Orbicella annularis (Ellis & Solander, 1786)

Korzhavina, Oksana A., Hoeksema, Bert W. & Ivanenko, Viatcheslav N., 2019, A review of Caribbean Copepoda associated with reef-dwelling cnidarians, echinoderms and sponges, Contributions to Zoology 88 (3), pp. 297-349 : 317-349

publication ID	https://doi.org/ 10.1163/18759866-20191411
persistent identifier	https://treatment.plazi.org/id/039287B9-965C-FFAE-FFE7-FE3FFC27FC01
treatment provided by	Felipe
scientific name	Orbicella annularis (Ellis & Solander, 1786)
status

Treatment

Orbicella annularis (Ellis & Solander, 1786) View in CoL Corallovexia sp. Cor Cur Pseudodiploria clivosa (Ellis & Solander, Corallovexia mediobrachium Stock, 1975 Cor VI

1786) (as Diploria clivosa (Ellis & Solander,

1786))

Pseudodiploria clivosa (Ellis & Solander, Hermacheres diploriae Stock, 1987 Ast Cur

1786)

Pseudodiploria clivosa (Ellis & Solander, Corallovexia mediobrachium Stock, Cor Cur, VI

1786) 1975

Pseudodiploria strigosa (Dana, 1846) Corallovexia brevibrachium Stock, Cor VI

(as Diploria strigosa (Dana, 1846)) 1975

Pseudodiploria strigosa (Dana, 1846) Corallovexia longibrachium Stock, 1975 Cor Cur

Pseudodiploria strigosa (Dana, 1846) Corallovexia mediobrachium Stock, Cor Cur, VI 1975

Pseudodiploria strigosa (Dana, 1846) Corallovexia similis Stock, 1975 Cor VI

Pseudodiploria strigosa (Dana, 1846) Corallovexia sp. Cor VI

Pseudodiploria strigosa (Dana, 1846) Hermacheres diploriae Stock, 1987 Ast Cur Octocorallia

Alcyonacea

Antillogorgia acerosa (Pallas, 1766) Acanthomolgus bilobipes Humes & Rhy Bar, Cur, Jam (as Pseudopterogorgia acerosa (Pallas, 1766)) Stock, 1973

Antillogorgia acerosa (Pallas, 1766) Lamippina aequalis Stock, 1973 Lam Cur Antillogorgia americana (Gmelin, 1791) Acanthomolgus dionyx Stock, 1975 Rhy Cur

(as Pseudopterogorgia americana (Gmelin,

1791))

Antillogorgia sp. (as Pseudopterogorgia sp. ) Lamippina aequalis Stock, 1973 Lam Cur Antillogorgia acerosa var. elastica Biel- Acanthomolgus bilobipes Humes & Rhy PR schowsky, 1929 (as Antillogorgia elastica Stock, 1973

Bielschowsky, 1929)

Stock, 1975a

Herriott & Immermann, 1979

Stock, 1987

Stock, 1975a; Herriott & Immermann, 1979 Herriott & Immermann, 1979

Stock, 1975a

Stock, 1975a; Herriott & Immermann, 1979 Herriott & Immermann, 1979

Herriott & Immermann, 1979

Stock, 1987

Humes & Stock, 1973; Stock, 1975c

Stock, 1973

Stock, 1975c

Stock, 1973

Humes & Stock, 1973

Invertebrate Host (valid name and as Copepod species name Copepod family Site Reference indicated in the original record) abbreviation* abbreviation**

Briareum asbestinum (Pallas, 1766) Enalcyonium variicauda Stock, 1973 Lam PR Briareum asbestinum (Pallas, 1766) Orecturus ortizi Varela & Lalana, 2007 Ast Cub Callogorgia sp. Sphaerippe caligicola Grygier, 1980 Lam Bah Eunicea calyculata (Ellis & Solander, 1786) Acanthomolgus verrucipes Humes, Rhy Ber

1973

Eunicea clavigera Bayer, 1961 Acanthomolgus mononyx Stock, 1975 Rhy Cur Eunicea flexuosa (Lamouroux, 1821) Acanthomolgus affinis Stock, 1975 Rhy Cur

