MORPHOLOGY OF THE LARVAL AND FIRST JUVENILE STAGES OF TWO JAMAICAN ENDEMIC

CRAB SPECIES WITH ABBREVIATED DEVELOPMENT, SESARMA WINDSOR AND METOPAULIASDEPRESSUS (DECAPODA: BRACHYURA: SESARMIDAE)

J. Ignacio Gonzalez-Gordillo, Klaus Anger, and Christoph D. Schubart

(JIG, correspondence, nacho.gonzalez@uca.es) Centro Andaluz de Ciencia y Tecnologıa Marinas (CACYTMAR), c/Republica

Saharaui s/n, Universidad de Cadiz, E-11510 Puerto Real – Cadiz, Spain;

(KA) Biologische Anstalt Helgoland, Stiftung Alfred-Wegener-Institut fur Polar- und Meeresforschung, 27498 Helgoland, Germany;

(CDS) Biologie I, Universitat Regensburg, 93040 Regensburg, Germany

A B S T R A C T

The complete larval development and the morphology of the first juvenile stages of two freshwater-breeding crab species endemic to

Jamaica are described and illustrated in detail in the present paper. One of these species, Sesarma windsor, lives in and near caves in the

karst regions of central western Jamaica, whereas the second species, Metopaulias depressus, occurs sympatrically but with a wider

range in western and central Jamaica in water-filled leaf axils of bromeliads. Even if these species are placed in separate genera, they are

extant representatives of the same adaptive radiation that resulted in at least ten Jamaican endemic crab species thriving in different land-

locked habitats. Consequently, larval morphologies of the two species are very similar, but conspicuously different from the

developmental patterns in their marine relatives. Both species display an abbreviated mode of development, showing morphological

reductions in some features and pre-displacement in the expression of several others. Both species pass through two non-feeding zoeal

stages, after which S. windsor moults to a facultatively lecithotrophic megalopa. In contrast, M. depressus directly moults from the zoea

II to a juvenile stage (also facultatively lecithotrophic) that shows a mixture of juvenile and vestigial larval characters, such as a partly

folded pleon, but no longer larval traits such as natatory pleopods. This represents the first record of larval development with no

megalopal stage for Sesarmidae. A closely related species from mangroves in the Caribbean and northeastern South America, Sesarmacuracaoense, shows a reduction in larval development, but with different morphological characteristics. We here discuss whether this

could be a shared ontogenetic character or the consequence of convergent evolution.

KEY WORDS: bromeliads, fresh water, larval development, mangroves, Thoracotremata

DOI: 10.1651/08-3110.1

INTRODUCTION

During its relatively short geological history since its lastemergence in the middle Miocene (Robinson, 1994;Iturralde-Vinent and MacPhee, 1999), the Caribbean islandof Jamaica has become a hot spot of evolution in theTertiary and Quaternary, revealing several conspicuousprocesses of adaptive radiation in both terrestrial and limnicenvironments that occur in various taxa of vertebrates,invertebrates, and plants (see Hedges, 1966; Graham,2003). Among Crustacea, a lineage of at least ten endemicspecies of sesarmid crabs has evolved from a single marineancestor, now inhabiting various types of non-marinehabitats in the interior of the island, including rivers andcreeks, subterranean limestone caves, the moist floor offorest-covered karst hills, snail shells, and leaf axils ofbromeliad plants (Hartnoll, 1964; Schubart et al., 1998;Diesel et al., 2000; Schubart and Koller, 2005).

Radiations originating from marine organisms in non-marine environments would be impossible without theevolution of major life-history adaptations. In particular, theplanktonic and typically planktotrophic larval phase of marinedecapod crustaceans may be considered a crucial bottleneckfor limnic and terrestrial invasions, because the early life-cycle stages are especially sensitive against planktonic foodlimitation, desiccation, variability in temperatures or ionconcentrations, and other stress factors occurring in non-

marine habitats (for review, see Anger, 2001; 2003). Amongthe endemic Jamaican crabs, reproductive and developmentaladaptations have been observed in about one half of thepresently known species, while the biology of the remainingspecies of this clade is still largely unknown (Anger et al.,2007, and earlier papers cited therein). In all species for whichlife history investigations have become available, the larvalphase is abbreviated, comprising only two non-feeding zoealstages and a facultatively lecithotrophic megalopa. Thesereproductive traits imply a shortening of the vulnerable free-living larval phase and a greatly reduced dependence onplanktonic food sources. Moreover, there seems to be a trendtowards an enhanced maternal brood care that may furthermitigate environmental stress and the risk of predation (forrecent discussion and references, see Anger et al., 2007).

While physiological and biochemical aspects of thelarval biology have recently been studied in severalendemic Jamaican species, details of larval morphologyhave remained almost unknown. Only an incompletedescription was included in the pioneering study byHartnoll (1964), showing for two species (the ‘‘bromeliadcrab,’’ Metopaulias depressus Rathbun, 1896, and a riverinespecies, Sesarma bidentatum Benedict, 1892) that theyhave a free-living larval phase and do not show directdevelopment like most other freshwater crabs.

The present study provides the first complete anddetailed description of larval and early juvenile morphol-

JOURNAL OF CRUSTACEAN BIOLOGY, 30(1): 101-121, 2010

101

ogy for any of the endemic Jamaican crab species. Westudied the early development in a riverine crab, Sesarmawindsor Turkay and Diesel 1994 [redescribed by Schubartet al. (1997)], as well as in the terrestrial species M.depressus. While S. windsor lives in or near to limestonecaves and subterranean streams in central Jamaica (Schu-bart et al., 1997; Schubart and Koller, 2005), M. depressusis associated with large bromeliad plants growing on forest-covered limestone hills and on trees in the northern parts ofcentral and western Jamaica (Hartnoll, 1964; Diesel et al.,2000). They live and breed in water-filled leaf axils of thebromeliads. In order to do so, they evolved a complexbrood care behaviour and an important degree of socialstructure (Diesel and Schubart, 2007 and referencestherein). Physiological aspects of their reproduction andlarval development, including fecundity, hatching patterns,storage and utilization of chemical energy, larval indepen-dence from food, oxygen consumption, and calciumdemand, have experimentally been investigated by Angerand Schuh (1992), Diesel and Schuh (1993), Diesel (1997),and Anger and Schubart (2005).

The larval morphology of these two endemic species iscompared with that of Sesarma curacaoense De Man, 1892,a crab that lives in brackish mangrove habitats on Jamaicaand other Caribbean islands, as well as in coastal regions ofAtlantic Central America and northeastern South America(Abele, 1992) southwards to the state of Bahia in Brazil(Almeida et al., 2006). This species is considered one of theclosest marine relatives of the limnic-terrestrial clade onJamaica and may therefore be a model for ancestral traits inlarval development and morphology (for morphological andmolecular evidence of phylogenetic relationships, seeHartnoll, 1964; 1971; Schubart and Cuesta, 1998; Schubartet al., 1998; 2000). Similar to all endemic Jamaicansesarmids, for which the life history has been studied, thiscrab reveals an abbreviated and partially food-independentlarval development (Anger, 1995; Anger et al., 1995;Schubart and Cuesta, 1998), making it plausible that thesepatterns may already had been present in the colonizingmarine species that gave rise to the adaptive radiation ofcrabs on Jamaica. Moreover, we include in our comparisonsof larval morphology the closely related estuarine or coastalmarine species, Sesarma reticulatum (Say, 1817) and S.rectum Randall, 1840, which present a more extended typeof larval development with three zoeal stages (Costlow andBookhout, 1962; Fransozo and Hebling, 1986).

