Symbiosis https://doi.org/10.1007/s13199-018-0566-z

Host selection and host switching in Gymnolophus obscura – a symbiotic ophiuroid associated with feather stars (Crinoidea: )

E. S. Mekhova1 & A. V. Martynov2 & T. A. Britayev1

Received: 8 August 2016 /Accepted: 27 June 2018 # Springer Nature B.V. 2018

Abstract The present paper aims to assess the host-selectivity and host-switching behaviour of the comatulid associated ophiuroid Gymnolohpus obscura. The relationships between size-structure, distribution and infestation characteristics of G. obscura were assessed among all available feather star species in the Bay of Nhatrang, Vietnam, together with the frequency of injuries among symbiont size classes. Our data show that despite the fairly wide host distribution ranges, not all of them are equally infested by G. obscura, likely because of host morphology, size and location on the substrate. The most preferred hosts were the comatulids Comaster nobilis and Comanthus parvicirrus, which were preferably infested by larger symbionts. The highest frequency of injuries was found in symbionts with disks ranging from 0.6 to1 cm in diameter, tracing a host-to-host migration behaviour leading to a sharp fall in abundance in the 1.1–1.5 cm size class. Our results suggest that host-switching (either between the same or among different host species) is a characteristic behaviour of G. obscura, driven by either intraspecific competition and/or by searching for more favourable trophic or protective conditions.

Keywords Symbiosis . Host specify . South China Sea . Crinobionts . Intraspecific interactions

1 Introduction to improve protection have also been suggested (Mekhova et al. 2015). In contrast, hosts-switching has been reported for just a Migration of post-settled juvenile or adult symbiotic few symbionts. Among them, the polychaete Arctonoe vittata from one host individual to another is a rather common phenom- Grube (Britayev and Smurov 1985; Britayev 1991;Tokajietal. enon in the marine ecosystems, particularly in decapods (e.g., 2014), and the crabs Allopetrolisthes spinifrons (Baeza and Stotz Baeza et al. 2001;Bell1984;Castro1978; Thiel et al. 2001)andDissodactylus primitivus (De Bruyn et al. 2010, 2003; Dgebuadze et al. 2012; Wirtz and Diesel 1983; 2011). In these cases, host switching leads to optimal host ex- Yanagisawa and Hamaishi 1986). Mating strategies have been ploitation and appears to be correlated with ontogeny. proposed as a main factor explaining host-to-host migration Intraspecific competition and mating behavior seem to explain (Baeza and Thiel 2007). However, other factors like food limi- symbiont host switching (Britayev 1991; De Bruyn et al. 2010). tation (related to symbiont growth), foraging for food outside the Despite such a behaviour having not yet been documented in host, intra- or interspecific competition, and finding of new hosts symbiotic , the juveniles of the ophiuroid Ophiomastix venosa Peters 1851 are known to change their residence. This species lives in association with another brittle * E. S. Mekhova star, Ophiocoma scolopendrina (Lamarck 1816), but becomes [email protected] free-living when adult (Fourgon et al. 2007). Symbiotic associations involving echinoderms are very A. V. Martynov common in the marine environment. However, in most cases, [email protected] they act as hosts harboring small, specialized symbionts (e.g., 1 A.N. Severtsov Institute of Ecology and Evolution RAS, Leninsky Barel and Kramers 1977; Coppard and Campbell 2004; Prospect 33, 119071 Moscow, Russia Jangoux 1987a, b; Lyskin and Britaev 2005; Deheyn et al. 2 Zoological Museum Moscow State University, Bolshaya Nikitskaya 2006). In contrast, a symbiotic mode of life is rather rare Str. 6, 125009 Moscow, Russia among echinoderms, except the Ophiuroidea, which are well Mekhova E.S. et al. known as associates of different invertebrates, i.e. sponges, against predation (Tinkova et al. 2014;Kasumyanetal. corals, and other echinoderms, including unstalked 2014). Therefore, it is likely that G. obscura gains protection or feather stars (e.g., Hendler 1984; Hendler et al. 1999; when attached to a host, and, like other migrating symbionts, Grange 1991; Mekhova and Britayev 2012;Mosherand becomes more vulnerable when moving from host-to-host Watling 2009; Ohtsuka et al. 2010; Stohr et al. 2012). (e.g. Castro 1978). Therefore, we hypothesize that the fre- At least 15 species of ophiuroids are known to live in asso- quency of traumas in the symbionts will increase during their ciation with feather stars (Clark 1921), with Ophiomaza host-to-host migration, with the highest occurring among cacaotica Lyman, 1871 and Gymnolophus obscura those symbionts that have recently migrated. (Ljungman, 1867) being the most common. G. obscura is an The present paper aims to assess the host-selectivity and obligatory symbiont inhabiting a wide variety of shallow water host-switching behaviour of the comatulid-associated ophiuroid feather stars in the tropical Indo-West Pacific (Price and Rowe G. obscura, based on a population of the symbiont and its 1996; Morton and Mladenov 1992;James1995; Huang et al. potential host feather star from the Bay of Nhatrang, Vietnam. 2005; Nigam and Raghunathan 2016). This species seems able Additionally, we studied the infestation characteristics among to infest any host species which is large enough to provide room the preferred hosts, as well as the relationships between their for the symbiont (James 1995). However, our preliminary data symbionts' size structure and the frequency of traumas. suggest that G. obscura has both preferred and avoided host species (Mekhova and Britayev 2012). G. obscura is able to migrate between individuals of its 2 Materials and methods host feather star Himerometra robustipinna (Carpenter, 1881) (Dgebuadze et al. 2012; Mekhova et al. 2015). Feather stars and their symbionts were hand-collected by However, only small symbionts are involved in this process SCUBA diving between 2006 and 2015 in the Bay of (Mekhova and Britayev unpublished observation). Moreover, Nhatrang, Central Vietnam, South China Sea (Fig. 1), with it seems likely that both small and large specimens may in- assistance from the Coastal Branch of the Russian- habit different feather star species. Feather stars have a com- Vietnamese Tropical Centre. Sampling was performed at plex morphology as well as mechanisms to be protected depths of 2–35 m. Feather stars were gently pulled