(as Plexaura flexuosa Lamouroux, 1821 )

Eunicea flexuosa (Lamouroux, 1821) Acanthomolgus longidactylus Stock, Rhy Cur

1975

Eunicea laciniata Duchassaing & Acanthomolgus intermedius Stock, Rhy Cur Michelotti, 1860 1975

Eunicea mammosa Lamouroux, 1816 Enalcyonium euniceae Stock, 1973 Lam PR

Eunicea mammosa Lamouroux, 1816 Orecturus antillensis Varela, 2011 Ast Cub Eunicea tourneforti Milne Edwards & Acanthomolgus longifurca Stock, 1975 Rhy Cur Haime, 1857

Gorgonia mariae Bayer, 1961 Acanthomolgus triangulipes Stock, Rhy Cub

1975

Gorgonia ventalina Linnaeus, 1758 Acanthomolgus bayeri Humes, 1973 Rhy Ber Gorgonia ventalina Linnaeus, 1758 Acanthomolgus gorgoniae Humes, Rhy Ber, Cur, SE

1973

Gorgonia ventalina Linnaeus, 1758 Acanthomolgus triangulipes Stock, Rhy Cur, SE, SM

1975

Gorgonia ventalina Linnaeus, 1758 Sphaerippe sp. Lam SE Muricea sp. Acanthomolgus intermedius Stock, Rhy Cub

1975

Stock, 1973

Varela & Lalana, 2007 Grygier, 1980 Humes, 1973

Stock, 1975c

Stock, 1973

Varela, 2011b

Stock, 1975c

Varela et al., 2008

Humes, 1973

Humes, 1973; Stock, 1975c

Stock, 1975c

Ivanenko et al., 2017 Varela et al., 2003 Muricea atlantica (Kukenthal, 1911) Acanthomolgus muriceanus Rhy Ber Humes, 1973 ; Stock,

Humes, 1973 1975c Muricea laxa Verrill, 1864 Acanthomolgus aequiseta Stock, 1975 Rhy Cur Stock, 1975c Placogorgia sp. Linaresia bouligandi Stock, 1979 Lam Flo Stock, 1979 Plexaura sp. Acanthomolgus affinis Stock, 1975 Rhy Cub Varela, 2011a Plexaura homomalla (Esper, 1794) (as Plex- Acanthomolgus affinis Stock, 1975 Rhy Cur Stock, 1975c aura homomalla f. homomalla Esper, 1794 ) Plexaura homomalla (Esper, 1794) Enalcyonium nudum Stock, 1973 Lam PR Stock, 1973 Plexaura homomalla (Esper, 1794) Enalcyonium ramosum Stock, 1973 Lam PR Stock, 1973 Plexaurella dichotoma (Esper, 1791) Acanthomolgus seticornis Stock, 1975 Rhy SM Stock, 1975c Plexaurella nutans (Duchassaing & Enalcyonium sp. Lam Cub Varela et al., 2005b Michelotti, 1860) Pseudoplexaura porosa (Houttuyn, 1772) Acanthomolgus bayeri Humes, 1973 Rhy Ber Humes, 1973 Pseudoplexaura Wright & Studer, 1889 Acanthomolgus bayeri Humes, 1973 Rhy Cub Varela et al., 2003 Thesea Magnippe caputmedusae Stock, 1978 Lam Flo Stock, 1978 Pennatulacea Renilla reniformis (Pallas, 1766) Macrochiron sargassi Sars, 1916 Mac SM Humes & Stock, 1973 Echinodermata Crinoidea Crinoidea Asterocheres crinoidicola Humes, 2000 Ast Jam Kim, 2010 Comatulida Davidaster rubiginosus (Pourtales, 1869) Asterocheres crinoidicola Humes, 2000 Ast Bel, Cub Humes, 2000 ; Varela,

2010 Nemaster grandis Clark, 1909 Asterocheres crinoidicola Humes, 2000 Ast Bel Humes, 2000 Echinoidea Echinoidea Asterocheres unioviger Kim, 2010 Ast Jam Kim, 2010 Camarodonta Echinometra lucunter (Linnaeus, 1758) Chelacheres longipalpus Stock & Ast Bah, Cub, Cur, Jam, MI, Stock & Humes, 1995 ;

