (zoea) stages (Gruner, 1993). Eggs are brackish nurseries on Jamaica. Sesarma curacaoense carried until the larvae hatch and larval development is the only non-endemic Sesarma on Jamaica. The ends with the metamorphic moult into the megalopa, endemic Sesarma species and the monotypic endemic which usually adopts a benthic life style and subse- bromeliad crab, Metopaulias depressus are monophyletic quently moults into the ®rst juvenile stage (for review (Schubart, Diesel & Hedges, 1998). 144 R. Diesel, C. D. Schubart and M. Schuh

De®nition of ecotypes and ecology Williams, 1989). We compare environmental conditions in the nursery habitats and developmental traits For our purposes, we distinguish between species between present species and draw conclusions on their according to the habitat in which larval development evolutionary past, assuming that the overall ecological takes place (`larval ecotypes') (see Table 1): conditions for the larvae of the ancestral species were 1. Marine species have the typical ancestral offshore- basically similar to those in the respective habitats larval development but the adults live on land. today. This procedure is justi®ed because there is no Examples are A. cinereum, A. ricordi, A. roberti, indication that overall environmental conditions have S. reticulatum, S. sp. (nr. reticulatum), S. rectum (as changed much in recent geological times, and because well as the so-called `land crabs' Cardisoma and we compare abiotic and biotic conditions in nursery Gecarcinus). habitats relative to each other, and these relations ± e.g. 2. Brackish species are those with a development in the salinity gradient from the sea into fresh water ± did brackish-water nurseries. These nurseries are landlocked not change. pools or ponds in supratidal areas and in relative isolation from the sea (for A. miersii, see Schuh & Diesel, 1995a; for Uca subcylindrica, see Thurman, METHODS AND DATA ANALYSIS 1984) or mangrove swamps (for S. curacaoense, see Schuh, 1995; Schuh & Diesel, 1995b). These nurseries We used a comparative approach, focusing on indepen- are predominantly situated on supratidal limestone dent cases (cf. Harvey & Pagel, 1992). Chie¯y, we platforms or on limestone rubble on the Jamaican north compare traits that evolved among closely related coast and in semiarid habitats along the western Gulf of species within the grapsid subfamily Sesarminae Mexico (southern Texas and north-eastern Mexico). (Fig. 1a), using a nested design or the calculated means Brackish-waters frequently include estuaries, coastal for ecotypes. That is, species and groups that differ lagoons, and mangrove swamps, where conditions are greatly in their ecology were treated as independent (see predominantly in¯uenced by exchange between sea Fig. 1a). The ecotypes used are marine, brackish and water and fresh water. Here, we explicitly distinguish freshwater, and among fresh water we distinguished between these and landlocked-brackish habitats, riverine, cave and terrestrial. because ecological conditions differ considerably (cf. In addition, we compare traits across the lineages Ketchum, 1983). Because of the very low tidal ampli- Armases, Sesarma and Uca which independently tude on Jamaica (mean 25 cm, Asprey & Robbins, 1953) colonized brackish nurseries (Fig. 1b), by comparing and in the western Gulf of Mexico (approx. 40 cm), the each single brackish species with their marine relatives landlocked-brackish nurseries have very limited (see Fig. 1b). Our comparative approach is limited to exchange with sea water. Jamaican mangrove swamps `only' 3 independent cases. Although there are nu- are shallow and have a limited tidal exchange with merous other true freshwater or terrestrial decapods marine waters. In landlocked-brackish nurseries, the that show life-history traits similar to that of the groups input of salts comes from sea spray, the saline ground analysed in the present study, they either lack marine water table or infrequent tidal inundation. Freshwater and brackish relatives or no reliable information on input depends mostly on precipitation. Hence, these life-history correlates is available. brackish-water nurseries are typically ephemeral and The data for the species of the American mainland heterogeneous habitats with unpredictable and ¯uctu- were mostly obtained from the literature. Where ranges ating abiotic conditions (rock pools and ponds: for body size and clutch size were given in the literature, McGregor, 1965; Rabalais & Cameron, 1985; Schuh & the mean value was used in the analysis. The egg volume Diesel, 1995a; mangrove swamps: Goodbody, 1961; was calculated for newly spawned eggs (formula: Walsh, 1967; Selvam, Azariah & Azariah, 1992; Schuh vol. = egg length * egg width2 * Pi/6) or obtained from & Diesel, 1995b). the literature. Relative clutch mass (%) was calculated 3. Freshwater species have a larval development in fresh as fresh weight of egg-mass/body-mass * 100. The water. Among these we distinguish between: (i) riverine overall mortality during the egg stage should be mea- species with nurseries in and near lotic systems sured as the number of eggs spawned compared to the (S. bidentatum, S. fossarum, S. dolphinum, S. windsor, number of larvae hatched. Because few such data were S. ayatum); (ii) one cave species (S. verleyi), a true available, we compared the numbers of fully developed troglodyte with larval development in small aggrega- eggs (ready to hatch) with the expected number of eggs tions of fresh water within caves; (iii) terrestrial species spawned for a female's body size. Non-developing eggs that rely on small aggregations of fresh water in are usually removed from the clutch by the female (for terrestrial habitats (S. jarvisi, S. cookei, M. depressus). egg mortality, see Kuris, 1991). Ovigerous females for The transitional stage in brackish waters occurred in the analysis were caught in the ®eld during different the Jamaican Sesarma about four million years ago (cf. breeding seasons. Schubart, Diesel & Hedges, 1998) and long after the last Larval response to abiotic and biotic factors was emergence of Jamaica above sea level (20±25 million studied in the laboratory or taken from the literature. years ago, see Sykes, McCann & Kafka, 1982; Per®t & For details on the methods see literature cited below. Invasion of land by crabs 145

(a) Armases miersii B

Armases ricordi M Armases cinereum M Armases roberti M

Sesarma rectum M Sesarma reticulatum M

Sesarma sp. (nr.reticulatum) M

Sesarma curacaoense B

Sesarma fossarum FW R Sesarma dolphinum FW R Sesarma ayatum FW R

Sesarma jarvisi FW T Sesarma cookei FW T

Sesarma verleyi FW C Metopaulas depressus FW T

(b) Armases marine

Armases miersii

Sesarma marine

Sesarma curacaoense

Uca marine

Uca subcylindrica Fig. 1. Tentative phylogenetic tree of the American Sesarminae used in (a) the analysis and (b) the grouping of taxa for the analysis of independent colonization of brackish nurseries in the American Armases, Sesarma and Uca lineages. M, marine, B, brackish; FW, freshwater; R, riverine; T, terrestrial; C, cave species. Data on marine and riverine species were pooled for the analysis. In (a) this is indicated by vertical bars and in (b) by bold lines which represent several marine species of the genus (a, after Schubart, Diesel & Hedges, 1998; J. Reimer, pers. comm.).

