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Crustacean symbionts of the sea anemone Telmatactis cricoides at Madeira and the Canary Islands*
Journal of Zoology
Abstract
The crustacean symbionts of the club-tipped sea anemone Telmatactis cricoides (Duchassaing, 1850) were studied at Madeira (n= 81 anemones) and the Canary Islands (n= 124 anemones).
Of all anemones, 86% had crustacean symbionts. Nineteen species of crustaceans were encountered in association with Telmatactis cricoides. There were up to 18 individuals of up to four crustacean species associated with the same anemone. Anemone size and number of crustacean symbionts were positively correlated (P < 0.001) but only weakly so (r=+0.27). The most common crustacean symbiont was the shrimp Thor amboinensis, encountered with 65% of all anemones.
Frequency and type of association with Telmatactis cricoides is described for each of the crustacean symbionts, Thor amboinensis, Lysmata grabhami, Lysmata seticaudata, Eualus occultus, Brachycarpus biunguiculatus, Stenorhynchus lanceolatus, Homola barbata, Pilumnus villosissimus, Gnathophyllum elegans, Inachus phalangium, Heteromysis sp. nuv., Palaemonella atlantica, Herbstia condyliata, Stenopus spinosus, Athanas nitescens, Dromia personata Xantho incisus, Galathea sp., Liocarcinus sp.
The shrimp Lysmata grabhami appears to live in stable pairs of two simultaneous hermaphrodites, a social structure not previously described for any crustacean species.
... Shrimps have been reported to inhabit the shallow subtidal and intertidal of subtropical and tropical rocky and coral reefs around the world. Some species of Lysmata live in groups, others are solitary, while some species are socially monogamous (pair-living; e.g., L. grabhami (Gordon, 1935)) (Wirtz, 1997). Several species with an inconspicuous coloration dwell freely among rocks in temperate zones, while other more colorful species inhabit tropical sponges (L. ...
... wurdemanni: Baeza, 2006). A second group (named "Pair" species by Bauer, 2000) was described as mostly tropical, occurring at low densities in the subtidal, and dwelling as socially monogamous pairs on sea anemones used as spots for fish-cleaning activities (i.e., L. grabham: Wirtz, 1997;L. amboinensis: Fiedler, 1998). ...
... On the other hand, hermaphroditic shrimps are known to experience brooding constraints (e.g., L. wurdemanni; Baeza, 2007c), a condition that theoretically favors simultaneous hermaphroditism (see Charnov, 1982, and references therein). Similarly, in socially monogamous Lysmata (e.g., L. grabhami; Wirtz, 1997), infrequent encounter rates among conspecifics should be favoring strict simultaneous hermaphroditism over PSH. It should pay (in term of fitness) for each individual in a pair to reproduce both as male and female as soon as possible during their life-SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES time because this strategy increases reproductive success through both sperm donation to the partner and female reproduction. ...
... In addition, five polyps of zoanthid Zoanthus sociatus (Ellis, 1768) associated with O. bicornuta ( Figure 4A) were also observed. The interspecific relationships of sea anemones with crustaceans have been well documented (Wirtz & Diesel, 1983;Fautin et al., 1995;Wirtz, 1997;Acuña et al., 2003;Gusmão et al., 2019Gusmão et al., , 2020among others). Furthermore, many of these crustacean species associate with sea anemones to protect themselves against predators such as fish and octopus (Wirtz, 1997), they also feed on anemone regurgitates and mucus from the anemone's surface, and even crops the tips of its host's tentacles (Wirtz & Diesel, 1983;Fautin et al., 1995). ...
... The interspecific relationships of sea anemones with crustaceans have been well documented (Wirtz & Diesel, 1983;Fautin et al., 1995;Wirtz, 1997;Acuña et al., 2003;Gusmão et al., 2019Gusmão et al., , 2020among others). Furthermore, many of these crustacean species associate with sea anemones to protect themselves against predators such as fish and octopus (Wirtz, 1997), they also feed on anemone regurgitates and mucus from the anemone's surface, and even crops the tips of its host's tentacles (Wirtz & Diesel, 1983;Fautin et al., 1995). ...
