Chastity Belts and Planktotrophic Larvae: Constraints on Gecarcinid Reproductive Behaviour

CHASTITY BELTS AND PLANKTOTROPHIC LARVAE: CONSTRAINTS ON GECARCINID REPRODUCTIVE BEHAVIOUR

RICHARD G. HARTNOLL1,2) 1) School of Biological Sciences, University of Liverpool and the Marine Biological Association of the U.K., Plymouth

ABSTRACT

Land crabs of the family Gecarcinidae all have planktotrophic larval development in the sea, with ﬁve or six zoeae and one megalopa. This imposes two constraints on the crabs. Firstly, females must migrate to the sea, sometimes over considerable distances, to release the larvae. This stresses them and limits reproductive investment and larval output. Secondly, at the end of their larval development the crabs must recolonize land, often onto small and remote islands. Limited larval output, and the vagaries of currents, climate and planktonic circulation, potentially restrict recruitment. In addition, female gecarcinids are available for mating only during the brief interval of decalciﬁcation of the genital operculum (the ‘chastity belt’). This may occur before, during, and/or after migration to the sea, depending on species. This diversity of mating opportunity constrains male migration patterns to optimize mating opportunity.

RÉSUMÉ

Les crabes terrestres de la famille des Gecarcinidae ont tous des développements larvaires en mer, comprenant cinq stades zoé et un stade mégalope. Cela impose deux contraintes aux crabes. Premièrement, les femelles doivent migrer vers la mer, souvent sur de longues distances, pour délivrer leurs larves. Cela les perturbe et limite leur investissement reproductif dans la production des larves. Deuxièmement, à la ﬁn du développement larvaire les crabes doivent regagner la terre, qui consiste souvent en petites îles éloignées. Une émission larvaire limitée et les aléas de la circulation planctonique limitent potentiellement le recrutement. Les femelles Gecarcinidae sont disponibles pour l’accouplement seulement pendant la brève période de décalciﬁcation de l’opercule génital (la « ceinture de chasteté »). Cela se produit, pendant, et/ou après la migration vers la mer, selon les espèces. Cette diversité d’opportunités d’accouplements contraint la stratégie de migration des mâles pour optimiser ces possibilités d’accouplement.

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INTRODUCTION

Crabs of the family Gecarcinidae are generally referred to as ‘land crabs’, but they are not the only land-living crabs, and in some respects not the best adapted to a terrestrial life. They are generally medium to large crabs of robust build, with six known genera and 21 recognized species worldwide (Ng & Guinot, 2001; Ng et al., 2008). A number of gecarcinid species exceed 100 mm carapace width (the little-studied genus Epigrapsus is rather smaller at <40 mm, see Liu & Jeng, 2005): Cardisoma guanhumi Latreille, 1828, is the largest, reaching 130 mm carapace width (Türkay, 1970). Adult gecarcinids show a variable degree of dependence on water. Gecarcinus, Gecarcoidea, and Johngarthia (and probably some Epigrapsus species) often live far from permanent water bodies (fig. 1A), and can be found a considerable distance inland and at substantial altitudes: in Jamaica, Gecarcinus ruricola (Linnaeus, 1758) reaches altitudes in excess of 1000 m (Britton et al., 1982). In contrast, Cardisoma and Discoplax, whilst sometimes living well away from the sea, are more dependent on water (see Hartnoll, 1988, for references). They either live close to permanent water, or inhabit burrows which penetrate to the water table. Nevertheless gecarcinids are all poorly adapted to desiccation stress in comparison to insects, and are predominantly active by night, or in humid conditions during and after rain. All gecarcinids concur in that their larval development shows no concession to a terrestrial life style. The larvae must hatch into the sea, where they pass through an extended series of planktotrophic stages before returning to land. This requirement imposes the first two constraints on reproductive behaviour: the necessity for the female to migrate to the sea for breeding and the need for the juvenile stages to recolonize the land. Gecarcinids are not alone in having this combination of adult terrestrial adaptation together with a lack of larval modification. The same pattern is seen in various hermit crabs: many Calcinus species, and the Coenobitidae, comprising Coenobita and the coconut or robber crab Birgus latro (Linnaeus, 1767). In the Grapsidae, Geograpsus crinipes (Dana, 1851) and G. grayi (H. Milne Edwards, 1853) are similar, as are a number of Sesarmidae species such as Armases ricordi (H. Milne Edwards, 1853), Chiromantes eulimene (De Man, 1895) and C. ortmanni (Crosnier, 1965). In the Ocypodidae, sev- eral species of Ocypode regularly burrow well above high tide, including O. africana (De Man, 1881), O. cordimanus Latreille, 1818, O. pallidula Jacquinot, 1846 and O. saratan (Forskål, 1775). However, none of the above species are as terrestrial as the better adapted gecarcinids. Further details of