Critical oxygen partial pressure was determined for each Data were log transformed to satisfy assumptions larval and the megalopa stage in a respiration chamber (Sokal & Rohlf, 1995). For analysis of egg size and (see Diesel & Schuh, 1993). For tolerance to pH, larvae clutch size we used a nested ANCOVA with log mean were raised in water of different pH ranging from pH 2 female size as covariate and breeding habitat as con- to 8 for S. ayatum and M. depressus and from pH 4 to trast. To investigate the potential trade-off between 10 for the marine and brackish species and the mortality clutch size and egg size, the residuals from the regression noted (see Diesel & Schuh, 1993; Schuh, 1995). Tests for of clutch size and female size were regressed against the salinity tolerance were conducted for a wide range of residuals from the regression of egg size and female size. values ranging from 0 to 65 PSU, with replicates of This removes the in¯uence of female body size from the individually reared larvae at a constant salinity. Survival relationship. Contrasts were evaluated by the LSD into successive larval stages was recorded up to post-hoc tests (Sokal & Rohlf, 1995: 243). All statistics metamorphosis (see Schuh & Diesel, 1995b,c; Diesel & were 2-tailed and performed using the CSS-Statistica Schuh, 1998). package. 146 R. Diesel, C. D. Schubart and M. Schuh

riverine and the cave species which breed near running Cave Armases water and show no parental care produced larger eggs Sesarma Riverine than terrestrial species with intense parental care (see 1000 ) Terrestrial Table 1). 3

m Clutch size was positively correlated with female size µ within species (Table 3), but was not signi®cantly related to female size between species (F(1, 14) = 1.70, P = 0.21). Largest clutch size decreased from 25500 in 100 marine, to 4330 in brackish, and to 460 in freshwater Egg volume ( species (Fig. 3). The terrestrial species, M. depressus and S. jarvisi, produced the smallest clutches with up to 117 and 23 eggs, respectively (see Table 2). For the same Marine Brackish Fresh water body size, mean clutch sizes signi®cantly decreased as Larval habitat following: marine > brackish > riverine > terrestrial Fig. 2. Egg volume of American Sesarminae grouped accord- (F(4, 223) = 2117.5, P < 0.0001, LSD test for all habitat ing to the location of the nursery habitat (see Table 2). combinations P < 0.0001). The residuals of log clutch size and log egg size on log female size were signi®cantly negatively related RESULTS (P < 0.001, Fig. 4). This result is consistent with the expected trade-off between clutch size and egg size. Comparison within the Sesarminae Hence, size speci®c fecundity and egg size re¯ect distinct reproductive strategies in relation to the nursery habitat Clutch size, egg size and reproductive effort (Figs 2 & 3). Between species, the relative clutch mass was not 3 In the Sesarminae, egg size varied from 17±48 mm in related to body mass (F(1, 9) = 0.77, P = 0.40), but with marine to 68±98 mm3 in brackish species and 527± the nursery habitat: It decreased from an average of 2878 mm3 in freshwater species (Fig. 2, Table 2). Egg 11% in marine to only 1.5% in terrestrial species size was not related to female body size among taxa (Fig. 5), and differed signi®cantly between all habitat (F(1, 7) = 0.98, P = 0.36) but there was a highly signi®cant groups, except between brackish and riverine (see relationship between egg size and the larval habitat Table 4). (F(2, 5) = 119.1, P < 0.0001). Post-hoc comparisons re- Total annual reproductive effort reported for the vealed signi®cant differences in egg size between marine, marine species is four to six clutches for A. cinereum and brackish and freshwater species (LSD test, for all two to three clutches for S. reticulatum (Seiple, 1979). P < 0.02). The considerable variation in egg size within The marine A. ricordi and A. roberti and the brackish the freshwater species possibly re¯ects different selective A. miersii and S. curacaoense produced at least two forces exerted by their particular breeding habitat and successive clutches within 6-month observation periods post-hatching maternal behaviours. For example, the (Schuh & Diesel, 1995a; Diesel & Schuh, 1998). The

10000

1000

100 Clutch size

& MarineMarine & BrackishBrackish 10 FreshFresh water water * RiverineRiverine ^ CaveCave * TerrestrialTerrestrial

51015 20 25 30 Carapace width (mm) Fig. 3. Fecundity vs female body size (carapace width) of Jamaican Sesarminae. Species included are marine: Armases roberti, A. ricordi; brackish: A. miersii, Sesarma curacaoense; riverine: S. fossarum, S. dolphinum, S. ayatum; terrestrial: S. cookei, S. jarvisi, Metopaulias depressus; cave: S. verleyi (see Table 2). Invasion of land by crabs 147 b ) n ( 1; (6) Schuh & sd x ) n ( sd x ) (%) 3 m m species Uca ) n ( sd x (mm) ( ; (10) Rabalais & Cameron, 1983, Rabalais, 1991; (11) Abele, 1992. a (mg) Egg no. Mean egg size Egg volume Relative egg mass Source a ) Range n ( sd x ) n ( sd x ; (8) Diesel & Horst, 1995; (9) Diesel, 1992 b 8.9±21.17.5±17.4 11.8 ‹ 2.2 (108) 920 ‹ 483 (63) 3560±14600 112±1510 594 ‹ 253 (53) 0.58 0.32 98 ‹ 11 (8) 8.5 ‹ 1.9 (16) 7 17.2 13.3 ‹ 5.4 (11) 1, 10 Range 12.0±19.711.4±26.9 15.818.0±30.0 ‹ 2.1 (58) 18.513.2±23.6 ‹ 3.3 (95) 1829 ‹ 662 (51) 3526 ‹ 1761 (74) 3408±10951 2737±1526313.1± 24.510.0±24.6 7046 ‹ 17.4 2261 ‹ (19) 7607 2.7 ‹ (75) 3511 (28) 0.35 2397 0.42 ‹ 1215 (58) 17.8 908±4334 21 ‹ 2 (7) 37 ‹ 7 (5) 2004 ‹ 1214 9.6 11.8 (14) ‹ ‹ 2.4 1.5 (15) (23) 25500 2890±11800 0.51 2 2 68 ‹ 7 (4) 25±1412 8.5 ‹ 2.8 (7) 6 0.45 580 (41) 0.45 1.06 47.7 47.7 8.7 ‹ 4.9 520 (7) 1 3, 4, 10 10 13.8±24.216.0±19.018.5±28.4 18.8 ‹ 2.4 (79) 17.4 23.1 (3) 2.5 3099 (19) ‹ 1045 (50) 6272 ‹ 2915 (12) 106±457 2740 (3) 155±302 232 ‹ 72 (31) 165±267 228 ‹ 46 1.38 (10) 1.33 1298 206 ‹ 0.1 (3) (9) 9.6 ‹ 1.8 (15) 1237 4 (2) 1.33 7.0 ‹ 2.5 (8) 4 1260 (3) 9.8 (3) 4 21.0±27.1 25.2 ‹ 1.1 (14) 7381 ‹ 1005 (10) 86±208 145 ‹ 53 (4) 1.79 2878 ‹ 567 (3) 6.0 ‹ 1.3 (4) 4 19.0±20.510.0± 14.413.7±23.2 19.8 11.8 (2) ‹ 0.9 (43) 17.5 ‹ 1.6 (62) 1109 ‹ 237 (20) 2233 ‹ 599 (43) 4326 (2) 4±23 14±117 71 13 55 ‹ ‹ 5.3 12 (22) (26) 1.11 1.20 527 (2) 887 (3) 0.7 ‹ 0.2 2.6 ‹ (20) 1.0 (13) 4, 8 4, 9 1023 (1) 1.6 (1) 4 ) 11.1±26.9 2728±18087 10000 0.35 22.4 5 ; (7) Schuh & Diesel, 1995 c reticulatum . Summary of female body size, egg number, egg size and relative egg mass for the American Sesarminae and spp. 8.0± 35.0 1700±50000 0.24±0.28 7.0±9.0 10 S. fossarum S. dolphinum S. ayatum S. verleyi S. cookei S. jarvisi Metopaulias depressus . sp. (nr Data from: (1) Seiple & Salmon, 1987; (2) Diesel & Schuh, 1998; (3) Fransozo & Hebling, 1986; (4) Diesel & Schuh, pers. obs.; (5) Zimmermann & Felder, 199 Data including all adult females. A. ricordi U. subcylindrica Marine Armases cinereum A. roberti Sesarma rectum S. reticulatum S Uca Brackish A. miersii S. curacaoense Fresh water Riverine Cave Terrestrial Table 2 a b Diesel, 1995 Species Female carapace width (mm) Fresh weight 148 R. Diesel, C. D. Schubart and M. Schuh