Fig. 1 Map of study area Host selection and host switching in Gymnolophus obscura – a symbiotic ophiuroid associated with feather... away from the substrate, immediately placed in individ- 3 Results ual zip-lock plastic bags, and transported to the labora- tory. 247 feather star specimens from 31 species were Host selectivity 16 of the 31 feather star species found in the used to assess the symbionts' host selectivity. Bay of Nhatrang harboured specimens of G. obscura In the laboratory, symbionts were gently removed, (Mekhova and Britayev 2012). Among them, Anessia bennetti preserved in 70% alcohol and counted. Prevalence (ratio (Müller, 1841) and Cenometra bella (Hartlaub, 1890) were between infested and total host number) and mean in- avoided to varying degrees; H. robustipinna and S. indica, tensity (mean number of symbionts per infested host in were indifferent; and C. parvicirrus and C. nobilis were pre- a sample) for the six most numerous (10–36 individ- ferred (Table 1). uals) host species in our samples were calculated (Table 1). Infestation characteristics The overall prevalence was 23.7%, Host selectivity was estimated by the Ivlev’s electivity ranging from 6.0% in A. bennetti to 57% in C. nobilis (Table index (Ivlev 1955)asE=(ri -pi)/(ri +pi), where E (i) – is 1). The overall mean intensity was 1.45 symbionts per host, the value for the host species i, ri is the frequency of indi- being 1.0 for S. indica, C. parvicirrus, C. nobilis, C. bella and viduals of the i-th feather star species among all infested, A. bennetti,and2.5forH. robustipinna. The maximum num- pi – the share of host species i in the samples. The index ber of symbionts living on a single specimen of H. ranges from -1 (absolute avoidance) to 1 (absolute prior- robustipinna was five. ity), with index values close to 0 indicating neither avoid- ance, nor preference. This index was developed to assess Location on hosts The symbionts commonly occupy the feeding selectivity in fish, but can be used as a first ap- host’s cup, firmly attaching themselves with their arms proach to test selectivity in other situations (Loehle and and the mouth close to that of the host (Fig. 3). We did Rittenhouse 1982; Lechowicz 1982). The index was cal- not recognize any obvious host damage induced by the culated for the six host species represented by more than symbionts, although the visceral masses of infested hosts ten specimens. were sometimes more lightly coloured than those in non- The size structure of G. obscura was estimated from 70 infested ones. In the case of multiple infestation by small additional specimens collected from Himerometra ophiuroids, they were located at the bases of the host's robustipinna (Carpenter, 1881), Stephanometra indica arms. (Smith, 1876), Comanthus parvicirrus (Müller, 1841) and Comaster nobilis (Carpenter, 1884). Size was estimated as Symbiont size structure The analysed ophiuroids showed the disk diameter, measured with a ruler to the nearest 1.0 sizes ranging from 0.1 to 2.4 cm in disc diameter, showing a mm. All measured specimens were examined carefully to de- great variability and differing significantly among hosts, ex- tect possible traumas. Only the traumas with evidence of re- cept between H. robustipinna and S. indica (ANOVA, F (3.66) generation were counted in order to distinguish those present = 41.9, p = 0.0001, Table 2). in living symbionts from those caused by symbiont sampling Symbionts were divided into five size classes (Fig. 4). and handling (Fig. 2). Small specimens (0.1–1.0 cm) predominantly inhabited H. The differences in symbiont size among hosts were robustipinna and S. indica, but occurred on all hosts, whereas assessed by analysis of covariance (ANCOVA) and post hoc large individuals (1.6–2.5 cm) were exclusively associated Tukey test, using the program Statistica 6.0 (StatSoft) with C. parvicirrus and C. nobilis (Fig. 4).