Sea anemones have developed various strategies for interspecific interaction with other organisms and their own ability to obtain food, due to their coevolutionary history, ranging from mutualistic (e.g. clownfish, crustaceans, etc.) and symbiotic associations (zooxanthellae or zoochlorellae) to depredation (e.g. sea slug). This study aims to record some observations on feeding habits and interspecific interactions of Actinostella flosculifera (Le Sueur, 1817) in the locality of Pedra da Sereia in Vila Velha, Espírito Santo, Brazil, and to describe the hunting strategy of the sea slug Spurilla braziliana MacFarland, 1909 and the escape strategy of A. flosculifera. We found that the habitat of A. flosculifera is characterized by shallow pools ∼10 cm deep at low tides, and this functions as a trap for many organisms and some biowaste (e.g. bones or fish drifting in from nearby populations) that fall into the oral disc. This is the first report of S. braziliana predating on A. flosculifera. We also report interspecific relationships between A. flosculifera with four species of crustaceans: Omalacantha bicornuta (Latreille, 1825), Menippe cf. nodifrons Stimpson, 1859, Alpheus cf. angulosus McClure, 2002, and Alpheus cf. carlae Anker, 2012.
... Eastern Atlantic: Cape Verde Islands (type locality) (Holthuis 1951a;Türkay 1982;Wirtz and d'Udekem d'Acoz 2001); Azores, Madeira, Canary Islands (Fransen and Wirtz 1997;Wirtz 1997), Gabon (Rossignol 1962); St Helena Island (new records from our study). Holthuis, 1973 (Fig. 3d.) ...
The pantropical genus Palaemonella Dana, 1852 (Caridea: Palaemonidae) currently includes 27 species of free-living and symbiotic marine shrimps. The monophyly of Palaemonella with respect to several closely related genera, however, has been questioned by recent analyses. We tested the monophyly of Palaemonella based on multigene phylogenetic analysis and the genus was revealed to be a paraphyletic assemblage by inclusion of species of the genera Eupontonia Bruce, 1971 and Vir Holthuis, 1952, and two genetic lineages of the western Atlantic Cuapetes americanus (Kingsley, 1878). We recognise one of the latter lineages as the previously described Periclimenes rhizophorae Lebour, 1949. Eupontonia and Vir are synonymised with Palaemonella. We also transfer Cuapetes americanus and Periclimenes rhizophorae to Palaemonella. Species previously assigned to Vir were revised; V. colemani Bruce, 2003, V. orientalis (Dana, 1852), V. philippinensis Bruce & Svoboda, 1984 and V. smiti Fransen & Holthuis, 2007 are regarded as valid species of Palaemonella; Vir longidactylus Marin, 2008 is synonymised with P. smiti; and the status of V. euphyllius Marin & Anker, 2005 remains unresolved. Palaemonella is currently regarded as a taxon with variable states of two main diagnostic characters, i.e. the plesiomorphic mandibular palp (fully reduced in P. americana) and the hepatic tooth (fully reduced in former species of Vir and Eupontonia – evidently due to symbiotic modes of life). ZooBank: urn:lsid:zoobank.org:pub:7EEBC655-7EDE-4E46-BCB2-2A3BA16ED7DD
... Shrimps from the genus Lysmata Risso, 1816 (Infraorder Caridea, family Lysmatidae Dana, 1852) are widely distributed in tropical and subtropical regions worldwide (De Grave & Anker 2018;Giraldes et al. 2018) and include 48 species (Rhyne & Lin 2006;Baeza & Anker 2008;De Grave & Fransen 2011;Anker & Cox 2011;Rhyne et al. 2012;Soledade et al. 2013;Gan & Li 2016;Pachelle et al. 2016;Prakash & Baeza 2017;Wang & Sha 2018;De Grave & Anker 2018;Giraldes et al. 2018). They present a wide range of lifestyle and habits, such as living in dense aggregations and moving freely among rocks [e.g., Lysmata californica (Stimpson 1866) (Bauer & Newman 2004) and Lysmata ankeri Rhyne & Lin 2006(Barros-Alves et al. 2016], or living in monogamous pairs usually in symbiotic associations [e.g., Lysmata grabhami (Gordon 1935) (Wirtz 1997) and Lysmata pederseni Rhyne & Lin 2006(Baeza et al. 2016]. ...