Table 3. Summary of regression statistics for analysis of the relationship between body size (carapace width = CW (mm)) and clutch size (E) of Jamaican Sesarminae

Equation of regression line Species log E = a log CW + br2 nP

Marine Armases ricordi log E = 2.263 log CW + 1.082 0.83 17 < 0.001 A. roberti log E = 2.742 log CW + 0.440 0.94 22 < 0.001 Brackish A. miersii log E = 2.774 log CW70.176 0.92 14 < 0.001 Sesarma curacaoense log E = 2.773 log CW70.262 0.88 49 < 0.001 Freshwater Riverine S. fossarum log E = 2.399 log CW70.708 0.72 57 < 0.001 S. ayatum log E = 1.344 log CW +0.571 0.41 8 = 0.088 Cave S. verleyi log E = 6.020 log CW76.310 0.88 4 = 0.055 Terrestrial S. jarvisi log E = 3.399 log CW72.533 0.30 22 = 0.008 Metopaulias depressus log E = 3.986 log CW73.215 0.78 37 < 0.001

20 1.5 18 Min–max 25–75% 1.0 16 Mean value 14 0.5 12 0.0 10 8 –0.5 6 Riverine Relative clutch size 4 –1.0 Cave Terrestrial Relative clutch mass (%) 2 –1.5 0 0.5 –1.5 –1.0 –0.5 0.0 20 1.0 Marine Brackish Fresh water Relative egg size Larval habitat Fig. 4. Relationship between residual egg size and residual Fig. 5. Relative clutch mass produced by Jamaican crabs clutch size on body size in Sesarminae. Mean values were used grouped according to the nursery habitat. Given is the group in the analysis for marine Sesarma, marine Armases, and median of average values for species calculated by using fresh 2 riverine Sesarma species (r = 0.88, F(1, 7) = 49.4, P < 0.001; weight of clutch mass and female body mass (see Table 2). y =72.642e-8 71.497x). freshwater species produced only one clutch within the studied under approximately similar ambient tempera- same periods. Field studies revealed that M. depressus tures (P < 0.001, see Fig. 6a). Embryonic development breeds only once per year, and has maximal lifetime in the freshwater species took up to four times longer reproductive output of up to three broods (R. Diesel, than in the marine species (Table 5). pers. obs.). If only three broods per year are considered Total egg-stage mortality within the Jamaican Sesar- for marine and brackish species, then their annual minae was not signi®cantly different in marine, brackish, reproductive effort amounts to at least 32% and 26% riverine and terrestrial species (F(4, 51) = 0.43, P = 0.78, total clutch mass of body mass, respectively. This is a see Table 6). Average total mortality also was not related magnitude higher than in M. depressus, and still higher to egg duration (F(1, 4) = 0.19, P = 0.69) or egg volume than its lifetime reproductive effort of about 8% total (F(1, 4) = 0.02, P = 0.88). Egg-stage mortality rates (calcu- clutch mass of body mass. lated from the egg-stage duration and total mortality), were higher in marine species with small eggs ( 0.5% eggs/day) than in terrestrial species with large eggs Embryonic development and mortality ( 0.23% eggs/day). That is, we ®nd a negative relation- ship between egg size and egg-stage mortality rate (log 2 The duration of the egg stage (embryonic development) egg volume vs log mortality/day, r = 0.76, F(1, 3) = 9.38, signi®cantly increased with egg size in Sesarminae crabs P = 0.055) among species that breed in different habitats. Invasion of land by crabs 149

Table 4. Differences in reproductive effort between Jamaican congeners which all have four zoeal stages (see Table 5). Sesarminae in different habitats. Results are of multiple Similarly, the brackish S. curacaoense as well as all comparisons (LSD) following nested ANCOVA endemic freshwater species, have an abbreviated devel- (F(4, 112) = 44.67, P < 0.00001). The endemic freshwater species are subdivided in riverine, cave and terrestrial according to the opment with two zoeal stages, compared to three zoeal location of their nurseries stages in all marine Sesarma species.

Habitat Developmental duration Brackish Riverine Cave Terrestrial

Marine < 0.0001 < 0.0001 < 0.0001 < 0.0001 The duration of the larval phase among the American Brackish = 0.56 < 0.0294 < 0.0001 Sesarminae ranged from 17.5 days in marine A. ricordi Riverine < 0.0140 < 0.0001 to 3 days in the terrestrial S. jarvisi and was signi®cantly Cave < 0.0001 negative related with egg size at spawning (P = 0.025; see Fig. 6b). But duration from spawning to metamor- 1.9 phosis increased with egg size, as a result of extremely prolonged embryonic development in the species with S. riv (a)a large eggs (Table 5). 1.7 Larval size and size at metamorphosis

1.5 The size of the ®rst larval stage was positively correlated with the egg size at spawning among the Sesarminae (P < 0.0001; Fig. 7). A comparison between the marine 1.3 A. mar and brackish species showed that the carapace length of S. mar the ®rst larval stage of brackish species was signi®cantly Log duration of egg stage (days) larger than that of marine species, but the megalopa size 1.1 was not different (F(1, 5) = 5.64, P = 0.03, one-tailed, 1.2 1.5 1.8 2.1 2.4 2.7 3.0 3.3 3.6 F = 1.08, P = 0.35, respectively). Correspondingly, µ 3 (1, 5) Log egg volume ( m ) the size of the megalopa was not related to the egg volume (regression analysis, P = 0.90, n = 7), and to the size of the ®rst larval stage (P = 0.62, n = 7). Hence, 1.2 A. mar (b)b metamorphosis in the marine and brackish species occurs at similar size. An analysis of relative growth to metamorphosis 1.0 S. mar revealed different traits in relation to initial yolk re- serves. In species with low endotrophic potential (food 0.8 is required to complete metamorphosis), mean relative growth (carapace length) from the ®rst larval stage to S. riv the megalopa was 97.5% (n = 8), and signi®cantly larger

