This review of copepod crustaceans associated with reef-dwelling cnidarians, sponges and echinoderms of the Greater Caribbean is based on published records, systematically arranged by the classification of symbiotic copepods and their hosts, sampling sites, coordinates, depth and date of sampling, literature sources, and three recent surveys (Cuba, St. Eustatius in the Eastern Caribbean and Curaçao in the Southern Caribbean). This resulted in totals of 532 records of 115 species of symbiotic copepods (47 genera, 17 families, three orders) hosted by 80 species of invertebrates, representing scleractinians (47%), octocorals (9%), echinoderms (3%), and sponges (1%). Among ten Caribbean ecoregions, the Greater Antilles (with 64 species of symbiotic copepods) as well as the Southern and Eastern Caribbean (with 46 and 17 species of copepods, respectively) are the most studied and best represented, whereas only six species of copepods are known from Bermuda, one from Southwestern Caribbean and none from the Gulf of Mexico. The absence of poecilostomatoid copepods (Anchimolgidae, Rhynchomolgidae and Xarifidae) on Caribbean stony corals as noted by Stock (1988) is confirmed. The results indicate that the diversity and ecology of Caribbean symbiotic copepods are still poorly investigated.
Symbiotic copepods are a widespread, numerous and diverse group of crustaceans living in association (parasitism, commensalism, mutualism) with other marine animals (Gotto, 1979, 1993; Humes, 1985a, 1994; Ho, 2001). At least one third of all known copepods are symbionts of marine fish and invertebrates. Symbiotic copepods are the most diverse in the tropics, and only a small number of their potential marine invertebrate hosts has been explored so far (1.14% according to Humes, 1994). A high degree of endemism as well as a remarkable difference in taxonomic composition of copepods living in a poorly studied symbiosis with Caribbean stony corals is noticed in comparison with the Indo-Pacific (Stock, 1988). The paucity of knowledge of symbiotic copepods of the Greater Caribbean region has repeatedly been noted (Stock, 1973, 1975a, 1987, 1988; Humes & Hendler, 1972; Herriott & Immermann, 1979; Grygier, 1980; Ivanenko et al., 2017).
The first study of symbiotic copepods living on cnidarians, echinoderms and sponges of the Greater Caribbean was conducted by Edwards (1891), who discovered Diogenidium nasutum (fig. 1c), living on the sea cucumber Holothuria scabra, in the Bahamas (species authorities in tables 1–2). Taxonomic studies of the Caribbean symbiotic copepods were continued by a number of researchers, who described large numbers of new species, as reviewed by Gotto (1993). A number of copepods representing two families (the ectosymbiotic Asterocheridae and the endoparasitic Corallovexiidae) have been found living on and in stony corals (Hoeksema et al., 2017b). Very few are reports have been published about the Asterocheridae living and usually abundant on sponges (Stock & Kleeton, 1964; Stock, 1967; Boxshall & Huys, 1994; Kim, 2010; Varela et al., 2005b, 2007a, b, 2008; Varela, 2010a, b, 2012). Twelve families of copepods have been reported on diverse Caribbean echinoderms (Edwards, 1891; Emson & Mladenov, 1987; Emson et al., 1985; Hendler & Kim, 2010; Humes & Hendler, 1972, 1999; Humes & Ho, 1970, 1971; Humes & Stock, 1973; Humes, 1969a, 1998, 2000; Kim, 2009, 2010; Stock & Gooding, 1986; Stock & Humes, 1995; Stock et al., 1962, 1963a, b; Stock, 1968; Varela et al., 2003, 2005b, 2008; Varela, 2010a, 2011a). Most of these studies on Caribbean invertebrate-associated copepods are from the last century and only 19 of them have been published since 2000 (Humes, 2000; Varela et al., 2003, 2005a, b, 2007a, b, 2008; Varela & Lalana, 2007; Kim, 2009, 2010; Hendler & Kim, 2010; Varela, 2010a, b, 2011a, b, 2012; Ivanenko et al., 2017; Shelyakin et al., 2018; Garcia-Hernandez et al., 2019).