Table 1 Parameters of host infestation by ophiuroids in the Host species Sample size Mean Prevalence r(i) p(i) Ivlev (specimens) intensity % index Nhatrang Bay, ri - frequency of individuals of the i-th species of (individual value feather stars among all hosts per host) infested by the symbiont, pi – share of the same species of Comaster nobilis 21 1 57 0.277 0.097 0.499 feather stars in the samples Comanthus parvicirrus 21 1 33 0.149 0.089 0.271 Himerometra robustipinna 36 2.4 17 0.128 0.146 -0.068 Stephanometra indica 10 1 20 0.043 0.040 0.023 Cenometra bella 26 1 12 0.085 0.117 -0.247 Annessia bennetti 17 1 6 0.021 0.073 -0.529 Mekhova E.S. et al.

Fig. 2 Injuries of G. obscura: a – old trauma of disk, b – trauma of disk and two arms, c, d, e – different traumas of arms, f – specimen without trauma

Traumatism of symbionts The frequency of traumatized ani- species, being highest in S. indica symbionts. The frequency of mals was 30.0% (21 individuals from 70). Arm traumas were traumas was the highest (57%) in the second size class (0.6 - 1.0 dominant (82%), whereas those on disks were found only in 39% cm), while in other size classes, it never exceeded 25% (Fig. 5). of the traumatized individuals, while only 22% showed traumas on both the arm and disc (Fig. 2). The frequency of traumas slightly varied (20-30%) among individuals from different host 4 Discussion

Our data on the infestation of feather stars by G. obscura in the Bay of Nhatrang show that, despite a fairly wide host range, not all species are equally exploited. This led us to assess the reasons for this local host selectivity. One may expect higher infestations among the most abundant and widely distributed hosts while our data reveal some of them being clearly avoided (i.e., C. bella or A. benneti). The other possible reason for the hosts’ preference is their morphology. The most preferred hosts, C. nobilis and C. parvicirrus, like other species of Comtulidae, have thin and flexible oral pinnules and a relatively large oral surface of the cup. One may expect that closely related species with a similar morphology should be also selected by symbionts (Poulin Fig. 3 Location G. obscura on the host C. nobilis 2005). However, the other studied comatulid A. benneti was Host selection and host switching in Gymnolophus obscura – a symbiotic ophiuroid associated with feather...