MATERIALS AND METHODS

Collection and Maintenance of Crabs

All crabs used in this study were collected on Jamaica during the period 9-22 March, 2003. Ovigerous females of S. windsor were obtained from thetype locality of this species, the Mouth River, next to the Printed CircuitCave near Albert Town in Trelawny, those of M. depressus from theDolphin Head area in western Jamaica (Hanover). After collection, thecrabs were transported to the Discovery Bay Marine Laboratory(Discovery Bay, St. Ann), and subsequently maintained in freshwaterkept at 24 6 3uC and a natural light cycle (ca. 12:12h L:D), providingplant materials from the Martha Brae River (Jamaica: Trelawny) as naturalfood sources. Later, the crabs were transported to the Helgoland MarineBiological Laboratory (Germany). Here they were maintained in aquariawith aerated tap water and limestone rocks added as a calcium source, at

similar conditions of temperature and light as on Jamaica (24 6 1uC; 12:12h L:D). Frozen isopods and grated carrots were given as food. Stones withcrevices were added as a substrate allowing the crabs to hide or to climbemerged in the air. Ovigerous females were checked at least twice daily forthe occurrence of freshly hatched larvae.

Larval rearing

Larvae of both S. windsor and M. depressus hatched in April–May 2003.The zoeae were transferred with wide-bore pipettes to individual 100 mlNuncTM plastic bowls filled with freshwater (conductivity 0.41 mS/cm;checked with a portable Hanna Instruments [Kehl, Germany] ‘‘Combo pHand EC’’ apparatus). The conditions of temperature and light were thesame as in the maintenance of adult crabs. Water was changed daily, andthe larvae were checked for moults or mortality. The zoeae of both speciesare non-feeding, whereas individuals of the next following stage(megalopa or juvenile) eat when food is available (complete andfacultative lecithotrophy, respectively; see Anger and Schubart, 2005).Hence, no food was given throughout the zoeal phase, while the followingstage was fed in daily intervals with freshly hatched Artemia sp. nauplii(ca. 10-15/ml). Before the nauplii were added to the cultures, they werecarefully rinsed with freshwater using a sieve (100 mm mesh size) and asqueeze bottle in order to avoid increased salinities in the larval cultures.

Morphological studies and size measurements

Exuviae and specimens were fixed and preserved in 70% ethanol.Descriptions of different instars were based on at least 10 specimens orexuviae of each larval stage. Prior to drawing, larval tissues were partiallydigested with heated lactic acid and stained with Clorazol Black,improving the observation of larval structures (Landeira et al. 2009).Appendages were dissected in water and mounted in permanent slidesusing Faure’s liquid Reyne (1949). Line illustrations were made under acompound microscope equipped with Nomarski differential interferencecontrast optics and a camera lucida. The sequence of the larval descriptionprogresses from anterior to posterior, and the setal armature on appendagesis described from proximal to distal segments, following Clark et al.(1998). Setal groups on successive segments are separated by a comma andgroups of setae on the same segment, or on different lobes of the sameendite, are separated by a plus sign (+).

The following measurements were taken in lateral view with acalibrated ocular micrometer: carapace length of zoeal stages as thedistance from the frontal to the posterior margin of the carapace (CL);megalopa or juvenile carapace width (CW) as the greatest distance acrossthe carapace; and megalopa or juvenile carapace length (CL) from thefrontal to the posterior margin of the carapace. The sizes given are thearithmetic mean 6 95% confidence intervals.

RESULTS

Sesarma windsor

Three larval stages (two zoeae and the megalopa) plus thefirst juvenile crab instar are described and illustrated indetail.

Zoea I (Fig. 1; Table 1).—Dimensions. CL: 1.87 60.02 mm

Carapace (Figs 1A, B). Globose and without tubercles.Rostrum very small. No dorsal and lateral spines.Posterolateral margin with several small plumose setae.Eyes stalked.

Antennule (Fig. 1C). Uniramous, endopod absent. Exo-pod unsegmented, broad at base with 3 short aesthetascsplus 1 simple distal seta.

Antenna (Fig. 1D). Unsegmented protopod undevelopedand without rows of spinules. Unsegmented endopod budapproximately three times as long as protopod. Exopodwith two short and equal terminal setae.

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Fig. 1. Sesarma windsor (Zoea I): A, lateral view; B, rostrum; C, antennule; D, antenna; E, maxillule; F, maxilla; G, first maxilliped; H, secondmaxilliped; I, third maxilliped; J-N, first to fifth pereiopod; O, P, pleon and telson. Scale bars: A 5 1 mm; B, J-P 5 500 mm; C-F 5 100 mm; G-I 5250 mm.

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 103

Mandible. Not well developed, with an unsegmentedpalp and glabrous.

Maxillule (Fig. 1E). Coxal endite with 7 small setalprocesses. Basial endite with 3 simple setae and 3 incipient

setal processes. Endopod unsegmented with 2 subterminalplus 2 terminal simple setae. Exopod absent.

Maxilla (Fig. 1F). Coxal endite bilobed with 6 min setalprocesses and 2 simple setae plus 2 incipient setal

Table 1. Setation pattern and others characteristics of zoea I of Sesarma reticulatum, S. rectum, S. curacaoense, S. windsor, and Metopaulias depressus.Setal groups on successive segments are separated by a comma and groups of setae on the same segment, or on different lobes of the same endite, areseparated by a plus sign (+). n: variable number of setae (indeterminable); 0: without seta; ‘‘-’’: no data available. (*): data taken at the expense of drawings.

Species

S. reticulatum S. rectum S. curacaoense S. windsor M. depressus M. depressus

Author description Costlow andBookhout, 1962

Fransozo andHebling, 1986

Schubart and Cuesta, 19981 present study present study Hartnoll, 1964Anger et al., 1995 2

Carapace Length (mm) 0.48* 0.52* 0.74 6 0.02 1 1.87 6 0.02 1.74 6 0.03 -0.81 6 0.04 2

Carapace

Eyes sessile sessile sessile stalked stalked stalkedDorsal spine yes yes yes no no noRostral spine yes yes yes very small small smallLateral spines no no no no no no

Antennule

Exopod 4 + 2 3 + 2 3 + 11/3 + 22 3 + 1 3 + 3 2

Antenna

Protopod long with spines long with spines long with spines reduced reduced reducedEndopod bud bud bud bud bud budRatio end./protop. 1/3 1/3 1/3 3 2 ?Exopod 2 2 2 2 1 2

Mandible palp absent absent absent 0 0 0

Maxillule

Protopod - - 0 0 0 0Coxal endite 5 5 6 7 5 0Basial endite 5 5 5 3 + 3 9 0Endopod 1,1 + 4 1,1 + 4 1,1 + 4 2 + 2 0 0

Maxilla

Coxal endite 7 5 + 3 5 + 4 6 + 4 3 + 2 0Basial endite 5 + 4 5 + 4 5 + 4 4 + 5 3 + 2 0Endopod 2 + 3 2 + 3 2 + 3 2 + 2 + 2 1 + 2 0Exopod 4 + 1 4 + 1 3-4 + 1 30-35 10 + 3 7

First Maxilliped

Coxa - 0 - 0 0 0Basis 2 + 2 + 3 + 3 2 + 2 + 3 + 3 2 + 2 + 3 + 3 2 + 2 + 2 + 2 0 0Epipod - - - 0 0 0Endopod 2,2,1,2,1 + 4 2,2,1,2,1 + 4 2,2,1,2,1 + 4 2,2,3,1 + 3 1,1,3,2 0,0,2Exopod 4 4 4 4 4 4