Caribbean reef corals are under threat from climate change and local impacts (Carpenter et al., 2008; Hughes et al., 2017) and some symbiotic (including parasitic) copepods potentially may have an impact on the state of corals and other invertebrate hosts (Stock, 1975a; Butter, 1979; Herriott & Immermann, 1979; Burke & Maidens, 2004; Ivanenko et al., 2017; Shelyakin et al., 2018). Despite a long history of marine biodiversity research in the Caribbean, our knowledge of microscopic symbiotic copepods does not satisfy the needs for defining priorities in conservation and the development of management plans (Miloslavich et al., 2010; Zeppilli at al., 2015, 2018). The goal of our review is to analyze all published data on copepods living in symbiosis with the Caribbean reef-dwelling anthozoans, echinoderms and sponges as important structural and functional components of Caribbean coral reefs in order to identify the least-studied ecoregions and groups of hosts as well as to identify directions for further research.
Characteristics of the Greater Caribbean
The Greater Caribbean (The Caribbean s.l.) in the present review consists of the Caribbean Sea plus the Gulf of Mexico and Bermuda (Spalding et al., 2007; Hoeksema et al., 2017a). The Caribbean Sea (Caribbean s.s.) is a large semi-enclosed sea of the western Atlantic Ocean with clear and warm water (22–29°C) and low tidal amplitude (0.4 m) (Kinder et al., 1985). The Caribbean is enclosed by the land masses of Central and South America (Brazil) from the west and south. It is separated by island arcs of the Great and Lesser Antilles in the north and east (Bayer, 1961; Spalding et al., 2004; Alvarado, 2011). The Caribbean is a unique biogeographic region with a number of endemic species (Rivera-Monroy et al., 2004; Alvarado, 2011). It is recognized as a global marine biodiversity hot spot and an important biogeographic coral reef province (Spalding et al., 2001; Roberts et al., 2002; Miloslavich et al., 2010; Alvarado, 2011). The Greater Caribbean includes ten marine ecoregions: Northern Gulf of Mexico, Southern Gulf of Mexico, Floridian, Western Caribbean, Greater Antillean, Southwestern Caribbean, Southern Caribbean, Eastern Caribbean, Bahamian, and Bermudian (Burke & Maidens, 2004; Spalding et al., 2007; Hoeksema et al., 2017a). The Bahamian and Bermudian are adjacent to the temperate northwestern Atlantic. The marine ecoregions of the Southern and Eastern Caribbean are affected by biota from adjacent Brazilian waters (Alvarado, 2011). The Gulf of Mexico has colder and more isolated water, which is relatively poor in species (Felder & Camp, 2009).
The data are combined in the originally designed Database on Caribbean copepod crustaceans associated with reef-dwelling corals, echinoderms and sponges. This database includes five main tables: Hosts, Symbionts, Samples, Sites, and Publications linked with each other and two combined tables Literature Records and Sample Records; each record contains data on the taxonomy of the host and its symbiont, the references to unique records in the World of Copepods (Walter & Boxshall, 2019), the number of associates per host, the nature of the association, the name and coordinates of the collection site, the depth and the date of collection, as well as their reference (Korzhavina & Ivanenko, 2019). In addition, data on samples of symbiotic copepods and their hosts collected at St. Eustatius (in 2015, with 104 samples), Curaçao (in 2017, with 77 samples) and Cuba (in 2019, with 56 samples) preserved in 96% ethanol and including underwater photographs have been added to the table Sample Records.