Table 2 Post-hoc test Tukey values for pair considered mean Host Comanthus Comaster Himerometra Stephanometra size of G. obscura from different parvicirrus nobilis robustipinna indica host species Comanthus 0.017882* 0.000152* 0.000181* parvicirrus Comaster nobilis 0.017882* 0.000152* 0.000152* Himerometra 0.000152* 0.000152* 0.923929 robustipinna Stephanometra indica 0.000181* 0.000152* 0.923929

*mark statistically significant differences in pars (p≤ 0.05) not attractive. We must note that this species is clearly smaller harboured all the largest symbionts, while small ones were rare than the other two comatulids (the mean arm number of A. on these hosts (Fig. 4). On the other hand, the smaller symbionts bennetti is 70 as opposed to 110 in C. nobilis and 90 in C. infested mainly H. robustipinna and S. indica, which cannot be parvicirrus) (Mekhova and Britayev 2012). Therefore, we infested by large brittle stars due to their size and peculiar mor- suggest that, in these cases, the other factors, namely host size phology (Fig. 4). This host-use pattern allows small symbionts and location may be crucial for their availability as hosts. to avoid competition with larger ones, but can also be the result The other two infested hosts, H. robustipinna and S. indica, of this competition, with the small symbionts being expelled by differ from comatulids in having large, hard oral pinnules that larger ones trying to colonize the two comatulids and, thus, form a thorny crown over the oral surface of the cup, a small being forced to occupy the less favourable hosts. The size seg- oral surface, and also a subdivided visceral mass which are regation in G. obscura individuals suggests host switching be- certainly not suitable for harbouring large symbionts. It is haviour similar to that reported for other marine and freshwater therefore interesting to consider why the brittle star selects symbionts (Britayev 1991, Britayev and Smurov 1985,De such apparently "inconvenient" hosts. Bruyn et al. 2010, 2011, Mikheev et al. 2007,Tokajietal.2014). Symbiotic associations are often driven by intraspecific and Additional arguments supporting this hypothesis were in- interspecific competition (e.g., Preston 1973; Chang et al. 1987). ferred from combining size distribution and traumatism analy- A strictly regular symbiont distribution (i.e.one symbiont per ses. Symbionts with a disk diameter of 0.6-1 cm occurred on all host), has been suggested to be the result of strong intraspecific host species (though they were most prevalent on H. competition (Dimock 1974; Baeza and Stotz 2001; Britayev et robustipinna), while showing the highest the percentage of in- al. 2007). The location of large symbionts in more comfortable jured individuals (57%). This is more than twice the percentage positions, shifting smaller ones to less convenient positions, may of the neighbouring size classes (less than 25%) and close to also be the result of intraspecific competition (Britayev et al. that of free-living brittle stars (52 – 100%) (Bourgoin and 1989; Baeza and Stotz 2001). C. nobilis and C. parvicirrus Guillou 1994; Clements et al. 1994; Munday 1993). Most

Fig. 4 Size structure of G. obscura population in Nhatrang Bay and distribution size classes between host species Mekhova E.S. et al.

Fig. 5 Percentage of traumatized individuals in size classes of Gymnolophus obscura