Log larval0.6 period (days) than 11.0% (n = 6) in species with high endotrophic potential (no food required, Kruskal±Wallis ANOVA, Log duration of egg stage (days) H(1, 7) = 4.5, P = 0.034). The megalopa of freshwater 0.4 species with a low relative growth and high larval –0.5 –0.4 –0.3 –0.2 –0.1 0.0 0.1 0.2 endotrophic potential were larger than those of the Log egg size (mm) marine and brackish species (see Table 5). Fig. 6. Relationship between duration of (a) embryonic and (b) larval development and egg size among American Sesar- minae. Mean values were used in the analysis for marine Endotrophic potential Sesarma (S. mar), marine Armases (A. mar), and riverine 2 Sesarma (S. riv) species. (a) r = 0.95, F(1, 5) = 87.7, P < 0.001, Among the Sesarminae, post-hatching yolk reserves and 2 y = 0.692 + 0.353x; (b) r = 0.66, F (1, 5) = 9.9, P = 0.025; nutritional independence of larvae signi®cantly y = 0.667 70.857x (see Tables 2 & 5). increased with egg size and body size of the ®rst larval stage (P < 0.001, Fig. 8). Starved larvae did not survive Larval development the ®rst stage in marine Armases (Diesel & Schuh, 1998), whereas in the brackish A. miersii, they always Larval stages survived one and occasionally two stages (Schuh & Diesel, 1995c). Similarly, in marine Sesarma species The brackish A. miersii has an abbreviated larval devel- only few starved larvae survived the ®rst larval stage opment with three zoeal stages compared to its marine (Staton & Sulkin, 1991), while in the brackish 150 R. Diesel, C. D. Schubart and M. Schuh

Table 5. Summary of the developmental pattern in the American Sesarminae and Uca. Duration of egg and larval development, number of larval stages, carapace length (CL) of the ®rst larval stage and the megalopa, and relative growth to megalopa from the ®rst larval stage. Ecotypes are: M, marine; B, brackish; FW, fresh water. Among FW we distinguish: R, riverine; C, cave; T, terrestrial

Duration Duration of CL of ®rst CL of Increase to of egg stage Larval larval stage larval stage megalopa megalopa Species Ecotype (days) stages (days) (mm) (mm) (%) Source a

Armases cinereum M 13.7 4 16.0 0.37 0.73 100.0 1, 2, 3 A. ricordi M 21.5 4 17.5 0.47 1.09 133.6 4 A. roberti M 16.0 4 16.8 0.52 1.26 142.3 4 A. miersii B 20.0 3 9.2 0.72 1.21 68.1 4, 5 Sesarma rectum M 3 9.0 0.71 1.00 41.4 6, 7 S. reticulatum M 15.2 3 9.0 0.48 1.00 83.9 1, 8 S. sp. (nr. reticulatum) M 17.3 3 8.0 9 S. curacaoense B 29.5 2 4.5 0.78 0.89 13.4 4, 10 S. fossarum FW / R > 60 2 5.9 1.69 2.00 18.3 13 S. ayatum FW / R > 60 2 3.0 1.82 2.01 10.4 13 S. verleyi FW / C 2 6.1 2.13 13 S. jarvisi FW / T > 40 2 3.0 1.48 1.42 74.1 13 Metopaulias depressus FW / T 60 2 5.2 1.75 1.99 13.7 11,12,13 Uca subcylindrica B 50 2 3.0 1.22 1.42 16.4 14 Uca spp. M 13±15 4±5 14±20 0.32±0.70 0.80±1.35 49±246 14 a Data from: (1) Seiple & Salmon, 1987; (2) Costlow & Bookhout, 1960; (3) Costlow et al., 1960; (4) Diesel & Schuh, 1998; (5) Schuh & Diesel, 1995c; (6) Fransozo & Hebling, 1986; (7) Fransozo & Negreiros-Fransozo, 1986; (8) Costlow & Bookhout, 1962; (9) Zimmerman & Felder, 1991; (10) Schuh & Diesel, 1995b; (11) Hartnoll, 1964a; (12) Diesel & Schuh, 1993; (13) Diesel & Schuh unpublished data; (14) Rabalais & Cameron, 1983, Rabalais & Gore, 1985.

Table 6. Overall mortality during the egg stage (Egg) calcu- aerobic respiration (see Herreid, 1980) has been studied lated from the number of prehatching eggs in ®eld-caught for each larval stage of marine A. ricordi, A. roberti, and females (n) and expected no. of newly spawned eggs. In brackish A. miersii,andS. curacaoense (see Schuh, addition some calculated mortalities from spawning to the larval (Larvae) and crab stage (Juveniles) based on the number 1995). Lowest lethal oxygen concentrations of 26% and of 2- to 6-day-old larvae and ®rst- or second-crab stage 27% were found for the ®rst larval stage of marine juveniles of cohorts (n) found with their mother in the ®eld. species, and increased within each species with larval Ecotypes are: M, marine; B, brackish; FW, fresh water with size and developmental stage, and with the size of the subgroups R, riverine; C, cave; T, terrestrial ®rst larval stage among the species (see Table 7). An analysis revealed a signi®cant positive partial correla- Mortality Ecotype (% ‹ sd) n Stage tion between body size of larvae and the critical oxygen saturation (y = 17.7 + 17.9x, r 2 = 0.60, P < 0.003, n = 13), Armases roberti M 16.5 ‹ 18.2 7 Egg by partialling out species (P = 0.77). In all species, A. miersii M 9.9 ‹ 18.7 7 Egg critical oxygen saturation decreased again in the Sesarma fossarum FW/R 12.4 ‹ 13.1 7 Egg megalopa stage, although it is larger than the respective Metopaulias FW/T 13.6 ‹ 21.0 16 Egg last larval stage. depressus M. depressus 20.1 ‹ 31.1 55 Larvae S. jarvisi FW/T 24.9 ‹ 29.4 8 Juveniles

PH-tolerance S. curacaoense all larval stages did (Anger & Schultze, 1994; Schuh & Diesel, 1995b). In the brackish The pH-tolerance of larvae during development to the S. curacaoense, larvae are facultative lecithotrophic, megalopa has been studied in the marine A. ricordi, whereas the larvae of all freshwater species so far A. roberti, the brackish A. miersii, S. curacaoense, the known are obligate lecithotrophic and survive riverine S. ayatum and the terrestrial crab M. depressus starvation to post-larval stages (Anger & Schuh, 1992; (Diesel & Schuh, 1993; Schuh, 1995; M. Schuh & R. Diesel & M. Schuh, pers. obs.). R. Diesel, pers. obs.). Because there are different number of larval stages, we here compare only survival through the ®rst larval stage. The comparison among Larval physiology species revealed that the ability to survive low pH signi®cantly increased with body size (r2 = 0.92, Oxygen requirements F(1, 3) = 34.2, P < 0.01), whereas survival in high pH was not related to body size of larvae (F(1, 3) = 0.19, P = 0.70; The critical oxygen saturation, that is, the limit of see Fig. 9a). Invasion of land by crabs 151

Table 7. Critical oxygen saturation (Cox, in mg/l) and body 2.6 size (CL, carapace length (mm)) of larvae (L1, ®rst larval stage, etc.) for marine and brackish species (data from Schuh, 1995)