Results and discussion
The database includes 532 records from 154 localities and 54 references published since 1891 (Edwards, 1891). There are 115 species of copepods (47 genera, 17 families, 3 orders) found in symbiosis with 80 invertebrate host species representing 58 genera, 39 families, 22 orders and 7 classes of corals, sponges and echinoderms (figs. 1–7, tables 1–7). Only one species of copepods, the poecilostomatoid cyclopoid Hemicyclops columnaris (syn Hemicyclops geminatus) was found in the area under consideration (Bahamas, Barbados, Curaçao, and Jamaica, associated with a burrowing ghost shrimp, a sponge, an ophiuroid, hermit crabs) and on the Pacific coast of Panama (on a stony coral) (fig. 1a) (Humes, 1984; Stock, 1992a; Kim, 2009). All other species of symbiotic copepods are found in the Caribbean only, which may be the result of high endemism of their host species (Miloslavich et al., 2010; Soest et al., 2012; Zea et al., 2014; Ivanenko, 2016).
The copepods were collected by washing of the hosts in seawater or tap water (Butter, 1979; Garcia-Hernandez et al., 2017), a solution of formalin (Varela & Lalana, 2007; Varela et al., 2003, 2005a, b, 2007a, b, 2008; Varela, 2010a, b, 2011a, b, 2012), a solution of ethanol (Stock et al., 1962, 1963a, b, Humes, 1969a, 1998, 2000; Humes & Stock, 1973; Stock, 1975a, b, d; Herriott & Immermann, 1979; Stock & Humes, 1995) or a solution of magnesium-chloride (Stock & Humes, 1995), dissecting of the host’s tissues or galls (see Stock et al., 1962; Humes & Hendler, 1972, 1999; Humes & Goenaga, 1978; Stock, 1978; Grygier, 1980; Emson et al., 1985; Emson & Mladenov, 1987; Hendler & Kim, 2010; Ivanenko et al., 2017), by a suction device (Humes & Stock, 1973) or by dissolving soft tissues of host corals with bleach (Stock 1975a, 1989). Most of the host invertebrates were collected by SCUBA living down to 41 m depth. The only exceptions are the three of eight species of the Caribbean copepods of the family Lamippidae tentatively included in the database found in galls or tissue of octocorals collected by a submersible away from reefs at depths of 55–330 m (fig. 2 a–d) (Stock, 1978, 1979; Grygier, 1980). It is noteworthy that there are no data on symbiotic copepods associated with reef-dwelling sponges, echinoderms and corals living at mesophotic depths; studies on reef communities and coral-associated fauna from mesophotic depths seems to be an important task that has just started (Bongaerts et al. 2010, 2015; van der Meij et al., 2015; Hoeksema et al., 2017c; García-Hernández et al., 2018; Veglia et al., 2018).
Symbiotic copepods are reported from eight out of ten ecoregions of the Greater Caribbean, but none from the Northern and Southern Gulf of Mexico (table 6, figs. 4–7; Spalding et al., 2007; Hoeksema et al., 2017a). Eight records are known for Bermuda: four species of poecilostomatoid cyclopoids representing genus Acanthomolgus and the siphonostomatoid Ophiopsyllus reductus were found associated with alcyonaceans and an ophiuroid, respectively (Stock et al., 1963a; Humes, 1973). Only one record is reported for the Southwestern Caribbean: the calanoid Ridgewayia fosshageni aggregating on the actinairian Bartholomea annulata. Only Aspidomolgus stoichactinus living on the actiniarian Stichodactyla helianthus and the corallimorpharian Corynactis denticulosa, recorded as Homostichanthus denticulosus, is found in five ecoregions (Humes, 1969a; Stock, 1975b). Five species of copepods are found in four ecoregions, viz. Caribulus sculptus living on holothurians, Chelacheres longipalpus and Macrochiron echinicolum (fig. 1d) found on sea urchins, Ophiopsyllus reductus living on ophiuroids. Seventeen and 87 species of copepods are recorded found in only two and one ecoregions, respectively (table 6).