traumas in ophiuroids are caused by predators (Linsday 2010), a disk diameter of approximately 0.6–1.0 cm is reached, which while symbionts are likely more vulnerable to predation when agrees with the increasing incidence of trauma and mortality. away from their hosts (Castro 1978). Therefore, our data sug- This scenario suggests ontogenic host switching in G. gest that the 0.6-1.0 cm size class includes the most frequent obscura, either between individuals of the same host species host-to-host migrators. Two reasons may help explain this mi- or between different host species, which may also be related to gration pattern. First, the replacement of small symbionts by ontogenic changes in host selectivity. Further laboratory ex- larger ones in the case of multiple infestation of preferred hosts periments are required to determine whether different symbi- (C. nobilis and C. parvicirrus). Second, the search for more ont size classes may have different host preferences. favourable trophic or protective conditions by symbionts set- Considering the wide distribution and abundance of G. tling on less favourable hosts (H. robustipinna and S. indica). obscura in the tropical Indo-West Pacific, it seems likely that The sharp decrease of symbionts in the next 1.1-1.5 cm size resource partitioning between adult and juvenile symbionts class on H. robustipinna and their slight increase on preferred compensates for the risk of migration and host switching, hosts (Fig. 4) possibly indicate a high mortality level when and favours survival and dispersal of the symbiont. colonizing preferred hosts. Based on our data on symbiont size-class distributions (and Acknowledgements The authors would like to thank the administration lacking information on larval phases), we suggest that symbiont and staff of the Coastal Branch of the Russian-Vietnam Tropical Center for their help in organizing and conducting field studies, Dr. P. Dgebuadze, settlement may occur on both preferred and non-preferred hosts. O. Savinkin, Yu. Deart for their help and collaborative work in the field and In the case of already-infested hosts, most of the juveniles colo- in the laboratory, and Dr. V.N. Mikheev for fruitful discussion of the man- nizing the preferred hosts, such as C. nobilis and C. parvicirrus, uscript. We are also grateful to two anonymous reviewers and the editor for will almost immediately be displaced by previously-existing their useful comments and text corrections. Material processing and prepa- ration of the manuscript were supported by the Russian Foundation for Basic large guests, thus being forced to migrate to another appropriate Research; project no. 18-05-00459. This study was also supported by a host such as H. robustipinna or S. indica. The juveniles trying to research project of MSU Zoological Museum (AAAA-A16- colonize these less preferred hosts are in a more favourable sit- 116021660077-3, depository of specimens) and The Russian Science uation, as they have no competitive pressure from the adults in a Foundation (grant 14-50-00029, morphological and taxonomic study). well-protected host cup. Also, their size allows them to feed not only from the host’s mouth, but also from the arms’ bases. Accordingly, they are able to survive in an environment with References reduced intraspecific competition for both food and space. As they grow, the requirement for resources increases, thus forcing Baeza JA, Stotz W (2001) Host-use pattern and host-selection during ontogeny of the commensal crab Allopetrolisthes spinifrons (H. them to leave the host, especially in the case of multiple infesta- Milne Edwards, 1837) (Decapoda: Anomura: Porcellanidae). J Nat tions. The maximum rate of these migrations likely occurs when Hist 35:341–355 Host selection and host switching in Gymnolophus obscura – a symbiotic ophiuroid associated with feather...