L1 L2 L3 L4 Meg S. riv 1.8 Armases ricordi CL 0.47 0.57 0.70 0.89 1.09 Cox 27 28 30 32 29 A. roberti CL 0.52 0.67 0.77 1.00 1.26 1.0 Cox 26 30 33 41 26 A. miersii CL 0.71 0.86 1.00 ± 1.21 S. mar Cox 29 30 32 ± 28 A. mar Sesarma CL 0.78 0.86 ± ± 0.89 curacaoense Cox 34 33 ± ± 31 0.2

Carapace length of first larval stage (mm) 0.2 0.6 1.0 1.4 1.8 Egg size (mm) Fig. 7. Relationship between size of the ®rst larval stage and 10 km from the sea, overall salinity tolerance of larvae egg size at spawning among American Sesarminae. Mean was 20±40 PSU, but the ®rst larval stage survived 2±3 days in fresh water. This permits the larvae to be values were used in the analysis for marine Sesarma (S. mar), transported downstream through estuaries and reach a marine Armases (A. mar), and riverine Sesarma (S. riv) higher (35 PSU) and stable salinity offshore (Diesel & species. r2 = 0.98, F = 236.3, P < 0.0001, y = 0.0867 + 1.224x (1, 6) Schuh, 1998). An analysis of data on body size of the (see Tables 2 & 5). ®rst larval stage and the highest and lowest salinity extremes that were tolerated during the ®rst larval stage 40 revealed no signi®cant correlation between size and the highest tolerated salinity (F(1, 2) =0.17, P = 0.71; Fig. 9b), S. riv but a highly signi®cant correlation between larval size 2 30 and the lowest tolerated salinity (r = 0.99, F(1, 2) = 236.7, P < 0.01).

20 U. sub S. mar Comparison across lineages

10 Analogous to the brackish A. miersii and S. curacaoense, A. mar

Starvation survival (days) the brackish U. subcylindrica evolved similar reproduc- tive and developmental traits compared to its marine 0 relatives: a low fecundity (580 vs > 10 000 eggs), sub- 0.0 0.5 1.0 1.5 2.0 2.5 stantially larger eggs (520 mm3 vs 7±24 mm3), a much Carapace length of first larval stage (mm) longer egg-stage duration (about 50 vs 12±15 days), and Fig. 8. Relationship between larval size at hatching and the an abbreviated larval development (two vs ®ve zoeal duration of survival without feeding among American stages and 3 vs 14±20 days of larval development; see Tables 2 & 5) (Rabalais & Cameron, 1983; Thurman, Sesarminae (closed circles). Mean values were used in the 1984; Rabalais & Gore, 1985). Data on the relative analysis for marine Armases (A. mar: A. ricordi, A. roberti, clutch mass and egg-stage mortality in U. subcylindrica A. cinereum) and riverine Sesarma (S. riv: S. ayatum, S. 2 are not available. The relationship between egg size and fossarum). y = 0.835 + 15.01x, r = 0.95, F(1, 5) = 89.5, P < 0.001; the size of the ®rst larval stage, as well as that between &, Uca subcylindrica (U. sub) is given for comparison, but endotrophic potential and growth during the larval was not included in regression analysis. Data from Staton & phase is the same as in Armases and Sesarma (see Table Sulkin (1991), Anger & Schultze (1994), Schuh & Diesel 5). Marine Uca species have typical planktonic larvae, (1995b,c), Diesel & Schuh, 1998 (see Tables 2 & 5). whereas the brackish U. subcylindrica has non-feeding larvae (Rabalais & Cameron, 1985). Larval response to abiotic factors has been studied only for salinity. Salinity-tolerance Overall salinity tolerated during larval development ranged from 0.08 to 50 PSU, whereas the smaller larvae In Armases and Sesarma, the range of salinity tolerated of the marine congeners only tolerated 20 to 40 PSU by larvae to complete development into the megalopa (Rabalais & Cameron, 1983, 1985). increased from 15 PSU (25±40 PSU) in marine species to 50 PSU (5±55 PSU) in brackish species. But higher and lower salinity extremes were tolerated for short DISCUSSION periods of time (Costlow, Bookhout & Monroe, 1960; Foskett, 1977; Schuh & Diesel, 1995b,c; Diesel & Schuh, Evolution of egg size in relation to biotic and abiotic factors 1998). For example, in the marine A. roberti in which adults live along freshwater courses up to approx. Our results clearly favour the hypothesis that the 152 R. Diesel, C. D. Schubart and M. Schuh

10 frequent anoxia should favour small eggs. This hypoth- (a) esis is not supported by crabs, because species whose eggs may become exposed to anoxia, for example in 9 A.mar brackish water (Schuh, 1995; Schuh & Diesel, 1995a)or some freshwater habitats (e.g. Diesel, 1992b; Diesel & 8 Schuh, 1993; see also Graham, 1990), produce much larger eggs than the marine species in which eggs are less 7 pH

pH exposed to anoxia. Another hypothesis suggests that the risk of desicca- 6 tion in terrestrial habitats may have favoured larger eggs due to their reduced surface-to-volume ratio Marine 5 Brackish (Gibbs, 1974; Powers, 1975; Rabalais & Gore, 1985). Riverine This too does not explain the observed variation in egg Terrestrial 4 size. Various species with eggs most prone to desiccation 0.0 0.5 1.0 1.5 2.0 in dry and hot habitats (e.g. Gecarcinus lateralis, see 100 Bliss, 1968, and A. ricordi, see Diesel & Schuh, 1998) (b) A. mar have very small eggs. On the other hand, the riverine Sesarma species that are less exposed to desiccation have large eggs. Thus, direct selection on egg size by these factors does not account for the observed larger

) 10 egg size in the species studied. ppm ( y it n li a Selection on the larval stage: nutritional resources S Salinity (ppm) 1 The hypothesis that large eggs and lecithotrophic larval development in riverine decapods evolved in response to lack of food (MagalhaÄes & Walker, 1985; Rabalais & Gore, 1985; Anger, 1995b) is not supported by the FW 0.0 0.5 1.0 1.5 2.0 present study. First, the increased egg size occurs in all Carapace length of first larval stage (mm) brackish species and nutritional resources are abundant Fig. 9. Tolerance to (a) low and high pH and (b) salinity in brackish nurseries. For example, in supratidal rock in relation to the body size of the ®rst larval stage of American pools there are abundant food resources and many prey species and individuals for A. miersii larvae (Schuh & Sesarminae. Data points represent the highest and lowest Diesel, 1995a; Schuh, 1995): The mean copepod density values tolerated for successful development to the second in two pools with A. miersii larvae ranged from 43300 to larval stage. Species included are: marine Armases (A. 178600 per litre. Given a larval density of 200 per litre, mar = mean values of A. ricordi, A. roberti, and A. cinereum); each larva could feed on 200±900 copepods/day, which brackish, A. miersii, S. curacaoense; riverine, S. ayatum; is only one of several food items that yielded high terrestrial, M. depressus. ^, Lower limits in salinity tolerance survival to metamorphosis (Schuh, 1995, see Table 8). for endemic freshwater species whose upper limits were not Even pools that dried out and became salt-encrusted studied (not included in regression analysis). Low pH, contained 400±17 600 copepods/litre 24 h after being y = 6.161 70.943x and low salinity, y = 1.854 71.614x (see re®lled by rainwater (resulting in an average salinity of text). After Costlow et al. (1960), Diesel & Schuh (1993, 1998), 21 PSU; see Schuh, 1995; Schuh & Diesel, 1995a). The and Schuh (1995). food resources for S. curacaoense larvae in Jamaican mangrove swamps are likewise abundant. For U. sub- colonization of land by crabs occurred via brackish- cylindrica, Rabalais & Cameron (1985) invoked lack of water nurseries. We demonstrate that egg size has food as one of several factors that may have favoured already increased before the colonization of fresh water. the large egg size of the species. However, nutritional Hence, our discussion focuses on possible selective resources in the brackish ponds were apparently not episodes that favoured the increase in egg size, which studied, and their ecology and nutritional resources accompanied the invasion of brackish-water and appear quite similar to that of the A. miersii rock pools. subsequently freshwater habitats. Present-day brackish species probably produce larger eggs and larvae with a higher endotrophic potential than did their ancestors that colonized these habitats. Direct selection on egg size Our results cannot rule out that food limitation for larvae may have been involved in the past. However, Strathmann & Strathmann (1982, 1995) suggested that this is unlikely as coastal brackish waters generally an increase in egg size might be constrained by low are, compared to offshore seas, highly productive oxygen availability for the embryo. Hence, habitats with and nutrient-rich habitats (see Hartland-Rove, 1972; Invasion of land by crabs 153