The data show that the three most intensively explored ecoregions are the Bahamian, Greater Antilles and Southern Caribbean, with studies centered at Curaçao (123 records, 36 species of hosts, 49 species of copepods), Puerto Rico (105, 22, 27) and the Bahamas (57, 11, 19). The mosaic data show poor knowledge of most ecoregions as well as and many host taxa. This current state of the knowledge limits analysis of the distribution of symbiotic copepods in the whole Caribbean. Well planned studies of different Caribbean regions and the application of modern methods of integrative taxonomy are needed to carry out such analyses (DeBiasse et al., 2016; Jossart et al., 2017; Ivanenko et al., 2018).
A comparison of taxonomic names from literature sources with their current nomenclature revealed name changes for 29 (of 80) species and 12 (of 58) genera of the hosts (WoRMS, 2019). The taxonomic names are changed for nine (of 115) species and six (of 47) genera of the copepods. There are six records of symbiotic copepods identified to genus (Asterocheres, Corallovexia, Corallonoxia, Critomolgus, Enalcyonium, Sphaerippe). These taxa are included in; among 16 hosts (for 18 records) that have no identification at species level; of these one is assigned to a phylum, three to a class and 12 to a genus. There are 41 records for which the hosts are identified only to taxonomic categories such as phylum, order or subclass. There are 81 records of copepods found on sponges, but hosts of 14 of them are defined only to phylum (Kim, 2009, 2010). The absence of precise identifications and the necessity of linking outdated host names with valid ones show the need for specimen collections of not only copepods but also of their invertebrate hosts, as well as morphological and molecular studies of this material (Rocha et al., 2014). The DNA-barcoding of the hosts, photographing of hosts alive underwater, and photographing of host skeletons along with basic locality data are important for both identification and maintaining information about each copepod host and the establishment of base line information about their distributions (Hoeksema et al., 2011).
In total, there are 253, 197 and 81 records of copepods found associated with echinoderms, cnidarians and sponges, respectively (figs. 1–3). Forty-seven and 20 records of copepods are linked to the scleractinian coral families Faviidae and Meandrinidae (updated classification in Hoeksema & Cairns, 2019), respectively; 36 and 16 of these records pertain to the endoparasitic copepod symbionts belonging to the family Corallovexiidae. Most records from holothurians from the families Holothuriidae and Stichopodidae (75 and 35 records), from ophiuroids the families Ophiocomidae and Ophiotrichidae (29 and 19 records) are most common, from sea cucumbers the family Stichopodidae (35 records) is well represented, alcyonaceans the family Plexauridae (29), and corallimorpharians (four records) also are represented (table 3). Many (25 of 81) records of copepods found on unidentified sponges.
Cyclopoida, representing mainly poecilostomatoids, with 317 records for 59 species is the most diverse order of copepods found in symbiosis with corals, sponges and echinoderms; Siphonostomatoida with 170 records of 55 species is the next (figs. 1–3, table 4). The order Calanoida is represented by the only known symbiotic calanoid copepod Ridgewayia fosshageni found associated with an actiniarian at the Atlantic coast of Panama (Humes & Smith, 1974). The absence in the literature of any records of symbiotic harpacticoids is contradicted by the results recently obtained from samples of undescribed harpacticoids representing the family Laophontidae (see Yeom et al., 2018). Siphonostomatoid copepods of the diverse but poorly investigated family Asterocheridae and poecilostomatoid cyclopoids representing endoparasitic Corallovexiidae have the greatest diversity of associations and the highest number of host families (table 5). Asterocheridae are found living on invertebrates belonging to 22 families of cnidarians, echinoderms and sponges; Rhynchomolgidae are recorded from eight families of anthozoans and echinoderms; Corallovexiidae from five families of stony corals only. Three families (Lamippidae, Pseudanthessiidae, and Synaptiphilidae) are found associated with four host families; Macrochironidae and Nanaspididae are found with three host families; Cancerillidae and Lichomolgidae are found with two host families; seven families (Clausidiidae, Entomolepididae, Micropontiidae, Pseudocyclopidae, Sabelliphilidae, Synaptiphilidae, and Thaumatopsyllidae) are restricted to only one family of invertebrate hosts (table 5). The remarkable absence on Caribbean host corals for copepods of the families Anchimolgidae (124 species in 32 genera) and Xarifidae (96 species in 6 genera) so far only found on Indo-Pacific scleractinians (Stock, 1988), is confirmed by literature data and results of our recent sampling (Cheng et al., 2016; Hoeksema et al., 2017b; table 1). To explain this distribution a study of phylogenetic relationships of Corallovexiidae with other families of the order and the additional search for endoparasitic copepods living in Indo-Pacific stony corals is needed. This proposed study should include methods that enable dissolution only of soft coral tissue while the chitinous exoskeletons of microscopic crustaceans to remain intact.