Humes, 1995 SM, PR Varela, 2011a

Invertebrate Host (valid name and as Copepod species name Copepod family Site Reference indicated in the original record) abbreviation* abbreviation**

Echinometra lucunter (Linnaeus, 1758) Chelacheres optans Stock & Humes, Ast PR

1995

Echinometra viridis A. Agassiz, 1863 Macrochiron echinicolum Humes & Mac Cur

Stock, 1973

Lytechinus variegatus (Lamarck, 1816) Asterocheres simulans (T. Scott, 1898) Ast Cur

(as Ascomyzon simulans T. Scott, 1898 )

Lytechinus variegatus (Lamarck, 1816) Macrochiron echinicolum Humes & Mac Bon, Cur, Jam, MI, PR Stock, 1973

Tripneustes ventricosus (Lamarck, 1816) Chelacheres longipalpus Stock & Humes, Ast Cur

1995

Tripneustes ventricosus (Lamarck, 1816) Macrochiron echinicolum Humes & Mac Bah, Bar, Cur, Jam, MI Stock, 1973

Cidaroida

Eucidaris tribuloides (Lamarck, 1816) Asterocheres unioviger Kim, 2010 Ast Bah, PR

Clypeasteroida

Clypeaster rosaceus (Linnaeus, 1758) Pseudanthessius pectinifer Stock, Humes Pse Bah, Jam, MI

& Gooding, 1964

Diadematoida

Diadema antillarum Philippi, 1845 Onychocheres alatus Stock & Gooding, Ast Cub, Cur

1986

Spatangoida

Meoma ventricosa (Lamarck, 1816) Meomicola amplectans Stock, Humes & Sync Cur, Jam Gooding, 1963

Meoma ventricosa (Lamarck, 1816) Micropontius glaber Stock, Humes & Mic Jam Gooding, 1963

Stock & Humes, 1995

Humes & Stock, 1973

Stock & Humes, 1995

Humes & Stock, 1973

Stock & Humes, 1995

Humes & Stock, 1973

Kim, 2010

Stock et al., 1963b

Stock & Gooding, 1986; Varela et al., 2005b

Stock et al., 1963b

Stock et al., 1963a Meoma ventricosa (Lamarck, 1816) Nanaspis pollens Stock, Humes & Nan Jam

Gooding, 1962

Meoma ventricosa (Lamarck, 1816) Pseudanthessius exilicornis Stock & Pse Cur

Humes, 1995

Holothuroidea

Actinopyga agassizii (Selenka, 1867) (as Caribulus sp. Sync Bah, Jam

Muelleria agassizi Selenka, 1867 )

Actinopyga agassizii (Selenka, 1867) Caribulus sculptus (Humes, 1969) Sync Bah, Jam

Actinopyga agassizii (Selenka, 1867) Diogenidium nasutum Edwards, 1891 Lic Bah

Actinopyga agassizii (Selenka, 1867) Diogenidium tectum Humes & Ho, 1971 Lic Bah, Jam

Holothuria (Halodeima) grisea Selenka, 1867 Caribulus sculptus (Humes, 1969) Sync Jam

Holothuria (Halodeima) grisea Selenka, 1867 Diogenidium nasutum Edwards, 1891 Lic Jam

Holothuria (Halodeima) mexicana Ludwig , Caribulus sp. Sync Bah, Cur, Jam

1875

Holothuria (Halodeima) mexicana Ludwig , Caribulus sculptus (Humes, 1969) (as Sync Bah, Bon, Cub, Cur, 1875 Scambicornus sculptus Humes, 1969 ) Jam

Holothuria (Halodeima) mexicana Ludwig , Diogenella spinicauda Stock, 1968 Lic Bah, Cur, Jam, MI, PR 1875

Holothuria (Halodeima) mexicana Ludwig , Diogenidium deforme Stock, 1968 Lic Bah, PR

1875

Holothuria (Halodeima) mexicana Ludwig , Diogenidium nasutum Edwards, 1891 Lic Cur, Jam, MI, PR 1875