Table 8. Potential nutritional resources in pools of different predation selects for an abbreviated development or salinities, and survival of A. miersii larvae (%) into the larger body size of larvae. megalopa stage if exclusively fed with a particular food item. In the brackish pool and pond nurseries of A. miersii Salinity in the pools ranged from 2 to 71 PSU (mean 35 PSU, n = 10). Biota density (ind, individuals) depended on the (see Schuh, 1995; Schuh & Diesel, 1995a) and salinity of pools, e.g. Cladocera occurred only in a pool with a U. subcylindrica (see Rabalais & Cameron, 1983), salinity of 2 PSU. Survival was tested in laboratory experi- predation is insigni®cant compared to other sources of ments with individually kept larvae (nt, food item not tested). larval mortality. Rabalais & Cameron (1983) even After data from Schuh (1995) and Schuh & Diesel (1995a) suggested that the lack of predation might have favoured large larval size in U. subcylindrica. Predator Mean Range Pools Survival Larvae Food resources (ind/litre) (ind/litre) (n) (%) (n) abundance in Jamaica mangrove swamps with a low tidal amplitude and low water depth, is low compared Cladocera 263 0±2633 10 65 20 to swamps in areas with high tidal amplitude. In the Ostracoda 3500 0±35000 10 nt latter, predation on larvae by planktivorous ®sh is likely Copepoda 13422 0±77000 10 100 20 178600 a to be intense and favour an export strategy (Morgan & 43300 a Christy, 1995). We did not quantify predator densities Nauplii 1866 0±8033 10 nt in Jamaican mangrove swamps, but frequent observa- Phytoplankton Abundant 10 95 20 tions showed that planktivorous ®sh were very rare, Detritus Abundant 10 100 20 whereas in an adjacent coastal lagoon, densities varied Artemia None 95 20 from zero to high. a Mean daily copepod density in two pools measured for 11 days An alternative hypothesis is that the observed larger while they contained A. miersii larvae (one hatch each). egg size in the brackish species evolved in their ancestors as a response to high predation in inshore larval habitats or estuaries and thus provided a predisposition for the Ketchum, 1983; Paulay, Boring & Strathmann, 1985; transition into landlocked-brackish nurseries (J. Christy, McLachlan & Yonow, 1989; Olson & Olson, 1989; pers. comm.). Accordingly, in areas with low tidal ampli- Osore, 1992; Selvam et al., 1992). tudes like Jamaica and the western Gulf of Mexico, Second, the further and considerable increase in egg larvae of the ancestral species may have experienced size following the transition from brackish to freshwater poor offshore dispersal, and spent more time inshore, nurseries is not explained by lack of food for planktonic exposed to intense predation. Such a scenario may have larvae. Eggs of the riverine Sesarma species have a 12- resulted in larger eggs if high inshore predation selected fold larger volume (1250 mm3) than that of the related for an abbreviated development or large body size of brackish S. curacaoense (98 mm3) despite having the larvae. We do not support this hypothesis because same number of larval stages. This enormous increase relatively few brachyuran species are reported to com- cannot be explained by lack of food for the following plete their larval development in inshore habitats or reasoning. If we assume that the ancestral freshwater estuaries (e.g. Rhithropanopeus harrisii, see Cronin, colonizer had the relative high endotrophic potential of Daiber & Hulbert, 1962), and these species clearly the larvae of S. curacaoense with very low nutritional evolved other anti-predator traits rather than abbre- requirements to complete metamorphosis, then egg size viating development (e.g. long spines, see Morgan, in the Jamaican freshwater Sesarma increased far 1987). Furthermore, various Caribbean congeners of the beyond the size required for obligate lecithotrophic brackish U. subcylindrica, A. miersii and S. curacaoense development because only 30% of the egg volume of live in similar coastal adult habitats and experience the riverine species is required for fully lecithotrophic larval same low offshore dispersal as larvae, but still adopt an development. This is exempli®ed by the brackish U. sub- export strategy and retained a non-abbreviated cylindrica with 520 mm3 and the terrestrial S. jarvisi with planktonic larval development (Morgan & Christy, 527 mm3 egg volume. In the latter there are still suf®cient 1995). yolk reserves to reach the second crab stage without feeding. Selection on the larval stage: abiotic factors