Baeza JA, Thiel M (2007) The mating system of symbiotic crustaceans. A Dimock RV Jr (1974) Intraspecific aggression and the distribution of a conceptual model based on optimality and ecological constraints. In: symbiotic polychaete on its host. In: Vernberg A (ed) Symbiosis in DuVy JE, Thiel M (eds) Reproductive and social behavior: crusta- the sea. University of South Carolina Press, Columbia, pp 29–44 ceans as model systems. Oxford University Press, Oxford, pp 250– Fourgon D, Jangoux M, Eeckhaut I (2007) Biology o f a Bbabysitting^ 267 symbiosis in brittle stars; analysis of the interactions between Baeza JA, Stotz W, Thiel M (2001) Life history of Allopetrolisthes Ophiomastix venosa and Ophiocoma scolopendrina. Invertebr spinifrons (H.M. Edwards, 1837), a crab associate of the sea anem- Biol 126:385–395 one Phymactis clematis. J Mar Biol Ass UK 81:69–76 Grange KR (1991) Mutualism between the antipatharian Antipathes Barel CDN, Kramers PGN (1977) A survey of the associates fiordensis and the ophiuroid Astrobrachion constrictum in New of the North-East Atlantic area. Zoologische Verhandelingen 156:1– Zealand fjords. Hydrobiologia 216–217:297–303 159 Hendler G (1984) The association of Ophiothrix lineata and Bell JL (1984) Changing residence: dynamics of the symbiotic relation- Callyspongia vaginalis: a brittlestar-sponge cleaning symbiosis? ship between Dissodactylus mellitae Rathbun (Pinnotheridae) and PSZN I: Mar Ecol 5:9–27. https://doi.org/10.1111/j.1439-0485. Mellita quinquiesperforata (Leske) (Echinodermata). J Exp Mar 1984.tb00304.x Biol Ecol 82:101–115 Hendler G, Grygier MJ, Maldonado E, Denton J (1999) Babysitting brit- Bourgoin A, Guillou M (1994) Arm regeneration in two populations of tle stars: heterospecific symbiosis between ophiuroids Acrocnida brachiata (Montagu) (Echinodermata: Ophiuroidea) in (Echinodermata). Invertebr Biol 118:190–201. https://doi.org/10. Douarnenez Bay (Brittany, France): an ecological significance. J 2307/3227060 Exp Mar Biol Ecol 184:123–139 Huang HD, Rittschof D, Jeng MS (2005) Multispecies associations of Britayev TA (1991) Life cycle of the symbiotic scaleworm Arctonoe macrosymbionts on the comatulid Comanthina schlegeli vittata (Polychaeta: Polynoidae). Ophelia 5:305–312 (Carpenter) in southern Taiwan. Symbiosis 39:47–51 Britayev TA, Smurov AV (1985) The structure of a population of symbi- Ivlev BC (1955) Expiremental ecology of fish feeding. Moscow, onts and related biological features, Arctonoe vittata (Polychaeta, Pisheprom, pp 1–252 Polynoidae) taken as an example. Zhurnal obschey Biologii 46(3): James DB (1995) associations in echinoderms. J Mar Biol Assoc 355–366 (In Russian, English summary) India 37:272–276 Britayev TA, Smurov AV, Adrianov AV, Bazhin AG, Rhzavsky AV Jangoux M (1987a) (a) Diseases of Echinodermata. 11. Agents metazoans (1989) Ecology of symbiotic Polychaete Arctonoe vittata according (Mesozoa to Bryozoa). Dis Aquat Org 2:205–234 to the peculiarity of starfish Asterias ratbunae ecology. [In Russian]. Jangoux M (1987b) (b) Diseases of Echinodermata. 111. Agents meta- In: Sveshnikov VA (ed) Symbiosis among marine animals. A.N. zoans (Annelida to Pisces). Dis Aquat Org 3:59–83 Severtzov Institute, Russian Academy of Sciences, Moscow, pp Kasumyan АО, Тinkova Т V, Is ae va ОМ,BritaevТА, Dgebuadze PYu, – 102 127 Оanh L ТК(2014) Taste deterrency of marine tropical hydrobionts Britayev TA, Martin D, Krylova EM, von Cosel R, Aksiuk TS (2007) as tools for chemical defense against fish. [In Russian]. In Fish Life-history traits of the symbiotic scale-worm Branchipolynoe behavior. V Russian conference. 8–9 November 2014, Borok, seepensis and its relationships with host mussels of the genus Russian Federation. Kostroma:Kostromskoy pechatny dom, pp Bathymodiolus from hydrothermal vents. Mar Ecol 28:36–48 101–106 Castro P (1978) Movements between corals colonies in Trapezia Lechowicz MJ (1982) The sampling characteristics of electivity indices. ferruginia (Crustacea: Brachyura), an obligate symbiont of Oecologia 52:22–30 – scleractinian corals. Mar Biol 46:237 245 Linsday SM (2010) Frequency of injury and the ecology of regeneration Chang KH, Chen YS, Chen CP (1987) Xanthid crabs in the corals, in marine benthic invertebrates. Integr Comp Biol 50(4):479–493 Pocillopora damicornis and P. verrucosa of southern Taiwan. Bull Loehle C, Rittenhouse LR (1982) An analysis of forage preference indi- – Mar Sci 41:214 220 ces. J Range Manage 35(3):316–319 Clark AH (1921) A monograph of the existing crinoids. Bul US Nat Mus Lyskin SA, Britaev TA (2005) Symbionts of holothurians from South – 82(2) (Parasites and Commensals)):616 660 Vietnam: intra- and interspecific interactions. Dokl Biol Sci 401: Clements LAJ, Bell SS, Kurdziel JP (1994) Abundance and arm loss of 116–119 the infaunal britlestar Ophiophragmus filograneus (Echinodermata: Mekhova ES, Britayev TA (2012) Feather stars (Crinoidea, Comatulida) Ophiuroidea), with an experimental determination of regeneration of Nhatrang Bay, Vietnam: fauna, habitat and symbionts. In: – rates in natural and planted seagrass beds. Mar Biol 121:97 104 Britayev TA, Pavlov DS (eds) Benthic fauna of the Bay of Coppard SE, Campbell AC (2004) Organisms associated with diadematid Nhatrang, Southern Vietnam, vol 2. KMK Press, Moscow, pp echinoids in Fiji. Echinoderms: München. Taylor & Francis, 447–478 – London, pp 171 176 Mekhova ES, Dgebuadze PY, Mikheev VN, Britayev TA (2015) De Bruyn C, David B, De Ridder C, Rigaud T (2010) Asymmetric ex- Colonization of depopulated crinoids by symbionts: who comes ploitation of two echinoid host species by a parasitic pea crab and its from the bottom and who from the water column? J Mar Biol consequences for the parasitic life cycle. Mar Ecol Prog Ser 398: AssocUK8:1607–1612 – 183 191. https://doi.org/10.3354/meps08315 Mikheev VN, Pasternak AF, Valtonen ET (2007) Host specificity of De Bruyn C, De Ridder C, Rigaud T, David B (2011) Chemical host Argulus coregoni (Crustacea: Branchiura) increases at maturation. detection and differential attraction in a parasitic pea crab infecting Parasitology 134:1767–1774 – two echinoids. J Exp Mar Biol Ecol 397:173 178. https://doi.org/ Morton B, Mladenov PV (1992) The associates of Tropiometra afra- 10.1016/j.jembe.2010.12.005 macrodiscus (Echinodermata: Crinoidea) in Hong Kong. In: Deheyn D, Lyskin SA, Eeckahaut I (2006) Assemblages of symbionts in Morton B (ed) The Marine Flora and Fauna of Hong Kong and tropical shallow-water crinoids and assessment of symbionts' host- Southern China III. Hong Kong University Press, Hong Kong, pp specificity. Symbiosis 42:161–168 431–438 Dgebuadze PY, Mehova ES, Britayev TA (2012) Recolonization of the Mosher CV, Watling L (2009) Partners for life: a brittle star and its Himerometra robustipinna (Himerometridae, Crinoidea) by octocoral host. Mar Ecol Prog Ser 397:81–88. https://doi.org/10. macrosymbionts: an in situ experiment. Symbiosis 58:253–258 3354/meps08113 Mekhova E.S. et al.