Second Maxilliped

Coxa - 0 - 0 0 0Basis 1 + 1 + 1 2 + 2 + 1 1 + 1 + 1 + 1 1 + 1 + 1 0 0Endopod 0,1,5 0,1,5 0,1,6 1 2 0 0

0,1,5 2

Exopod 4 4 4 4 4 4

Third Maxilliped absent absent biramous bud biramous bud biramous bud biramous bud

First Pereiopod absent absent uniramous bud uniramous bud uniramous bud uniramous bud

Second Pereiopod absent absent uniramous bud uniramous bud uniramous bud uniramous bud

Third Pereiopod absent absent uniramous bud uniramous bud uniramous bud uniramous bud

Fourth Pereiopod absent absent uniramous bud uniramous bud uniramous bud uniramous bud

Fifth Pereiopod absent absent uniramous bud uniramous bud uniramous bud uniramous bud

Abdominal knobs on somites II, III on somites II, III on somites II, III no somite II -

Pleopods absent absent buds buds buds buds

Telson 3 + 3 3 + 3 3 + 3 3-4 + 3-4 3-4 + 3-4 3 + 3

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processes, respectively. Basial endite bilobed with 4 and5 min setal processes, respectively. Endopod unsegmented,trilobed with 2 simple long setae on each lobe respectively.Scaphognathite well developed with 30-35 marginalplumose setae.

First Maxilliped (Fig. 1G). Coxa naked. Basis with 8medial short simple setae arranged 2 + 2 + 2 + 2. Endopod4-segmented with 2, 2, 3, 1 + 3 simple setae. Exopodunsegmented, with 4 long terminal plumose natatory setae.Epipodal bud present.

Second Maxilliped (Fig. 1H). Coxa glabrous. Basis with3 medial short setae arranged 1 + 1 + 1. Endopodunsegmented with 1 subterminal plus 1 terminal simplesetae. Exopod unsegmented, with 4 long terminal plumosesetae.

Third Maxilliped (Fig. 1I). Rudimentary, unsegmentedand lacking setae, with differentiated endopod, exopod andepipodite.

Pereiopods. (Figs. 1J-N) Five pereiopods developed, butnon-functional, 5-segmented and without setae. First pairbilobed (cheliform). Exopods lacking.

Pleon (Figs. 1O, P). Six pleomeres. First somite with 4dorsal simple setae. Somites II to V with a pair of smalldorsal setae. No lateral knobs. Uniramous pleopod buds onsomites II to V.

Telson (Fig. 1O). Telson bifurcated, each furcal armwithout lateral or dorsal spines and with 3 or 4 serrulatespinous processes on posterior margin, not necessarilybearing the same number of setae on each arm. Tiny dorsalspines are visible on the distal part of furcal arms.

Zoea II (Fig. 2; Table 2).—Dimensions. CL: 1.91 60.03 mm.

Carapace. Similar morphology to that of stage I. Eyesstalked.

Antennule (Fig. 2A). Setation unchanged from that ofzoea I.

Antenna (Fig. 2B). Protopod unchanged. Endopod 6-segmented, exceeds three times the protopod length.Exopod half length of the endopod with setationunchanged.

Mandible (Fig. 2C). Similar in form to previous stage.Maxillule (Fig. 2D). Protopod with very small seta on

dorsal margin, corresponding probably to a degeneratedexopod. Coxal endite unchanged. Basial endite with 5simple setae (2 thin and 3 larger) and 7 small setalprocesses. Endopod 2-segmented with 1 + 1 small setalprocesses and 2 + 2 longer simple setae.

Maxilla (Fig. 2E). Coxal endite bilobed with 10 smallsetal processes and 2 simple setae plus 2 small setalprocesses, respectively. Basial endite bilobed with 7 and 6small setal processes, respectively. Number of setalprocesses on the coxal and basial endites hard to determine,due to their small size, could show variation. Endopodunchanged. Scaphognathite with 63-65 plumose marginalsetae plus 2 medial plumose setae on inner side.

First Maxilliped (Fig. 2F). Coxa and basis unchanged.Epipod bud with several marginal protuberances on distalend. Endopod 5-segmented with 2, 2, 1, 2, 1 + 3 simplesetae. Exopod totally segmented, with 11-13 long terminalplumose natatory setae.

Second Maxilliped (Fig. 2G). Coxa and basis un-changed. Endopod 4-segmented with 0, 0, 1, 2 simplesetae. Exopod partially segmented, with 10 or 11 longterminal plumose natatory setae.

Third Maxilliped (Fig. 2H). Endopod 5-segmentedwith small protuberances on the distal end of the fifthsegment. Exopod unsegmented with several terminalprotuberances. Epipod 2-segmented, with numerousincipient marginal sparsely plumose setae on the distalsegment.

Pereiopods. Uniramous five-segmented lacking setae.Non-functional.

Pleon (Figs. 2I, J). First somite with 6-7 anterior dorsalsetae. Somites II to V with a pair of posterior dorsal setae.Five pairs of pleopods on somites II to VI as buds.

Telson (Fig. 2I). Telson with 4 pairs of serrulate spinousprocesses on posterior margin.

Megalopa (Figs. 3-4; Table 3).—Dimensions. CL: 1.94 60.06 mm; CW: 1.85 6 0.04 mm.

Carapace (Figs 3A-B). Longer than broad and withoutspines. Frontal region broad with wide angled frontal edge,ending in a short rostrum bent downward. Tubercles andsetation as shown in Fig. 3B. Eyes stalked.

Antennule (Fig. 3D). Peduncle 3-segmented with 2plumose, 1 simple, and 1 simple setae, respectively; basalsegment bulbous. Endopod not present. Exopod asunsegmented flagellum with 2 subterminal simple setaeplus 4 aesthetascs and 1 simple seta.

Antenna (Fig. 3E). Peduncle 2-segmented, glabrous.Endopod (flagellum) slender, 6-segmented, with 1, 1, 0,3, 3 + 1 (longer simple seta), 3 setae, respectively. Noexopod present.

Mandible (Fig. 3C). Fully developed, bearing a hardplate-like structure with distal cutting edge and a molarprocess. Mandibular palp (endopod) 2-segmented with 5-7simple setae on the distal segment.

Maxillule (Fig. 3F). Protopod with 2 long plumose setaeon dorsal margin. Coxal endite fringed with 13 plumo-denticulate setae. Basial endite with 6 denticulate processesplus 10 sparsely plumose setae. Endopod 2-segmented with2 sparsely plumose setae on the proximal segment and 2medial simple setae plus 1 short distal simple seta on distalsegment.

Maxilla (Fig. 3G). Coxal endite bilobed with 8 or 9sparsely plumose setae and 3 plumose setae, respectively.Basial endite bilobed with 10 sparsely plumose setae oneach lobe and 1 simple seta between both. Endopodunsegmented with 1 short plumose seta on the dorsalmargin. Scaphognathite with 61 to 65 marginal plumosesetae plus 2 plumose setae on the inner side and 3 plumosesetae on the outer side.

First maxilliped (Fig. 4A). Coxal endite with 12 sparselyplumose setae. Basial endite with 14 sparsely plumosesetae. Epipodite of triangular shape with 3 sparselyplumose setae proximally plus 10 sparsely plumose setaedistally. Endopod unsegmented with 6 simple setae.Exopod 2-segmented, glabrous on proximal segment andbearing 5 plumose setae on distal segment.

Second maxilliped (Fig. 4B). Coxa and basis notdifferentiated and glabrous. Epipodite reduced to glabrous

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 105

bud. Endopod 4-segmented with 1 plumose seta, 0, 4sparsely plumose setae, 6 sparsely plumose setae plus 2plumodenticulate setae, respectively. Exopod 2-segmentedwith 0 and 5 plumose setae, respectively.