Selection on the larval stage: predation The most important physicochemical factors that may in¯uence larval survival in brackish-water nurseries Selection by intense predation during the larval stages are ambient temperature, oxygen saturation, pH and, may favour: (1) an abbreviated development in stages in particular, salinity (Kinne, 1967; Pechenik, 1987). and duration; (2) an export strategy of larvae from Increased chances of mortality as a result of ¯uctu- inshore habitats with high predation to low predation ating extreme temperatures could favour a fast and offshore nurseries (Christy, 1982; Morgan, 1990, 1992); abbreviated development. Such conditions occur in (3) larger body size; (4) traits like long spines, cryptic brackish nurseries, but less so in freshwater streams colours and predator avoidance behaviours (Morgan, and in the sea. For example, temperatures up to 1989; Morgan & Christy, 1995). Among these factors, 42.2 8C occurred in supratidal rock pools (A. miersii) increased egg size should only be favoured if intense for short periods, though, mortality related to high- 154 R. Diesel, C. D. Schubart and M. Schuh temperature peaks was not observed (see Schuh & 90 0 Diesel, 1995a,b). 80 Characteristic for landlocked brackish-water habitats is diurnal ¯uctuating oxygen saturation, including 70 10 anoxia (Schuh & Diesel, 1995a,b), which usually do not 60 occur in offshore plankton and freshwater streams (see 20 50 Hart, 1964). Hence, tolerating low oxygen saturation might be favourable for larvae of brackish species. This, 40 30 Salinity (PSU) however, would constrain an increase in larval size Salinity (ppt) 30 rather than support it. At least in the zoea stages of the Precipitation (mm) marine and brackish species (which lack proper gills) 20 40 oxygen uptake seems to be negatively related with size 10 or surface/volume ratio. Lamella gills for oxygen uptake 0 50 ®rst occurs in marine crabs in the megalopa stage (Yang May June July & McLaughlin, 1979; Hong, 1988). This appears to be Fig. 10. Salinity conditions of a supratidal rock pool on the the case in the brackish species too, as in both species a north coast of Jamaica, the larval habitat of Armases miersii. clear drop in the critical oxygen concentration occurs in the megalopa stage. Shown are salinity (left) and precipitation (right from top) The larvae of brackish A. miersii survive anoxia in over 3 months (redrawn after Schuh & Diesel, 1995a). rock pools by avoiding low oxygen concentrations and swimming within the surface layer where oxygen con- centration is above critical (Schuh & Diesel, 1995a). The mortality factor for larval development of Crustacea freshwater crab, M. depressus is an exception because (Goodbody, 1961; Kinne, 1967). These conditions the critical oxygen concentration at 17.3% is very low, clearly favour resistance of larvae towards abiotic stress but the larvae are very large. This species may be as well as a fast larval development. specially adapted to the extremely unfavourable oxygen Here, we analysed critical oxygen concentration, pH conditions that may occur in bromeliad leaf axils and salinity tolerance in relation to larval size across (Diesel, 1992b; Diesel & Schuh, 1993), or probably have species that are adapted to different habitats. These an advanced gill development. correlations may not re¯ect a causal relationship, for Among the species of Sesarminae, the tolerance to example, if larvae of freshwater species are large for survive low pH increases with the body size of the ®rst reasons other than the low salinity of fresh water. Only larval stage. Therefore, low pH in the nursery grounds salinity, and not pH and oxygen show a clear gradient may favour the production of large eggs and larvae. On between marine, brackish and freshwater nurseries. Jamaica only moderate variations in pH occur within This supports a hypothesis that correlates of larval size and between the sea water, brackish water and fresh are related to the performance under different physico- water (Hart, 1964; Hinga, 1992; Schuh & Diesel, 1995a; chemical regimes. A possible explanation for salinity Schuh, 1995). That is, during the colonization of fresh tolerance in relation to larval size could be that sodium water there was apparently no selection for an extreme loss in larger larvae is reduced because of their smaller pH tolerance. Though, acid conditions of pH 3 to 4 body-surface-to-volume ratio (see also Lucas, 1972). occur in the water stored in bromeliad-leaf axils where the larvae of M. depressus develop (Diesel, 1992b; Diesel & Schuh, 1993). CONCLUSIONS ON ENVIRONMENTAL FACTORS The range of salinity tolerated by larvae increased from marine to brackish species. Furthermore, the The results show that egg size in the studied crabs is tolerance of low salinity increased with the body size of correlated with many aspects of larval biology. Large the ®rst larval stage. Thus, episodes of low salinity in eggs hatch into large larvae with an abbreviated devel- the nurseries may favour large larvae. The ecology of opment (see also Rice, 1980; Gore, 1985), a high landlocked-brackish water nurseries supports this hy- endotrophic potential, and greater stress resistance. But, pothesis. With the colonization of these habitats, larval the size at metamorphosis is not related to egg size in development moved from a stable and constantly high marine and brackish species. This strongly suggests that salinity in the sea (35 PSU), to an ephemeral habitat there is a minimum or optimal size for metamorphosis. with extremely ¯uctuating salinity conditions (see Our results support only hypotheses that relate the Fig. 10). This is a common characteristic of the larval evolution of the increase in egg size that accompanied nurseries of S. curacaoense (see Schuh & Diesel, 1995b), the transition from the sea to brackish nurseries to the A. miersii (see Schuh & Diesel, 1995a), and of the abiotic conditions in the new larval habitat. An ephem- ephemeral nursery ponds of U. subcylindrica (see eral character distinguishes the ecology of these Rabalais & Cameron, 1983, 1985), where salinity may landlocked-brackish pools and ponds. Initially favour- ¯uctuate from fresh water (following heavy rain) to able abiotic conditions ± particularly in salinity ± may highly hypersaline conditions. Fluctuating salinity in ¯uctuate, become unfavourable and deteriorate in time coastal habitats is considered the paramount abiotic (e.g. drying out). These situations favour a fast larval Invasion of land by crabs 155 development, less critical moults during which mortality abundance. If physical conditions in a particular is highest and probably large and stress resistant larvae. nursery remained favourable for a few weeks, larval But the size at metamorphosis appears to be constrained mortality was extremely low (e.g. in U. subcylindrica, see in these crabs and an abbreviated larval development Rabalais & Cameron, 1983), much lower than in the must, therefore, be accomplished by: (1) reducing the marine plankton. However, the initially favourable number of free larval stages by passing through earlier physicochemical conditions may change suddenly and stages in the egg; (2) producing large larvae that have to unpredictably (heavy rainfall) or deteriorate with time grow little; (3) providing the larvae with large quantities (desiccation). In such ephemeral habitats, natural of yolk to speed up development. This is accomplished selection should favour a fast larval development and by the production of larger eggs. larger, more stress-resistant larvae. Both traits would be The comparisons between marine and brackish crabs associated with larger egg size. That is, larvae that show that species that allocate greater parental invest- hatched from larger eggs had higher survival chances in ment per offspring produce larvae that tolerate a brackish nurseries than their conspeci®cs hatched from broader range of environmental conditions. These a smaller egg. Considering the extremely high offshore results are basically consistent with models that predict mortality rates, the shift in larval development into increased mean parental investment per offspring in landlocked-brackish nurseries probably conferred a stochastic environments (Crump, 1981; McGinley, higher lifetime reproductive success to individual Temme & Geber, 1987; Schultz, 1991). However, the females, than a planktonic development. Under these increase in egg size accompanying the colonization of circumstances larger egg size should evolve, provided fresh water is related to different evolutionary scenarios that heritable variation in egg size occurs. than that outlined for brackish species and further A heritable component of egg size has been demon- research is needed here. strated for the shrimp Macrobrachium nipponense,of Various reproductive and developmental aspects of which three genotypes occur in the same aquatic system: the brackish-water species are intermediary between the one in fresh water, one in brackish lagoons and one in marine and the freshwater species and some interesting lower estuaries of Japan (Mashiko, 1992; Mashiko & patterns coincide with the colonization of land. For Numachi, 1993). Egg size increases and fecundity example, the drastic decrease in relative clutch mass decreases within these populations