The early larval stages of the shrimps Lysmata ankeri and L. bahia were described, illustrated, and compared among other Lysmata species, providing important information on post-embryonic development and insights into its evolutionary history. Ovigerous specimens of L. ankeri and L. bahia were sampled from southeastern and northeastern Brazilian coast, respectively. For L. ankeri and L. bahia, five and three larval stages were obtained, respectively. Unique features were observed for L. ankeri and L. bahia larvae, and some characteristics may differ only for L. ankeri and L. bahia, which were not observed in the other species analyzed, such as: presence of a pair of simple setae on the third pleonal somite in zoea I and number of setae on the uropod exopod greater than 11. Moreover, several other features are similar between species from the diferent clades of the Lysmata-Exhippolysmata complex, making it possible to identify the early stages of Lysmata larvae. However, future studies will be essential to confirm or not the existence of some phylogenetic patterns and their relevance and other larval characters for better understanding the evolutionary history of this group.
... One interesting aspect of sea anemone biology is the association with vertebrates and invertebrates (Shick 1991). Surprisingly, while some sea anemones are well known for their symbiotic relationships (e. g. Wirtz 1997, Calado et al. 2007, Huebner & Chadwick 2012, the relationships of eye-catching species such as Homostichanthus duerdeni (Carlgren, 1900) are poorly documented. Homostichanthus duerdeni is a large and colourful sea anemone with a broad distribution ranging from Mexico to Brazil. ...
Crustaceans have diversified sexual systems, incorporating various reproductive modalities such as gonochorism and a wide variety of hermaphroditism. In particular, the coral reef-dwelling caridean shrimps, living in symbiosis with other
marine invertebrates, have developed unusual sexual systems that have given origin to a range of social systems, including the highly advanced eusociality. Protandric hermaphroditism, common among the caridean shrimps, has also reached a
unique sexual condition, known as protandric simultaneous hermaphroditism in the genus Lysmata. Similarly, mating systems in the caridean shrimps are highly diverse and divergent. In addition, their occurrence in the coral reef shrimps is correlated to their lifestyle adaptations such as their commensal association with other invertebrates. Other ecological factors like the predation risk from outside of the host animals and differences in the host characteristics may also be the driving forces in determining mating associations. Furthermore, the transition from sexual monogamy to social monogamy under conditions of their symbiotic life led to a complex community living in several synalpheid shrimps. Understandably, the existence of various sexual and mating systems in these caridean shrimps has a dependence on the eco-social conditions prevalent in the coral reef biota.
Most shrimp species have separate sexes. However, approximately 90 caridean species show some form of protandric hermaphroditism. In protandry, individuals mature first as males but when older and larger, change sex to females. Protandric sexual systems vary in form among species from pure protandry to protandric simultaneous hermaphroditism. Identification of protandric systems is based on the study of male and female size-frequency distributions, presence of sexually transitional individuals, and direct observation of sex change in captive individuals. To date, hermaphroditism has been observed only in caridean shrimps but not in any dendrobranchiates or stenopodideans. The distribution of hermaphroditism among different caridean families is spotty. The number of hermaphroditic species per family ranges from none to low to most to all. Sex change is physiologically mediated by the androgenic glands. In at least some species, environmental conditions, especially social organization, may influence the frequency of hermaphroditic individuals in a population. Hypotheses about the original sex of hermaphroditic individuals are compared and evaluated. The apparent absence of hermaphroditic species in dendrobranchiate and palaemonoid shrimps is a puzzle that awaits resolution. The sexual system of the many uninvestigated species will likely reveal a number of undiscovered hermaphroditic ones.KeywordsGonochorismSex changeHermaphroditismProtandryAndrogenic gland