Third maxilliped (Fig. 4C). Fully developed. Basis with22-24 plumose setae. Long epipodite with 14-16 plumosesetae plus 27-28 sparsely plumose setae, placed as shown.Endopod 5-segmented with 20-22, 11, 4, 4, 9 sparsely

Fig. 2. Sesarma windsor (Zoea II): A, antennule; B, antenna; C, mandible; D, maxillule; E, maxilla; F, first maxilliped; G, second maxilliped; H, thirdmaxilliped; I, J, pleon and telson. Scale bars: A-E 5 100 mm; F-H 5 200 mm; I-J 5 1 mm.

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Table 2. Setation pattern and others characteristics of zoea II of Sesarma reticulatum, S. rectum (not final stage in these species), S. curacaoense, S.windsor, and Metopaulias depressus. For coding see Table 1.

Species

S. reticulatum S. rectum S. curacaoense S. windsor M. depressus M. depressus

Author description Costlow andBookhout, 1962

Fransozo andHebling, 1986

Anger et al., 1995 present study present study Hartnoll, 1964

Carapace Length (mm) 0.62 0.9* 0.92 6 0.07 1.91 6 0.03 1.82 6 0.05 -

Carapace

Eyes stalked stalked stalked stalked stalked stalkedDorsal spine yes yes yes no no noRostral spine yes yes yes very small small smallLateral spines no no no no no no

Antennule

Peduncle 0 0 0 0 0 0Exopod 4 + 2 4 + 1 6 + 2 3 + 1 1 2

Antenna

Protopod long with spines long with spines long with spines reduced reduced reducedEndopod bud unsegmented bud unsegmented bud 2-segmented bud 6-segmented bud 4-segmented bud

unsegmentedRatio end./protop. - - - .3 .2 -Exopod 2 2 2 2 2 0

Mandible palp - absent absent 0 0 0

Maxillule

Protopod 1 1 1 1 0 0Coxal endite 5 5 7 7 0 0Basial endite 7 7 8 + 1 + 3 5 + 7 8 3Endopod 1,1 + 4 1,1 + 4 1,1 + 4 1 + 1,4 0,0 0

Maxilla

Coxal endite 5 + 3 4 + 4 4-5 + 4 10 + 4 3 + 1 0Basial endite 5 + 4 5 + 4 4-5 + 4 7 + 6 0 + 4 0Endopod 2 + 3 2 + 3 2 + 3 2 + 2 + 2 0 0Exopod 5 + 3 5 + 3 8 + 3 63-65 + 2 14 + n 14 + n

First Maxilliped

Coxa - 0 0 0 0 0Basis 2 + 2 + 4 + 3 2 + 2 + 3 + 3 10 2 + 2 + 2 + 2 0 0Epipod - - - n d 0 0Endopod 2,2,1,2,1 + 4 2,2,1,2,5 2,2,1,2,3 + 2 2,2,1,2,1 + 3 0,0,0,0 0,1Exopod 6 6 6 11-13 14 13

Second Maxilliped

Coxa - 0 - 0 0 0Basis 1 + 1 + 1 1 + 1 + 1 + 1 1 + 1 + 1 + 1 1 + 1 + 1 0 0Endopod 0,1,1 + 2 + 3 0,1,6 0,1,4 + 2 0,0,1,2 0 0Exopod 6 6 6 10-11 13-14 12

Third Maxilliped absent absent biramous bud

Coxa 0 0 0Basis 0 0 0Epipod 0, n 0 0Endopod 0,0,0,0,n 0 0Exopod n 0 0

First Pereiopod absent absent uniramous bud 5-segmented 5-segmented -

Second Pereiopod absent absent uniramous bud 5-segmented 5-segmented -

Third Pereiopod absent absent uniramous bud 5-segmented 5-segmented -

Fourth Pereiopod absent absent uniramous bud 5-segmented 5-segmented -

Fifth Pereiopod absent absent uniramous bud 5-segmented 5-segmented -

Abdominal knobs on somites II, III on somites II, III on somites II, III no variable -

Pleopods buds buds biramous buds biramous buds biramous buds buds

Telson 3 + 3 3 + 3 3 + 3 4 + 4 3-4 + 3-4 -

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 107

plumose setae. Exopod 2-segmented with 5-6 shortplumose setae on outer margin of the proximal segment,and 5 long plumose setae on distal one.

Pereiopods (Figs. 4D-H). Fully developed with allsegments well differentiated.

Pleon (Fig. 4N). First somite medio-dorsally fringedwith a row of 13 min setae. Rest of setation as shown.

Pleopods (Figs. 4I-L). Biramous. Endopod of first to fourthpairs with 1 terminal cincinnuli. Exopod of first to fourth pairsunsegmented with 6, 6, 6 and 3 plumose setae respectively.

Fig. 3. Sesarma windsor (Megalopa): A, dorsal view; B, carapace, lateral view; C, mandible; D, antennule; E, antenna; F, maxillule; G, maxilla. Scalebars: A-B 5 1 mm; C-G 5 100 mm.

108 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 30, NO. 1, 2010

Fig. 4. Sesarma windsor (Megalopa): A, first maxilliped; B, second maxilliped; C, third maxilliped; D-H, first to fifth pereiopod; I-M, first to fifthpleopod; N, pleon and telson. Scale bars: A-C, I-L 5 100 mm; D-H 5 250 mm; M, N 5 500 mm.

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 109

Uropod (Fig. 4M). Uniramous. Exopod with 3 plumosesetae.

Telson (Fig. 4N). Subquadrate, broader than long,smooth, with posterior margin concave and glabrous.

First juvenile crab (Fig. 5).—Dimensions. CL: 2.07 60.17 mm; CW: 2.10 6 0.09 mm.

Carapace (Fig. 5A). Slightly broader than long andflattened. Frontal region broad, measuring one half ofcarapace width, bearing a row of small setae on the anteriormargin. Anterolateral margin with an acute spinousprocess. Posterior lateral margin filled with simple setae.

Third maxilliped (Fig. 5B). Increased in size comparedto previous instar, but with similar shape.

Pleon (Fig. 5C). Six somites present with setation asshown.

Pleopods. Small buds on somites II to V.Telson (Fig. 5C). Triangular shape with setation as

shown.

Metopaulias depressus

Two larval stages (zoeae) and the first two juvenile crabinstars are described and drawn in detail. No megalopal

Table 3. Setation pattern and other characteristics of the megalopal stage of Sersarma reticulatum, S. rectum, S. curacaoense, and S. windsor. For codingsee Table 1.