Holothuria (Halodeima) mexicana Ludwig , Pseudanthessius deficiens Stock, Humes Pse Cur

1875 (as Ludwigothuria mexicana (Ludwig)) & Gooding, 1963

Holothuria (Metriatyla) scabra Jaeger, 1833 Diogenidium nasutum Edwards, 1891 Lic Bah

Holothuria (Platyperona) parvula (Selenka, Nanaspis truncata Stock, Humes & Nan MI, PR

1867) (as Microthele parvula (Selenka)) Gooding, 1962

Holothuria (Selenkothuria) glaberrima Diogenidium deforme Stock, 1968 Lic PR

Selenka, 1867

Stock et al., 1962

Stock & Humes, 1995

Humes, 1969b

Humes, 1969b Hendler & Kim, 2010 Hendler & Kim, 2010 Humes, 1969b Hendler & Kim, 2010 Humes, 1969b

Humes, 1969b; Varela et al., 2003

Stock, 1968; Humes & Ho, 1970

Hendler & Kim, 2010

Stock, 1968; Hendler & Kim, 2010

Stock et al., 1963b

Edwards, 1891

Stock et al., 1962

Stock, 1968

Invertebrate Host (valid name and as Copepod species name Copepod family Site Reference indicated in the original record) abbreviation* abbreviation**

Holothuria (Semperothuria) surinamensis Diogenella seticauda Stock, 1968 Lic MI, PR

Ludwig, 1875

Holothuria (Semperothuria) surinamensis Nanaspis pollens Stock, Humes & Nan MI

Ludwig, 1875 (as Halodeima surinamensis Gooding, 1962

(Ludwig))

Holothuria (Thymiosycia) arenicola Semper , Diogenella deichmannae Humes & Lic Bar

1868 Ho, 1970

Holothuria (Thymiosycia) arenicola Semper , Diogenella impar Humes & Ho, 1970 Lic Bar

1868 (as Brandtothuria arenicola (Semper,

1868))

Holothuria (Thymiosycia) arenicola Semper , Diogenidium deforme Stock, 1968 Lic Bar

1868

Holothuria (Thymiosycia) arenicola Semper , Diogenella seticauda Stock, 1968 Lic MI

1868

Holothuria (Thymiosycia) arenicola Semper , Nanaspis pollens Stock, Humes & Nan Jam

1868 Gooding, 1962

Holothuria (Thymiosycia) arenicola Semper , Nanaspis truncata Stock, Humes & Nan MI

1868 Gooding, 1962

Holothuria (Thymiosycia) impatiens Diogenella seticauda Stock, 1968 Lic PR

(Forsskal, 1775)

Synallactida

Isostichopus badionotus (Selenka, 1867) Caribulus sp. Sync Bah, Bar, Jam Isostichopus badionotus (Selenka, 1867) Caribulus sculptus (Humes, 1969) Sync Bah, Bar, Jam, MI, PR Isostichopus badionotus (Selenka, 1867) Diogenidium spinulosum Stock, 1968 Lic Jam, PR

Stock, 1968; Humes & Ho, 1970

Stock et al., 1962

Humes & Ho, 1970

Hendler & Kim, 2010

Humes & Ho, 1970

Stock et al., 1962

Stock, 1968

Humes, 1969b Humes, 1969b

Stock, 1968; Hendler & Kim, 2010

Isostichopus badionotus (Selenka, 1867) Nanaspis exigua Stock, Humes & Nan Jam

Gooding, 1962

Isostichopus badionotus (Selenka, 1867) Nanaspis media Stock, Humes & Nan MI, PR Gooding, 1962

Isostichopus badionotus (Selenka, 1867) Nanaspis pollens Stock, Humes & Nan Bah, Jam Gooding, 1962

Ophiuroidea

Euryalida

Astrophyton muricatum (Lamarck, 1816) Critomolgus Humes & Stock, 1983 Rhy Cub

Astrophyton muricatum (Lamarck, 1816) Critomolgus astrophyticus (Humes & Rhy Bar, Jam, MI, PR Stock, 1973) (as Doridicola astrophyticus Humes & Stock, 1973 )