Numerous shrimp species live in intimate, long-term associations (symbioses) with invertebrates and gobiid fishes. Symbioses can be characterized as commensal, mutualistic, or, more rarely, parasitic. Symbioses are found in caridean and stenopodidean but not in dendrobranchiate shrimps. The morphology and feeding behavior of many symbiotic shrimps have been adapted to living with their hosts. A number of symbiotic shrimps live within the canals of sponges, receiving protection and food. The social organization of Synalpheus sponge shrimps varies from pair-living to communality to eusociality most similar to that of termites. Shrimps living with corals, anemones, and jellyfishes may both receive or give protection to their hosts, in addition to food and shelter. Many shrimp species live among the spines or below sea urchins. Other echinoderms, such as ophiuroids, starfishes, and especially crinoids, serve as shrimp hosts. Some shrimps live with molluscs, especially within shells of bivalves, feeding on the food-laden mucus or feces of the host. Still others have a similar lifestyle within branchial or atrial chambers of ascidians. Some shrimps share the burrows made by invertebrates and other crustaceans. A unique mutualistic relationship has evolved between alpheid shrimps and gobiid fishes, in which a male–female shrimp pair give the fish shelter in their burrow while the fish provides both food and a warning system. Some shrimps clean ectoparasites and injured tissues from fishes. The shrimp cleaner and fish client have evolved communication so that the shrimps can clean without danger of predation. Hypotheses on the evolution of shrimp symbioses are evaluated.KeywordsCommensalismMutualismEusocialityCleaner shrimpsGoby shrimps
Males and females have evolved a particular set of tactics and strategies, or mating systems, to find and successfully inseminate or be inseminated by a high-quality mate. Both sexes use visual, tactile, and chemical cues to seek out suitable and receptive mates. Various appendages, especially the antennules and antennae, have receptors for detecting chemical cues (sex pheromones) emitted by the other sex. Olfactory (distance, “smell”) pheromones are soluble compounds emitted at low concentrations and perceived at a distance. Contact (“taste”) pheromones are released onto the exoskeleton and must be touched to be sensed. Progress has been made on chemical identification of pheromones but is still controversial. In pure-searching (promiscuous) mating systems, males constantly search for sexually receptive females, followed by little pre- or post-copulatory interaction. In temporary mating systems, males seek out prespawning females, guard them until she molts, and then mating occurs. But in some species, females seek out a dominant male to protect them until the female molts and is receptive. Many species live in long-lasting, often monogamous pairs, which ensures successful reproduction with a reduced risk of predation. Although males are usually the more eager and aggressive sex, females have a variety of tactics for rejecting unsuitable mates. Females of some dendrobranchiate species may be mated by multiple males, but insemination may be assured by the male which first plugs or seals the apertures to female seminal receptacles.KeywordsPheromonesPromiscuityPairingMonogamyPaternity
To provide a background for the investigations dealt with in this paper, it is necessary to summarize some fundamental experiments on the protection of anemone fishes.
The small shrimp Gnathophylloides mineri is a common inhabitant of the short spines of the sea urchin Tripneustes ventricosus found in shallow waters of eastern St. Croix, United States Virgin Islands. It shows remarkable cryptic coloration and behavioral and morphological features suggesting a past history of intense predation pressure. Gnathophylloides mineri feeds on the epithelium covering the sea urchin spines which is abraded by toothed setae on the second maxillipeds and perhaps also by small, handlike structures on the dactyls of the walking legs. It seems likely that dark pigment from the host test is incorporated by the shrimp. Filter feeding also occurs. The shrimp are usually found in groups (up to 13 on a given host) with females greatly outnumbering males. Although there is a broad overlap in size distributions, males are significantly smaller. There is evidence that shrimp move between urchins. Differential male mortality during migration may explain the uneven sex ratio.
ABSTRACT The distribution of Inachus phalangium (Decapoda: Majidae) on the sea anemone Anemonia sulcata was investigated from 1982 to 1984 in the coastal region of Banyuls-sur-Mer (southern France). Most adult crabs (64.5%) were found alone on an anemone, but groups of 2, 3, and 4 adults sharing an anemone were decreasingly frequent. Spider crabs were randomly distributed on the anemones; 79.5% of the occupied anemones held only one crab. In cases of multiple occupation of a given anemone, (1) heterosexual pairs were more frequent than could be expected for random association, and homosexual pairs less frequent, (2) reproductive males were paired more frequently than expected with females ready to spawn, and (3) adult males pairing with females ready to spawn were larger than solitary males or those males with females not yet ready to spawn. In multiparous females 27% of the variance in the number of eggs per brood was explained by body size; egg number was positively correlated with body size but varied strongly within the same body-size class. Assortative pairing for body size in pairs was not found, probably because any fitness advantage accruing to males in choosing large females is offset by the costs of longer seeking time and the loss of mating opportunities with smaller females.