Species

S. reticulatum S. rectum S. curacaoense S. windsor

Author description Costlow and Bookhout,1962

Fransozo and Hebling,1986

Anger et al., 1995 present study

Carapace length (mm) 0.90 0.79* 1.04 6 0.07 1.94 6 0.06

Carapace width (mm) 0.65 0.60* 0.65 6 0.04 1.85 6 0.04

Carapace

Rostral spine long, forwards small, downwards small, downwards small, downwards

Antennule

Peduncle 3,0,1 3,1,1 1,1,1 2,1,1Exopod 4 + 2,5 4 + 1,5 + 2 1 + 3,2 + 3 2 + (4 + 1)

Antenna

Peduncle 1,1,1 0,1,1 0,1,1 0,0Protopod no - reduced, with spines noEndopod 0,1,4,? 0,2,0,4,0,4 0,2,1,5,0,2 1,1,0,3,3 + 1,3Exopod no No 2 no

Mandible palp 0,4 0,4 0,0,4 0,5-7

Maxillule

Protopod 2 2 2 2Coxal endite 10 7 3 + 6 13Basial endite 15 13-15 6 + 5 + 2 6 + 10Endopod 1,1 + 1 + 2 1,5 1 + 1,2 + 2 1 + 1,2 + 1

Maxilla

Coxal endite 12 8 + 4 (4 + 3) + 4 8-9 + 3Basial endite 15 7p + 5 (4 + 3) + (4 + 3) 10 + 1 + 10Endopod 2 + 2 0 2 + 3 1Exopod 32 33-36 + 2 1 + 2 + 22-24 2 + 3 + 61-65

First Maxilliped

Coxa 5 6 - 12Basis 14 10 3-4 + 2-3 14Epipod 1 + 3 2 + 3 4 3 + 10Endopod 1,1 + 2,1 + 1,2,1 + 4 2 1p + 1,1,3 + 1,4 + 1 5 + 1Exopod 1,8 2,1 + 3 2-3,5 0,5

Second Maxilliped

Coxa - - - 0Basis 4 1 + 1 4 0Endopod 1,1,4,8 0,1,3,6 1,1,4,3 + 2 + 3 1,0,4,6 + 2Exopod 7 1 + 1,4 0,6 0,5

Third Maxilliped

Basis 6 7 6 22-24Epipod 12 3 + 12 5 + 9 16 + 27Endopod 8,6,2,4,6 8(9),6,3,4,5(6) 6 + 2,5 + 4,1 + 2,3 + 1,6 20-22,11,4,4,9Exopod 0,5 0,5 0,5 6,5

Pleopods

Endopod (hooks) 2,2,2,2,2 2,2,2,2 2,2,2,2 1,1,1,1Exopod 14,13,12,11,6 13,13,13,11,6 12,12,12,9,6 6;6;6;3;3

110 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 30, NO. 1, 2010

stage was observed during the larval development, but thefirst juvenile shows vestigial characters (e.g., not com-pletely folded pleon, quadratic telson) resembling mega-lopae.

Zoea I (Fig. 6; Table 1).—Dimensions. CL: 1.74 6 0.03.Carapace (Figs 6A-B). Globose and without tubercles.

Rostrum small, directed downwards. No dorsal and lateralspines. Lateral margins without setae, but 1 small setalwreath on dorsal surface. Eyes stalked.

Antennule (Fig. 6C). Uniramous, endopod absent. Exo-pod unsegmented broad at base with 3 short aesthetascsplus 3 simple seta located distally.

Antenna (Fig. 6D). Unsegmented protopod not muchdeveloped and without rows of spinules. Unsegmentedendopod bud approximately two times of the length ofprotopod. Exopod with 1 short terminal simple seta.

Mandible. Not well developed, with an unsegmentedpalp lacking setae.

Maxillule (Fig. 6E). Coxal endite with 5 small setalprocesses. Basial endite with 9 small setal processes.Endopod unsegmented and glabrous. Exopod absent.

Maxilla (Fig. 6F). Coxal endite bilobed with 3 plus2 min setal processes, respectively. Basial endite bilobedwith 3 plus 2 min setal processes, respectively. However,the number of processes on basial and coxal endites is verydifficult to determine due their minute size. Endopodunsegmented not clearly lobuated, with a medial pricklyprojection plus 2 simple setae. Scaphognathite with 10 plus3 marginal plumose setae.

First Maxilliped (Fig. 6G). Coxa and basis glabrous.Endopod 4-segmented with reduced setal processes on firstto third segment, and 2 simple distal setae on third andfourth segments. Exopod unsegmented, with 4 longterminal plumose natatory setae. Epipodal bud present.

Second Maxilliped (Fig. 6H). Coxa and basis naked.Endopod unsegmented and glabrous. Exopod unsegmented,with 4 long terminal plumose setae.

Third Maxilliped (Fig. 6I). Rudimentary, unsegmentedand lacking setae, with differentiated endopod, exopod andepipod.

Pereiopods. (Figs 6J-N) The five pereiopods are devel-oped but not functional. They are unsegmented andwithout setae. First pair bilobed (cheliform). There areno exopods.

Pleon (Fig. 6O). Six abdominal somites. First somitewith 7 dorsal simple setae. Somites II to V with a pair ofsmall dorsal setae. A pair of small dorsal-lateral knobs isobserved on the second segment. Pleopod buds on somitesII to V.

Telson (Fig. 6O). Telson bifurcated, each furcal armlacking lateral or dorsal spines and with 3 or 4 serrulatespinous processes on posterior margin.

Zoea II (Fig. 7; Table 2).—Dimensions. CL: 1.82 60.05 mm.

Carapace. Similar morphology to that of stage I. Eyesstalked (Fig. 7A).

Antennule (Fig. 7B). Peduncle 3-segmented withoutsetation; basal segment bulbous. Endopod not present.Exopod consistst only of 1 segment with 1 long simple seta.

Antenna (Fig. 7C). Protopod unchanged. Endopod 4-segmented, exceeds two times the protopod length.Exopod half length of the endopod with 2 distal smallsimple setae.

Mandible. Similar in form to previous stage.Maxillule (Fig. 7D). Similar in form to previous stage.

Endopod 2-segmented but, glabrous.Maxilla (Fig. 7E). Coxal and basial endites similar in

form to previous stage, but with setal processes nowscarcely visible. Endopod unsegmented, without setae.Scaphognathite with 14 plumose marginal setae andnumerous protuberances on the posterior margin.

First Maxilliped (Fig. 7F). Coxa and basis unchanged.Endopod 4-segmented, but unarmed. Exopod 2-segmented,with 14 long terminal plumose natatory setae.

Second Maxilliped (Fig. 7G). Coxa and basis un-changed. Exopod 2-segmented, with 13-14 long terminalplumose setae.

Third Maxilliped (Fig. 7H). Unchanged.Pereiopods (Figs. 7I-M). Uniramous, 5-segmented, lack-

ing setae. Non-functional.Pleon (Figs. 7N, O). First somite with 7 dorsal setae.

Somites II to V with a pair of dorsal setae. Presence ofknobs on second segment variable. Five pairs of pleopodson somites II to VI as buds.

Telson (Figs 7N, O). Telson with 3 or 4 pairs of serrulatespinous processes on posterior margin, varying as the firststage.

First juvenile crab (Fig. 8).—Dimensions. CL: 1.87 60.06 mm; CW: 1.70 6 0.08 mm.

Carapace (Figs. 8A, B). Longer than broad and withoutspines. Frontal region glabrous, ending in a very shortrostrum bent downward. Tubercles and setation asshown.

Antennule (Fig. 8C). Peduncle 3-segmented with 0, 1,and 1 simple setae, respectively; basal segment bulbous.Endopod not present. Exopod as 2-segmented flagellumwith 1 seta plus 4 aesthetascs on distal segment.

Antenna (Fig. 8D). Peduncle 2-segmented, glabrous.Endopod slender, 6-segmented with 1, 0, 0, 0, 2, 1 seta,respectively. No exopod present.

Mandible (Fig. 8E). Full development bearing a hardplate-like structure with distal cutting edge. Mandibularpalp 2-segmented with 6 plumose setae on the distalsegment.

Maxillule (Fig. 8F). Protopod with 2 long plumose setaeplus 1 short simple seta on dorsal margin. Coxal enditefringed with 12 plumodenticulate setae. Basial endite with7 denticulate processes plus 10 setae. Endopod unsegment-ed with 2 simple setae distal end.

Maxilla (Fig. 8G). Coxal endite bilobed with 12 + 3plumose setae. Basial endite bilobed with 7 sparselyplumose setae on each lobe and 1 simple short setabetween both. Endopod unsegmented and glabrous. Sca-phognathite with 48 marginal plumose setae plus 2 plumosesetae on the inner side.