from the sea to fresh produced per lifetime that apparently occurred from water, as does salinity tolerance of larvae (Armada, marine to terrestrial species. A possible hypothesis to Ohno & Taki, 1993). A similar case is reported for the explain this pattern is that it re¯ects a trade-off between Amazon prawn Macrobrachium amazonicum, in which pre-spawning (yolk investment) and post-spawning egg size increases with the distance of populations from (parental care) reproductive effort. Marine species spend the sea (Odinetz Collart & Rabelo, 1996). Crossing only little time caring for the relative fast- developing Japanese brackish (small eggs) and freshwater (large small eggs, whereas the terrestrial M. depressus and eggs) strains produced F-1 hybrids with intermediate S. jarvisi show lengthy egg care and prolonged post egg and clutch sizes (Mashiko, 1992). hatching care (Diesel, 1989; Diesel & Horst, 1995). We We propose an evolutionary `one-step' invasion from found that with increasing emancipation from the sea offshore into landlocked nurseries as outlined above, and increasing egg size, the overall developmental time rather than a `progressive' approach of larval nurseries to metamorphosis increased considerably, because of the via inshore. Landlocked-brackish waters, which are lengthy embryonic development. geologically short-lived and ecologically unfavourable, are transitional habitats that were probably passed through in evolutionary short periods. This could Reconstruction of the transition onto land explain the paucity of species known to breed in this type of habitat, compared to the species-rich tropical Considering the reproductive pattern of the Sesarminae, marine and freshwater crab fauna (see `the paradox of their phylogenetic relationships and the particular brackish water' in Remane & Schlieper, 1971). ecological and topographic circumstances on Jamaica, The brackish ancestor of the endemic Jamaican fresh- we suggest the following scenario for the transition to water crabs is not available for current studies and the land. The proto-Sesarma that colonized the Jamaican present-day brackish S. curacaoense and A. miersii coast had the typical life history of marine Sesarminae: certainly made their transition into brackish nurseries it lived on land near the coast and released numerous relatively recently and possibly represent contemporary larvae for offshore development. Larval mortality in `transitory' species. crabs with marine planktonic larvae is usually very high The `second invasion step' was the colonization of (99.96%, see Warner, 1967). Instead of migrating to the nearby permanent fresh waters, followed by an adaptive sea, some females released larvae nearby in one of the radiation in the lotic system, which resulted in the numerous brackish limestone pools, or mangrove riverine species. Tolerance of low salinities, abbreviated ponds. This also occasionally occurs in species with development, and increased lecithotrophy achieved in marine planktonic larvae, such as A. ricordi and landlocked-brackish nurseries were important predispo- Cardisoma guanhumi (see Henning, 1975). In these sitions for this step. A further predisposition to breed in pools, larvae encountered no predators and high food riverine habitats was the burrowing behaviour of 156 R. Diesel, C. D. Schubart and M. Schuh brackish species. Riverine species too, live in burrow brackish and freshwater crabs with only one assump- systems in the riverbank, which extend down into the tion: larger embryos (eggs) show increased survival and water table. Larval development of the riverine developmental rates. Similar, to the argument of S. fossarum and S. dolphinum takes place in burrows, Sargent et al. (1987) for the advantage of large size on where they are protected from predators and the post-embryonic stages, our results suggest that large current. The general ecological conditions along embryos (eggs) have lower mortality rates. This is also freshwater courses vary little and presumably have not supported by a study on copepods where a negative changed much since the early colonization of riverine relationship between egg size and egg-stage mortality habitats. This may explain that the riverine species show was found (Guisande & Harris, 1995). However, more relatively similar reproductive pattern. From a riverine data are required to resolve the relationship between egg ancestor, a second radiation occurred into subterranean size and instantaneous egg-stage mortality. and terrestrial habitats (Hartnoll, 1964a,b; Schubart, Diesel & Hedges, 1998). Ecological conditions in the nursery habitats differed from riverine conditions and The evolution of developmental traits terrestrial species evolved various specializations in their life histories (see below). The evolution of egg size and developmental traits in Jamaican Sesarminae is related to the history of their colonization of land and the ecological conditions in Embryonic vs larval mortality ± the `safe harbour' the larval nurseries encountered during this process. hypothesis With the colonization of brackish nurseries, egg size and therefore fecundity appear to be strongly in¯uenced The `safe harbour' model of Shine (1978, 1989) and by the survival prospects of the larvae. With the Sargent et al.'s (1987) model (see above) differ in their colonization of fresh water, the mortality risk for early viewpoint. In one mode, emphasis is on the duration of juvenile crabs (e.g. predation, desiccation) when disper- the larval phase and in the other on the body size of the sing from the nursery, may have selected for larger size larvae. Our results support both models: (1) with the at metamorphosis and thus larger eggs. invasion into landlocked-brackish nurseries, the larval Other decapod lineages that independently colonized phase became the life-history stage that was prone to freshwater and terrestrial habitats essentially evolved mortality; (2) large larvae tolerate a broader range of similar traits as that reported here, although, these cases environmental conditions than small ones, and a fast, are not well documented. For example the Hymenoso- abbreviated development was advantageous in ephem- matidae (Lucas, 1980; Ng & Chuang, 1996) and the eral habitats. But, the traits of large larval size and Palaemonidae (South America: Walker, 1992; Odinetz abbreviated larval development are not independent Collart & Rabelo, 1996, Japan: Armada et al., 1993) from each other and both depend on egg size. have representatives in marine, estuarine-brackish water Our results do not coincide with the assumption of and freshwater habitats. Both taxa show an increased Shine (1978) and Sargent et al. (1987) that the longer egg size, decreased fecundity, and an abbreviated egg-stage duration of larger eggs increases overall egg- development with increasing independence from the sea. stage mortality. They suggest a negative correlation Further cases occur among the Sesarminae from East between egg-stage mortality rate and egg size. Total Asia, where marine species have many small eggs and egg-stage mortality did not increase in Jamaican four to ®ve zoeal stages (Baba & Miyata, 1971; Fukuda Sesarminae with large eggs despite their prolonged & Baba, 1976), the riverine species, Geosesarma embryonic development. This rather testi®es that egg- peraccae, has larger eggs and two zoeal stages (Soh, stage mortality per day decreased considerably with 1969), and the highly terrestrial species, Geosesarma increasing egg size. Possible explanations are: (1) the notophorum, has only one dozen large eggs and a direct mortality rates may be related to ecological factors in development (Ng & Tan, 1995). Species with a the habitat (extrinsic factors) and decrease with development in brackish water are not known from increasing tendency to breed in fresh water; (2) large Asia. eggs are less prone to mortality than small eggs (intrinsic The two non-feeding larval stages of the Jamaican factors). Extrinsic factors are unlikely to occur because endemic freshwater species are a rather non-adaptive the species in all habitats invariably carry and protect life-history stage on land where a direct development their eggs under their body. Therefore, instantaneous would be highly adaptive and eventually, direct develop- egg-mortality rates as a result of environmental factors ment may evolve. Dobkin (1963) suggested that vary less between species and habitats (e.g. sympatric modi®cations in the mode of development in decapods, coastal species with similar adult habitat but different e.g. a direct development, might be a function of evolu- egg sizes) than in free spawning taxa (e.g. anurans, tionary time that different lineages had colonized fresh teleosts; for free spawning vs brooding copepods; see water. Thus, the retention of two stages is consistent Kiorboe & Sabatini, 1994). with the relative recent origin of Jamaican freshwater Intrinsic factors are usually not considered by life- crabs. This is supported by the developmental mode of history models. Assuming an intrinsic egg-size advan- other decapod taxa known to have a long evolutionary tage, we can explain the mortality rates in the marine, history in fresh water. For example, the Malaysian Invasion of land by crabs 157

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