Ophiurida

Ophiuroida Caribeopsyllus sp. A Tha SE

Amphioplus sp. Parophiopsyllus ligatus Humes & Can FK

Hendler, 1972

Amphioplus sp. Presynaptiphilus amphiopli Humes & Synp FK

Hendler, 1972

Ophiocoma echinata (Lamarck, 1816) Ophiopsyllus reductus Stock, Humes & Can Bel, Cur Gooding, 1963

Ophiocoma pumila Lutken, 1856 Ophiopsyllus latus Humes & Hendler, Can Bel, FK

1999

Ophiocoma wendtii Muller & Troschel, 1842 Hemicyclops columnaris Humes, 1984 Cla Bah

(as Ophiocoma riisei Lutken, 1856 )

Ophiocomella ophiactoides (Clark, 1900) Ophiopsyllus latus Humes & Hendler, Can Bel

1999

Ophiocomella ophiactoides (Clark, 1900) Ophiopsyllus reductus Stock, Humes & Can Bel, Jam Gooding, 1963

Stock et al., 1962

Varela et al., 2008 Humes & Stock, 1973

Ivanenko, unpublished Humes & Hendler, 1972

Humes & Hendler, 1972

Humes & Hendler, 1999; Stock et al., 1963a

Humes & Hendler, 1999

Kim, 2009

Humes & Hendler, 1999

Emson & Mladenov, 1987; Emson et al., 1985

Invertebrate Host (valid name and as Copepod species name Copepod family Site Reference indicated in the original record) abbreviation* abbreviation**

Ophioderma brevispina (Say, 1825) Pseudanthessius deficiens Stock, Humes Pse Bel

(as Ophioderma brevispinum (Say, 1825)) & Gooding, 1963

Ophioderma cinerea Muller & Troschel , Pseudanthessius deficiens Stock, Humes Pse Bel, Cur, MI, SM 1842 (as Ophioderma cinereum Muller & & Gooding, 1963

Troschel, 1842)

Ophiomyxa flaccida (Say, 1825) Ophiurocheres bellulus Humes, 1998 Ast MI

Ophiothrix (Acanthophiothrix) suensoni Collocheres lunulifer Humes, 1998 Ast Bar

Lutken, 1856

Ophiothrix (Ophiothrix) angulata (Say, 1825) Caribeopsyllus sp. A Tha Bel

Ophiothrix (Ophiothrix) angulata (Say, 1825) Caribeopsyllus chawayi Suarez-Morales, Tha Bel

In: Suarez-Morales & Castellanos, 1998

Ophiothrix (Ophiothrix) angulata (Say, 1825) Collocheres lunulifer Humes, 1998 Ast Bar

Ophiothrix (Ophiothrix) oerstedii Lutken , Caribeopsyllus chawayi Suarez-Morales, Tha Bel

1856 In: Suarez-Morales & Castellanos, 1998

Porifera

Porifera Asterocheres bahamensis Kim, 2010 Ast Bah

Porifera Asterocheres oricurvus Kim, 2010 Ast Jam

Porifera Asterocheres peniculatus Kim, 2010 Ast Bah

Porifera Asterocheres plumosus Kim, 2010 Ast Bah

Porifera Asterocheres trisetatus Kim, 2010 Ast Bah

Porifera Eupolymniphilus occidentalis Kim, 2009 Sab Jam

Porifera Hemicyclops columnaris Humes, 1984 Cla Bah

Porifera Hetairosynella aculeata Kim, 2010 Ast Bah

Porifera Hetairosynella angulata Kim, 2010 Ast Jam

Porifera Hetairosynella bifurcata Kim, 2010 Ast Jam

Humes & Hendler, 1999

Stock et al., 1963b; Humes & Hendler, 1999

Humes, 1998 Humes, 1998

Hendler & Kim, 2010 Hendler & Kim, 2010

Humes, 1998 Hendler & Kim, 2010

Kim, 2010

Kim, 2009

Kim, 2010

Porifera Kimcheres fastigatus (Kim, 2010) (as Ast Bar Asterocheres fastigatus Kim, 2010 )