First maxilliped (Fig. 8H). Coxal endite with 1 simpleseta plus 10 sparsely plumose setae. Basial endite with 10sparsely plumose setae. Epipodite with triangular shapewith 2 sparsely plumose setae proximally plus 8 sparsely

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 111

plumose setae distally. Endopod unsegmented with 4sparsely plumose setae plus 1 plumose seta. Exopod 2-segmented, naked on proximal segment and bearing 4simple setae on distal segment.

Second maxilliped (Fig. 8I). Coxa and basis notdifferentiated and glabrous. Endopod 4-segmented with 2+ 1 plumose setae, 1 plumose seta, 5 sparsely plumosesetae, and 6 sparsely plumose setae plus 5 plumodenticulatesetae, respectively. Exopod 2-segmented with 0 and 4 veryshort simple setae, respectively.

Third maxilliped (Fig. 8J). Fully developed. Basis with18-20 plumose setae. Long epipodite with 7 plumose setaeplus 24-26 sparsely plumose setae, located as shown.Endopod 5-segmented with 18-20, 7 + 2, 2 + 5, 4 and 6sparsely plumose setae. Exopod 2-segmented, with 4 shortplumose setae on outer margin of the proximal segment,and 4 long plumose setae on distal one.

Pereiopods. Fully developed with all segments welldifferentiated.

Pleon (Figs 8K, L). 6-segmented and not totally folded.First somite with a row of 11-12 simple setae; theremaining somites with setation as shown.

Pleopods. Biramous buds very small, as previous stage insize, non-functional.

Telson (Fig. 8K). Subquadrate, broader than long,smooth, with posterior margin concave and glabrous.

Second juvenile crab (Fig. 9).—Dimensions. CL: 2.20 60.07 mm; CW: 2.00 6 0.06 mm.

Carapace (Fig. 9A). Longer than broad, flattened.Frontal region broad, measuring one half of carapacewidth, bearing a row of small setae on the anterior margin.Cephalothorax margin without spinous processes or setae.

Maxillule and maxilla. Similar form and setation asprevious instar.

First and second pereiopodos. Similar form and setationas previous instar, except exopods now showing 4 longsimple setae.

Fig. 5. Sesarma windsor (First crab): A, dorsal view; B, third maxilliped; C, pleon and telson. Scale bars: A 5 1 mm; B-C 5 500 mm.

112 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 30, NO. 1, 2010

Fig. 6. Metopaulias depressus (Zoea I): A, frontal view; B, lateral view; C, antennule; D, antenna; E, maxillule; F, maxilla; G, first maxilliped; H, secondmaxilliped; I, third maxilliped; J-N, first to fifth pereiopod; O, pleon and telson. Scale bars: A-B 5 1 mm; C-F 5 100 mm; G, H, O 5 250 mm; I-N 5200 mm.

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 113

Fig. 7. Metopaulias depressus (Zoea II): A, rostrum and eyes; B, antennule; C, antenna; D, maxillule; E, maxilla; F, first maxilliped; G, secondmaxilliped; H, third maxilliped; I-M, first to fifth pereiopod; N, O, pleon and telson. Scale bars: A, N, O 5 500 mm; B-E 5 100 mm; F-M 5 250 mm.

114 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 30, NO. 1, 2010

Fig. 8. Metopaulias depressus (First juvenile): A, dorsal view; B, lateral view; C, antennule; D, antenna; E, mandible; F, maxillule; G, maxilla; H, firstmaxilliped; I, second maxilliped; J, third maxilliped; K, pleon and telson. Scale bars: A, J, K 5 500 mm; B 5 1 mm; C-G 5 100 mm; H, I, L 5 200 mm.

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 115

Third maxilliped (Fig. 9B). Similar form as previousstage.

Pleon (Fig. 9C). Six somites present with setation asshown.

Pleopods. Very small buds on somites II to V.Telson (Fig. 9C). Triangular shape with setation as

shown.

DISCUSSION

After Hartnoll’s (1964) preliminary account, the presentstudy provides the first complete and detailed morpholog-ical description of larval morphology for any of theendemic Jamaican species of freshwater-breeding sesarmidcrabs. Both S. windsor and M. depressus show anabbreviated mode of larval development (the former withonly two non-feeding zoeal stages and a megalopa; thelatter with only two zoeal instars), whereas the coastalmarine or estuarine congeneric species S. reticulatum and S.rectum follow the apparently typical generic pattern withthree planktotrophic zoeal stages (Costlow and Bookhout,1962; Fransozo and Hebling, 1986).

The zoeal stages of S. windsor and M. depressus showsimilar morphological characteristics. Nevertheless, in S.windsor, the zoea II is followed by a typical brachyuranmegalopal stage with functional pleopods and an unfoldedpleon, while in M. depressus the zoea II moults to an instarwith a partially bent pleon underneath the carapace and withscarcely developed (rudimentary) and non-functional pleo-pods (in fact, laboratory observations confirm that this stagedoes not swim). Nevertheless, it displays other characterstypically found in megalopae such as a quadrangular telson.The distinctive features of functional morphology in themegalopal stage have been reviewed in several occasions(Gurney, 1942; Williamson, 1982; Anger, 2001; 2006), andit is generally accepted that the megalopal stage of theBrachyura is morphologically characterised by the presenceof functional (natatory) pleopods. Later in ontogeny, theseappendages will be functional again only after several post-larval moults and then their function will be reproductive(copulation, attachment of eggs) instead of locomotory. Bycontrast, the majority of juveniles of Brachyura, andsesarmids in particular, do not display functional larvalorgans, such as natatory pleopods, although they mightpresent it as vestigial appendages. In early juveniles thetelson morphology is also distinct from the megalopa,changing from a quadrangular shape to a triangular one.There are evidences that in many decapod and euphausiidspecies the transition from megalopa (or decapodite) tojuvenile is gradual: many of the larval features displayed bythe megalopae are not completely absent in the earliestjuvenile instars (for example, the exopods of pereiopods inCaridea or the pleopods in Brachyura). Nevertheless, thesecharacters lose their functionality and may graduallydisappear during the first moults of the juvenile. This hasbeen observed in Euphausiacea, Penaeoidea and Sergestoi-dea (see Williamson, 1982), some Pinnotheridae (seeHyman, 1924) and also S. windsor (present study) and S.dolphinum Reimer, Schubart and Diesel, 1998 (unpublisheddata), whose megalopae exhibit well-developed natatoryT

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116 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 30, NO. 1, 2010

pleopods while in the first juvenile instar these appendagesare only vestigial. Thus, the occurrence of such non-functional larval characters in more advanced ontogenicstages should be interpreted as a reminiscence of theprevious stage.

Accordingly, the development stage that follows the zoeaII in M. depressus should not be considered as a megalopa(and thus a larva), but instead it should be viewed as apostlarval stage showing some persisting but non-function-al larval features. The development of M. depressus is thusreduced to just two zoeal instars and lacks a megalopalstage. It should be noted here that the so-called megalopastage in previous studies on larval biology of this species(Hartnoll, 1964; Anger and Schuh, 1992; Diesel and Schuh,1993; Anger and Schubart, 2005) was, according to ourpresent morphological insight, actually the first juvenile,and the so-called first juvenile in these previous studies isnow considered the second juvenile instar. In addition totheir morphological traits, the two first juvenile instars alsodiffer in their feeding mode, the first juvenile beingfacultatively lecithotrophic, whereas the second juvenile is

fully dependent on exogenous food sources (Anger andSchuh, 1992; Anger and Schubart, 2005).