Fifty of 115 species of symbiotic copepods are mentioned in literature only once; 83 of 115 species of copepods are reported from only one species or one genus of the host. Only 13 species are reported in symbiosis with representatives of different families. Four species of copepods, the poecilostomatoids Eupolymniphilus occidentalis (fig. 1g), Hemicyclops columnaris, Pseudanthessius deficiens (fig. 1e) and the siphonostomatoid Nanaspis pollens (fig, 3e) are found in symbiosis with representatives of different classes. Of these species only Hemicyclops columnaris is found associated with invertebrates representing different phyla: echinoderms, corals, sponges and arthropods. The finding on sponge and on a compound ascidian of the copepod Eupolymniphilus occidentalis (family Sabelliphilidae) typically living on tubicolous polychaetes requires additional confirmation (Kim, 2009). Only two species of copepods are reported living on different classes: Pseudanthessius deficiens is found on three species of echinoderms to holothurians and echinoids; Nanaspis pollens is found on holothurians and ophiurioids. Thus, most species of symbiotic copepods are found associated with invertebrate hosts belonging to a single genus or only one family. These finding suggest the need to study the effect of host specificity more extensively. Similar studies of host switching events may show that this phenomenon has occurred several times during in the evolution of symbiotic copepods, as it has among decapod crustacean taxa (Fransen & Hoeksema, 2014; Brinkmann & Fransen, 2016; García-Hernández et al., 2016; Horká et al., 2016; Hoeksema & Fransen, 2017; Hoeksema et al., 2018). The very nature of the specificity of copepods to the host or to the group of hosts requires a thorough sampling program as well as the use of molecular methods (Ivanenko et al., 2018).
The number of copepod species found on a single host species varies from one to six. The sea cucumber Holothuria arenicola hosts six species of copepods (table 2). Three scleractinian and two holoturian species host five copepod species. The sea urchin Meoma ventricosa and the sea cucumber Actinopyga agassizii host four copepod species; three corals and one sponge host three species each; 18 host species have been recorded with two associated species of symbiotic copepods. Numerous findings of different species of symbiotic copepods on the same hosts as well as the presence on these hosts of other symbionts (shrimps, polychaetes, decapods, amphipods, fish etc.) shows little knowledge of species relationships in the symbiotic complexes (Stella et al., 2011; Hoeksema et al., 2012).
Copepod crustaceans living in symbiosis with the Caribbean reef invertebrates express diverse body shapes (cyclopiform, spherical, flattened etc.), remarkably different body sizes ranging from 0.25 mm (such as Collocheres lunulifer) to 4.75 mm (such as Corallovexia ventrospinosa), and various types of feeding apparatuses as well as host utilizations. Analysis of literature and sorting of samples shows a different, and sometimes very large number of individual copepods living on a single host. The most numerous are the poorly studied asterocherid copepods living on and in diverse sponges: in one sample on one sponge thousands of individual copepods belonging to several species (Schirl, 1973; Ivanenko & Smurov, 1997; Ivanenko, 1998; Klinger et al., 2019; present study). The diversity, host specificity and phylogenetic relationships of these copepods with other siphonostomatoid copepods, especially species found in association with Caribbean stony corals are among the most interesting unexplored topics in coral reef ecology.
