CHAPTER 71-10

SYMBIOTIC BRACHYURA1)

BY

PETER CASTRO

Contents. – Introduction – The meaning of symbiosis – Categories of symbiosis. Cryptochi- roidea: Cryptochiridae – Hosts, biogeography, and ecology – Life history – Nutrition. Pilum- noidea: Pilumnidae – Hosts, biogeography, and ecology – Life history – Nutrition. Pinnotheroidea: Aphanodactylidae and Pinnotheridae – Hosts, biogeography, and ecology – Life history – Nutri- tion. Trapezioidea: Domeciidae – Hosts, biogeography, and ecology. Trapezioidea: Tetraliidae – Hosts, biogeography, and ecology – Life history – Nutrition. Trapezioidea: Trapeziidae –Hosts, biogeography, and ecology – Life history – Nutrition. Other Brachyura – Majoidea – Portunoidea – Xanthoidea – Other Xanthoidea – Miscellaneous groups of Brachyura. Acknowledgements. Ap- pendix. Bibliography.

INTRODUCTION Close heterospecific associations are ubiquitous in most if not all biotic communi- ties. These associations vary widely in character, and can include a wide range of mor- phological, ecological, physiological, and/or behavioural adaptations, at times the result of coevolution between the partners. Brachyuran crabs are common participants in such asso- ciations, e.g., as hosts for internal or external parasites (see Chapter 71-12 in this volume), in associations with other organisms for concealment (see Chapter 71-11 in this volume), and as close associates living on or within an invertebrate host (the symbiotic associations discussed in this chapter). The variety and range of complexity among these symbioses is remarkable and difficult to categorize. Brachyuran associates are often referred to as “commensals”, “parasites”, “mutualists”, or, as herein, simply as “symbionts”. The groups of symbiotic brachyurans discussed in this chapter are listed alphabetically by superfamilies, which follow the classification in Chapter 71-18 in this volume. Various

1) Manuscript concluded October 2014; final additions May 2015.

© Koninklijke Brill NV, Leiden, 2015 Crustacea 9C (71-10): 543-581 544 P. CASTRO aspects of the biology of the symbioses are discussed, with particular importance given to the more recent investigations.

The meaning of symbiosis

“Symbiosis” was first used by de Bary (1879) to denote the “living together of dissim- ilar organisms” [“Zusammenleben ungleichnamiger Organismen”], a broad category that for de Bary included associations traditionally known as “commensalism”, “mutualism”, and “parasitism”. Frank (1877) had first used the term “symbiotismus”[“... Zusammen- leben begründet ist, und wofür sich die Beziehung Symbiotismus empfehlen dürfte”] (see Seckbach & Grube, 2010), but it was de Bary’s concept of symbiosis, linked with his work on the mutualistic associations of autotrophs and fungi in lichens, that prevailed. “Sym- biosis” unfortunately remained for some as a synonym of mutualism, only one of several types of symbioses. There has been much confusion and ambiguity surrounding the use of “symbiosis”, even if the American Society of Parasitologists recommended its use as a general term comprising parasitism and other associations in the context of de Bary’s original definition (Hertig et al., 1937). There has been a trend toward abandoning the restrictive meaning of symbiosis as an equivalent of mutualism in favour of the original broader definition. “Symbiosis”, “mutualism”, and “commensalism” have also been used in an ecological context, together with terms such as “facilitation” and “positive interac- tions”, to refer to a broad range of intraspecific relationships that are beyond the concept of symbiosis as used herein (Boucher et al., 1982; Stachowicz, 2001; Bruno et al., 2003; Grutter & Irving, 2007). Symbiotic brachyurans are specialized in form and function to various degrees. Some are known as obligate symbionts because they always occur associated with particular groups of living hosts and are rarely found on non-living substrates or free living for ex- tended periods of time as non-larval stages. Hosts nevertheless remain unknown in some rare species. Six families of Brachyura (Aphanodactylidae, Cryptochiridae, Domeciidae, Pinnotheridae, Tetraliidae, Trapeziidae) consist exclusively, with rare exceptions, of obli- gate symbionts. Obligate symbionts are also found in at least four additional brachyuran families (Epialtidae, Pilumnidae, Portunidae, Varunidae). Other symbionts, known as fac- ultative symbionts and found in at least three families (Inachidae, Majidae, Xanthidae), lead a symbiotic existence because they tend to occur on particular living hosts but can also be found on non-living substrates. Facultative symbionts for the most part lack the morphological and functional adaptations of obligate symbionts.

Categories of symbioses

Symbioses can be regarded as a broad continuum of close heterospecific associations encompassing many types and degrees of interactions between the partners. The meaning and scope of symbiosis and its categories have been examined by numerous authors (Caullery, 1952; Dales, 1966; Cheng, 1967; Read, 1970; Smith & Douglas, 1987; Castro, 1988; Saffo, 1992, 2002; Sapp, 1994; Paracer & Ahmadjian, 2000; Grutter & Irving, 2007;