An absence of the megalopal stage in the larvaldevelopment of brachyurans has already been reported forsome pinnotherid species (Hyman, 1924), and is a distinctivecharacter, for Hymenosomatidae (Lucas, 1971; Wear andFielder, 1985). Nevertheless, the suppression of the megalopalstage has not been recorded yet for the ontogeneticdevelopment of sesarmid crabs. However, there are certainmorphological similarities between the last larval stagedescribed by Soh (1969) as ‘‘larval stage 3’’ for the freshwatercrab Geosesarma perracae Nobili, 1903 and the earliestjuvenile stage of M. depressus. Observations suggest thatSoh’s ‘‘larval stage 3’’ should not be considered a larval stageeither, but an earlier juvenile stage homologous to the onefound in M. depressus. Consequently, Sesarmidae should nowbe included in the small group of brachyuran crabs that mayomit the megalopal stage in their development. In order tocheck for the absence of megalopal stages in other species ofJamaican endemic freshwater sesarmids and to better establishphylogenetic relationships among these, further studies are

Fig. 9. Metopaulias depressus (Second juvenile): A, dorsal view; B, third maxilliped; C, pleon and telson. Scale bars: A 5 1 mm; B 5 200 mm; C 5500 mm.

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 117

needed to deepen our knowledge about morphologicalchanges taking place during the larval development of thisbrachyuran group. Unpublished observations by Schubartsuggest that the Jamaican snail-shell crab Sesarma jarvisiRathbun, 1914 also develops without a megalopa stage.

Consistent with patterns of abbreviated development inother decapod taxa (for review, see Rabalais and Gore,1985; Clark, 2000; Anger, 2001; 2005), and similar to otherendemic Jamaican sesarmids (S. fossarum Reimer, Schu-bart and Diesel, 1998, S. meridies Schubart and Koller,2005, 1998; see Anger, 2005; Anger et al., 2007), both S.windsor and M. depressus produce much larger eggs thanclosely related species with an extended mode of larvaldevelopment (cf. Seiple and Salmon, 1987; Anger, 1995).Correspondingly, also the larvae of S. windsor and M.depressus are conspicuously larger at hatching than those ofS. reticulatum and S. rectum (1.87 and 1.74 vs. 0.48 and0.71 mm, respectively).

The estuarine mangrove-dwelling species S. curacaoenseDe Mann, 1892 also shows an abbreviated larval develop-ment with only two zoeal stages (Anger et al., 1995;Schubart and Cuesta, 1998). While the size of its eggs(0.60 mm) and newly hatched larvae (cl: 0.74-0.81 mm) isclearly smaller than in the endemic freshwater-breedingforms, it is only slightly larger than in the coastal estuarinespecies S. rectum and S. reticulatum, which pass throughthree zoeal stages (present study; cf. Anger et al., 1995;Schubart and Cuesta, 1998). Hence, the size of eggs andlarvae increases in a sequence S. reticulatum , S. rectum ,S. curacaoense % M. depressus , S. windsor.

This pattern corresponds to the tendency towardsincreasing reproductive independence from the ancestralenvironment, the sea, reflecting differential degrees ofevolutionary transition from marine to brackish, and,possibly independently, to limnic conditions (Schubartand Diesel, 1999; Diesel et al., 2000). This sequence is alsoconsistent with increasing larval lecithotrophy, i.e., utili-zation of enhanced maternal energy reserves stored in theegg yolk (Staton and Sulkin, 1991; Anger, 1995; 2001;Anger and Schubart, 2005). A lecithotrophic reproductivestrategy allows for a reduced dependence on planktonicfood sources, which may be rare or unpredictable in somenon-marine environments (Anger, 2001). Internal reservesare utilized not only as a fuel for larval energy metabolism,but also as raw material for ‘‘developmental reconstructionprocesses’’ and the ontogenetic expression of new struc-tures. As a consequence of endotrophy, larval growth tendsto decrease with increasing lecithotrophic potential (Anger,1995; Anger and Moreira, 2002; 2004). While size andbiomass of planktotrophic marine brachyuran larvae canmultiply during development from hatching to metamor-phosis (see e.g., Harms, 1990; review in Anger, 2001), thesuccessive larval stages of S. windsor and M. depressuschange only little in body size (present study) and losesubstantial amounts of weight and organic matter (Angerand Schubart, 2005; Anger, 2005; Anger et al., 2007).

The abbreviation of the larval phase in S. windsor and M.depressus is closely associated with pre-displacement(earlier onset) or acceleration (faster developmental rate)in the expression of some character states, but also with a

reduction in others (for terminology of heterochronicdevelopmental processes, see Clark, 2000; Clark et al.,2005). In these species, newly hatched zoea-I larvae show aconspicuous pre-displacement in the expression of theantennal endopod, the third maxilliped, the pereiopods, andthe pleopods. The same patterns of overdevelopment athatching were observed in other sesarmid species with anabbreviated development, namely S. dolphinum Reimer,Schubart and Diesel, 1998 (unpublished data), S. bidenta-tum (see Hartnoll, 1964) and G. perracae (see Soh, 1969).In the more marine S. reticulatum and S. rectum, incontrast, these appendages are expressed only after themoult to the second zoeal stage, which is typical for thevast majority of brachyuran crabs with an extended modeof larval development (Ingle, 1982; Clark, 2000; Clark etal., 2005).

In spite of these similarities, however, not all patterns ofheterochrony are congruent in species with an abbreviatedtype of development. For instance, the larvae of S.curacaoense hatch with sessile eyes, like those of S.reticulatum and S. rectum, and stalked eyes appear only inthe second zoeal stage. The endemic Jamaican sesarmids,by contrast, hatch already with stalked eyes. Similarly,newly hatched larvae of S. curacaoense, S. reticulatum andS. rectum have only 5 abdominal somites, while the 6thsomite is expressed only at the moult to the second zoealstage. The larvae of S. windsor, M. depressus, S.bidentatum, S. dolphinum, and G. perracae, in comparison,show a pre-displacement of this character state, hatchingwith the complete set of 6 abdominal somites (presentstudy; cf. Hartnoll, 1964; Soh, 1969). Moreover, sesarmidspresenting an abbreviated development (except S. cura-caoense) hatch with a longer antennal endopod than theprotopod, and with appreciable endopod segmentation fromthe second zoeal stage on. Such features have never beenobserved in zoeal stages of sesarmids with an extended(regular) development. Also in the abbreviated develop-ment of S. curacaoense the segmentation of the endopodonly occurs at the megalopal stage. Lack of pre-displacement in S. cuaracaoense as compared to otherspecies with an abbreviated mode of development was alsoobserved in the zoeal scaphognathite setation and in thedevelopment of epipod buds on the first maxilliped(Tables 1, 2; cf. Hartnoll, 1964; Soh, 1969; Anger et al.,1995).

Besides pre-displacements of some character states,abbreviated developments also imply various morpholog-ical reductions. This includes another interesting differencebetween the larvae of S. curacaoense and those of all otherknown sesarmid crabs with an abbreviated mode ofdevelopment: in the zoeal stages of S. windsor, M.depressus, S. bidentatum, S. dolphinum, and G. perracae,a dorsal spine is completely absent, and the rostral spine isreduced. Also in a species of fiddler crab which breeds inephemeral rainfall puddles, Uca subcylindrica (Stimpson,1859) (Ocypodidae), larval development is abbreviated(with only 2 zoeal stages, vs. 5 in most other species ofUca), and the zoeal carapace spines are rudimentary(Rabalais and Cameron, 1983). In comparison, the zoeaeof most estuarine and coastal marine crabs, including S.