Munday BW (1993) Field occurrence and significance of regeneration in Stohr S, O’Hara T, Thuy B (2012) Global diversity of brittle stars Amphiura chiajei (Echinodermata: Ophiuroidea) from Killary (Echinodermata: Ophiuroidea) PLoS ONE/www.plosone.org 7(3) Harbour, west coast of Ireland. Mar Biol 115:661–668 e31940:1–14 Nigam NK, Raghunathan C (2016) New record of crinoid associated Thiel M, Zander A, Baeza JA (2003) Movement of the symbiotic crab brittle star Gymnolophus obscura (Ljungman, 1976) from Liopetrolisthes mitra between its host sea urchin Tetrapygus niger. Andaman and Nicobar Islands, India. World J Fish Mar Sci 8(1): Bull Mar Sci 72(1):89–101 06–09 Tinkova TV, Kasumyan AO, Dgebuadze PY, Oanh LTK, Britaev TA Ohtsuka S, Kondo Y, Sakai Y, Shimazu T, Shimomura M, Komai T et al (2014) Deterrence of feather stars (Crinoidea, Comatulida) from (2010) In-situ observations of symbionts on medusae occurring in Southern Vietnam for the Indo-Pacific sergeant-fish Abudefduf Japan, Thailand, Indonesia and Malaysia. Bulletin of the Hiroshima vaigiensis. Dokl Biol Sci 456:195–198 University Museum 2:9–18 Tokaji H, Nakahara K, Goshima S (2014) Host switching improves sur- Poulin R (2005) relative infection levels and taxonomic distances among vival rate of the symbiotic polychaete Arctonoe vittata. Plank Benth the host species used by parasites: insights into parasite specializa- Res 9(4):189–196 tion. Parasitology 130:109–115 Wirtz P, Diesel R (1983) The Social Structure of Inachus phalangium,a Preston EM (1973) A computer simulation of competition among five Spider Crab Associated with the Sea Anemone Anemonia sulcata. sympatric congeneric species of xanthid crabs. Ecology 54:469–483 Ethology 62:209–234. https://doi.org/10.1111/j.1439-0310.1983. Price A, Rowe F (1996) Indian Ocean echinoderms collected during the tb02152.x Sindbad Voyage (1980-81): 3. Ophiuroidea and Echinoidea. Bull nat Yanagisawa Y, Hamaishi A (1986) Mate acquisition by a solitary crab Hist Mus Lond (Zool.) 62(2):71–82 Zebrida adamsii, a symbiont of the sea urchin. J Ethol 4:153–162