Porifera Pseudanthessius acutus Kim, 2009 Pse Jam

Porifera Stenomyzon edentatum Kim, 2010 Ast PR

Calcarea

Calcinea

Clathrinida

Clathrina lutea Azevedo, Padua, Moraes , Copepoda PR

Rossi, Muricy & Klautau, 2017

Demospongiae

Heteroscleromorpha

Agelasida

Agelas sp. Asterocheres reginae Boxshall & Huys, Ast Cub 1994

Agelas clathrodes (Schmidt, 1870) Asterocheres reginae Boxshall & Huys, Ast Bel 1994

Agelas dilatata Duchassaing & Michelotti , Asterocheres cubensis Varela, 2010 Ast Cub

1864

Agelas wiedenmayeri Alcolado, 1984 Asterocheres fernandezmilerai Varela, Ast Cub 2010

Axinellida

Ptilocaulis walpersii (Duchassaing & Asterocheres garridoi Varela, Ortiz & Ast Cub

Michelotti, 1864) Lalana, 2007

Haplosclerida

Callyspongia sp. Asterocheres antillensis Varela, 2010 Ast Cub

Callyspongia vaginalis (Lamarck, 1814) Asterocheres Boeck, 1859 Ast Cub

Callyspongia vaginalis (Lamarck, 1814) Asterocheres espinosai Varela, Ortiz & Ast Cub Lalana, 2007

Callyspongia vaginalis (Lamarck, 1814) Neoasterocheres humesi (Varela, 2012) Ast Cub

Kim, 2010

Kim, 2009

Kim, 2010

Garcia-Hernandez et al., 2019

Varela et al., 2008

Boxshall & Huys, 1994

Varela, 2010b

Varela et al., 2007

Varela, 2010

Varela et al., 2005b Varela et al., 2007a

Varela, 2012 coral) ( fig.1a View FIGURE 1 ) (Humes, 1984; Stock, 1992a; Kim, Southern Gulf of Mexico ( table 6, figs. 4–7 View FIGURE 4 View FIGURE 5 View FIGURE 6 View FIGURE 7 ; 2009). All other species of symbiotic cope- Spalding et al., 2007; Hoeksema et al., 2017a). pods are found in the Caribbean only, which Eight records are known for Bermuda: four may be the result of high endemism of their species of poecilostomatoid cyclopoids rephost species (Miloslavich et al., 2010; Soest resenting genus Acanthomolgus and the si- et al., 2012; Zea et al., 2014; Ivanenko, 2016). phonostomatoid Ophiopsyllus reductus were The copepods were collected by washing found associated with alcyonaceans and an of the hosts in seawater or tap water (Butter, ophiuroid, respectively (Stock et al., 1963a; 1979; Garcia-Hernandez et al., 2017), a solu- Humes, 1973). Only one record is reported tion of formalin (Varela & Lalana, 2007; Varela for the Southwestern Caribbean: the cala- et al., 2003, 2005a, b, 2007a, b, 2008; Varela, noid Ridgewayia fosshageni aggregating on 2010a, b, 2011a, b, 2012), a solution of ethanol the actinairian Bartholomea annulata . Only (Stock et al., 1962, 1963a, b, Humes, 1969a, 1998, Aspidomolgus stoichactinus living on the ac- 2000; Humes & Stock, 1973; Stock, 1975a, b, d; tiniarian Stichodactyla helianthus and the Herriott & Immermann, 1979; Stock & Humes, corallimorpharian Corynactis denticulosa , 1995) or a solution of magnesium-chloride recorded as Homostichanthus denticulosus , is (Stock & Humes, 1995), dissecting of the host’s found in five ecoregions (Humes, 1969a; Stock, tissues or galls (see Stock et al., 1962; Humes & 1975b). Five species of copepods are found in Hendler, 1972, 1999; Humes & Goenaga, 1978; four ecoregions, viz. Caribulus sculptus living Stock, 1978; Grygier, 1980; Emson et al., 1985; on holothurians, Chelacheres longipalpus and Emson & Mladenov, 1987; Hendler & Kim, Macrochiron echinicolum ( fig. 1d View FIGURE 1 ) found on sea 2010; Ivanenko et al., 2017), by a suction device urchins, Ophiopsyllus reductus living on ophi- (Humes & Stock, 1973) or by dissolving soft tis- uroids. Seventeen and 87 species of copepods sues of host corals with bleach (Stock 1975a, are recorded found in only two and one ecore- 1989). Most of the host invertebrates were col- gions, respectively ( table 6). lected by SCUBA living down to 41 m depth. The data show that the three most inten- The only exceptions are the three of eight spe- sively explored ecoregions are the Bahamian, cies of the Caribbean copepods of the family Greater Antilles and Southern Caribbean, Lamippidae tentatively included in the da- with studies centered at Curaçao (123 records, tabase found in galls or tissue of octocorals 36 species of hosts, 49 species of copepods), collected by a submersible away from reefs at Puerto Rico (105, 22, 27) and the Bahamas (57, depths of 55–330 m ( fig. 2 a–d View FIGURE 2 ) (Stock, 1978, 11, 19). The mosaic data show poor knowledge 1979; Grygier, 1980). It is noteworthy that there of most ecoregions as well as and many host are no data on symbiotic copepods associated taxa. This current state of the knowledge limwith reef-dwelling sponges, echinoderms and its analysis of the distribution of symbiotic cocorals living at mesophotic depths; studies on pepods in the whole Caribbean. Well planned reef communities and coral-associated fauna studies of different Caribbean regions and the from mesophotic depths seems to be an im- application of modern methods of integrative portant task that has just started (Bongaerts taxonomy are needed to carry out such analy- et al. 2010, 2015; van der Meij et al., 2015; Hoek- ses (DeBiasse et al., 2016; Jossart et al., 2017; sema et al., 2017c; García-Hernández et al., Ivanenko et al., 2018). 2018; Veglia et al., 2018). A comparison of taxonomic names from Symbiotic copepods are reported from literature sources with their current nomeneight out of ten ecoregions of the Greater clature revealed Downloaded name from changes Brill.com for 12/12/2023 29 (of 80) 03:03:35PM Caribbean, but none from the Northern via Open and Access. This species is an open and access 12 (of article 58) genera distributed of under the hosts the terms of the CC-BY 4.0 License.