The symbiotic copepods are characterized by different ways of attachment to their host (loosely associated with or aggregating on the host’s surface, tightly attached to the host by claw-like appendages, inducing a gall-like structure, or residing inside of intestine, body cavity, or the host tissues). They also show marked variation in the number of embryos present in the egg-sacs (from one embryo, as in Peltomyzon rostratum, to 50 embryos, as in Caribulus sculptus) or numerous embryos laid in copepod-induced galls. The symbiotic copepods have different types of lecithotrophic and planktotrophic naupliar stages, some of which, like Thaumatopsyllidae, are parasitic in the stomach of its host brittle star (fig. 2e; Hendler & Kim, 2010).
Most of the ecological observations of the Caribbean symbiotic copepods are short comments added to the taxonomic descriptions and describe behavioral features and/or location on the host. Exceptions are the study of Ophiopsyllus reductus parasitizing on shallow-water ophiuroids (Emson & Mladenov, 1987; Emson et al., 1985), the ecological observations of the endoparasitic copepods of the family Corallovexiidae living in stony corals (Butter, 1979; Herriott & Immermann, 1979), the studies of the life cycle and ecology of copepods of the family Thaumatopsyllidae parasitizing living in the ophiuroids at naupliar stages and having non-feeding adult and subadult copepodid stages (Suarez-Morales & Castellanos, 1998; Suarez-Morales & Tovar, 2004; Hendler & Kim, 2010; Ferrari et al., 2010; Ferrari & von Vaupel Klein, 2019), and the experiments on calanoid copepods that were discovered in a host-specific association with only one species of actinarian (Humes & Smith, 1974). Recent field trips to sample Caribbean symbiotic copepods lead to the discovery of new species of highly transformed gall-inducing copepods of the genus Sphaerippe (Lamippidae) causing the Multiple Purple Spot Syndrome previously found in Gorgonia ventalina (Ivanenko et al., 2017; Tracy et al., 2018).
The Caribbean symbiotic copepods are found on 47% species of scleractinians, 9% species of octocorals, 3% of echinoderms and of less than 1% species of sponges (table 7). They are found on 4% of potential hosts of the Caribbean invertebrates which corresponds with previous data on symbiotic copepods (Humes, 1994). The literature and samples analyses indicate a poor knowledge of the diversity and distribution of symbiotic copepods living on different hosts in various ecoregions, and a particularly poor knowledge of copepods living on corals and sponges (Boxshall & Huys, 1994; García-Hernández et al., 2019; present study) with unknown but potentially high impact on their host and reef community (Ho, 2001; Berkenbusch & Rowden, 2003; Hatcher et al., 2012; Shelyakin et al., 2018; Zeppilli et al., 2015, 2018).
EDITOR: R.W.M. VAN SOEST
The preparation of the database, sampling in Cuba and processing of the paper were supported by the Russian Foundation for Basic Research (grant 18-54-34007). The data on samples from St. Eustatius (2015) and Curaçao (2017) were obtained with support of a Temminck-Fellowships to VNI by Naturalis Biodiversity Center. BWH and VNI want to thank staffs of the Caribbean Netherlands Science Institute (CNSI) at St. Eustatius and the Carmabi Research Station at Curaçao for hospitality and assistance. Sorting of samples and identification of copepods were conducted with partial support of the Russian Foundation for Basic Research (grant 18-04-01192). Jaaziel Emmanuel Garcia-Hernandez (University of Puerto Rico at Mayagüez) provided identification of sponges collected during the field trips; Frank Ferrari commented on a draft of the manuscript; Maickel Armenteros (University of Havana) hosted VNI and OAK during the field trip to Cuba.
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