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curacaoense, S. reticulatum, S. rectum, and almost allspecies of Uca, show well-developed dorsal and rostralspines. This recurrent and obviously convergent reductionof zoeal carapace spines in various species with anabbreviated mode of larval development may be explainedby differential selection pressures occurring in the marineplankton vs. non-marine breeding habitats. Experimentalstudies provide evidence that long carapace spines have anadaptive value in the plankton, reducing the otherwisestrong predation pressure by small pelagic fishes andcarnivorous invertebrates (Morgan, 1990; Morgan, 1992,and earlier papers cited therein). In the larvae of S.curacaoense, which probably develop in shallow coastalmangrove swamps (Schuh and Diesel, 1995), the carapacespines may thus reduce mortality by predation. In theendemic freshwater-breeding sesarmids on Jamaica, bycontrast, the evolutionary transition from coastal to land-locked limnic breeding habitats may have rendered thismorphological adaptation obsolete. As far as their repro-ductive behaviour is known, their larval developmentseems to take place in isolated and hidden micro-habitatssuch as water-filled bromeliad leaf axils (M. depressus; seeDiesel, 1997), empty snail shells (S. jarvisi; see Diesel andHorst, 1995), deep burrows dug in river banks (S. fossarum;see Anger, 2005), or shallow vegetated puddles near rivers(S. meridies; for recent discussion see Anger et al., 2007).Moreover, female brood-care behaviour, at least in somespecies, may have further reduced the selective role ofpredation (Diesel, 1992).

The abbreviated mode of development is typicallyassociated with further morphological reductions, inparticular in the segmentation and/or setation of variousappendages including the antennules, the antennae, mandi-bles, maxillae, and the endopods of first and secondmaxillipeds (Clark et al., 2005 for Carpiliidae; Bolanos etal., 2004 for Pinnotheridae; Taishaku and Konishi, 2001 forMajidae). Furthermore, the strict lecithotrophic conditionof the zoeal stages is associated with an occurrence of non-functional mouthparts, and probably a progressive degen-eration of the setal ornamentation involved in foodmanipulation. S. windsor, M. depressus, S. bidentatum, S.dolphinum, and G. perracae show such a conspicuous setalreduction on the coxal and basial endites of the maxillulesand maxillae, so that the setae are only discernible asincipient setal processes, almost imperceptible in manycases, causing a lack of functionality of the mouthparts, i.e.,a post-displacement event sensu Clark (2005). This lack offunctionality is also observed in other decapods with alecithotrophic mode of development (see McLaughlin etal., 2001; 2003 for anomuran species). Nevertheless, it isremarkable that the setal reduction is limited to the coxaland basial endites (involved in feeding), and that no suchreduction is observed in the setae of the scaphognathites,which have a respiratory function. In fact, the characteristicnumber of setae on the scaphognathites in the first zoealstage of brachyurans is 4 (10 in Majidae), while specieswith some degree of lecithotrophy usually bear more than10 setae (Taishaku and Konishi, 2001; Clark et al., 2005;present study). This represents again a pre-displacement,this time in the development of the scaphognathite. The

typical setation pattern of these appendages is onlyobservable when zoeae moult to the megalopal stage,coinciding with first feeding. In the case of S. curacaoense,where the lecithotrophic condition of the zoeae isfacultative, no setal reduction is observed on the coxaland basial endites of the maxillules and maxillae, allowingto process food, when prey is available. These observationssuggest a strong relationship between the morphologicalfeatures of mouthparts and the degree of lecithotrophyduring larval development.

Mitochondrial DNA reconstructions of phylogenetic rela-tionships among all American representatives of the generaSesarma and Metopaulias allowed to determine that allJamaican endemic species are monophyletic and a sister cladeto a second one consisting of Sesarma reticulatum, Sesarmasp. (nr. reticulatum), S. curacaoense (all from the westernAtlantic) and Sesarma rhizophorae Rathbun, 1906 (from theeastern Pacific) (Schubart et al., 1998). Thus phylogeneticdistances and time of separation should not differ between theJamaicans and S. reticulatum on one hand and the Jamaicansand S. curacaoense on the other. This allows two possibleinterpretations: either the ancestor of these two clades alreadyhad an abbreviated development with two zoeal stages, whichwas extended secondarily in S. reticulatum, or the abbrevi-ation took place convergently in S. curacaoense and theancestor of the Jamaican endemics. The first scenario of asecondary extension of larval development does not appearvery likely. This is supported by the fact that larvaldevelopment of Sesarma sp. (nr. reticulatum) from the Gulfof Mexico follows the same ontogenetic pattern as S.reticulatum, despite the fact of being genetically intermediatebetween S. reticulatum and S. curacaoense (Schubart andFelder, unpublished). Also the morphology of the first stage ofS. rhizophorae from the Pacific coast of Panama does notshow any morphological reductions compared to S. reticula-tum and thus no indication of an abbreviated larvaldevelopment with less than three zoeal stages (Schubart andCuesta, 1998). The interpretation of morphological changesresulting from abbreviated development in S. curacaoense onone hand and the Jamaican endemic species on the other,should thus be treated as two independent evolutionaryprocesses with a similar, but not identical morphological andecological outcome.

The phylogenetic reconstruction of Schubart et al. (1998)failed to clearly resolve evolutionary lineages withinJamaica. There seems to be an east-west subdivision ofspecies, but sister species relationships are not satisfactorilysolved. One outcome, however, is the insight that the sixcurrently described species from mountain streams do notform a monophyletic unit, despite strong morphologicalsimilarities. At most, three clades of these river species canbe determined with S. dolphinum and S. fossarum (weaklysupported sister species) from the west of the island, S.windsor and S. meridies (strong support for sister speciesrelationship) from the central part, and S. bidentatum and S.ayatum Reimer, Schubart and Diesel, 1998 (strong supportfor sister species relationship) from the eastern part of theisland (Schubart et al., 1998; Schubart and Koller, 2005;Schubart, unpublished). The more terrestrial and special-ized forms have evolved posteriorly from these regional

GONZALEZ-GORDILLO ET AL.: SESARMID EARLY DEVELOPMENT 119

clades of river forms, e.g., the eastern S. cookei from theclade of S. bidentatum and S. ayatum (Schubart et al.,1998). The bromeliad crab M. depressus and the cave crabSesarma verleyi Rathbun, 1914 occur in the western andcentral part of Jamaica. Accordingly, they are probablyderived from ancestral river crabs from that part of theisland (Schubart et al., 1998: Fig.1). Therefore, morpho-logical similarity between the here described larvae of S.windsor and M. depressus is not surprising, despite theclear cut morphological and ecological differences of theadults. Most ontogenetic changes reflected in larvalmorphology and ecology probably took place before thecolonization of bromeliads and speciation by M. depressus.Nevertheless, it can be expected that subsequent adapta-tions to conditions in bromeliad leaf axils took place on aphysiological level and should be studied in detail.

ACKNOWLEDGEMENTS

KA is grateful to the staff of the Discovery Bay Marine Laboratory (St.Ann, Jamaica) for kind hospitality and support, Uwe Nettelmann fortechnical assistance in the laboratory, and Gabriela Torres, Luis Gimenez,and Karin Boos for occasional help in the long-term maintenance ofJamaican crabs on Helgoland. Sampling activities in Jamaica were partlyfunded by the Deutsche Forschungsgemeinschaft (project 1460/3 to CS).The participation of Tobias Santl and Tobias Weil from the University ofRegensburg during field work in 2003 is acknowledged. JIG-G wassupported by the Ramon y Cajal Research Program from Spanish Scienceand Technology Ministry and FEDER.

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