https://creativecommons.org/licenses/by/4.0/

Host family Number of copepod Number of copepod records species

Echinodermata

Holothuriidae 75 Stichopodidae 35 Ophiocomidae 29 Ophiotrichidae 19 Toxopneustidae 18 Echinometridae 17 Gorgonocephalidae 13 Ophiodermatidae 10 Amphiuridae 9 Brissidae 9 Clypeasteridae 6 Diadematidae 4 Comatulidae 3 Cidaridae 2 Ophiomyxidae 1 Cnidaria

Faviidae 47 Plexauridae 29 Stichodactylidae 22 Gorgoniidae 21 Meandrinidae 20 Actiniidae 16 Montastraeidae 13 Merulinidae 7 Acroporidae 5 Corallimorphidae 4 Briareidae 4 Aiptasiidae 2 Antipathidae 2 Ricordeidae 2 Renillidae 1 Phymanthidae 1 Primnoidae 1 Porifera

Clathrinidae 42 Chondrillidae 12 12 5 3 2 3 3 1 1 2 4 1 1 1 1 1

12 16 2 6 5 3 6 2 2 2 2 1 1 1 1 1 1

1 2 (WoRMS, 2019). The taxonomic names are 41 records for which the hosts are identified changed for nine (of 115) species and six (of 47) only to taxonomic categories such as phygenera of the copepods. There are six records lum, order or subclass. There are 81 records of symbiotic copepods identified to genus of copepods found on sponges, but hosts of ( Asterocheres , Corallovexia , Corallonoxia , 14 of them are defined only to phylum (Kim, Critomolgus , Enalcyonium , Sphaerippe ). These 2009, 2010). The absence of precise identifitaxa are included in; among 16 hosts (for 18 cations and the necessity of linking outdated records) that have no identification at species host names with valid ones show the need for level; of these one is assigned to a via phylum Open, specimen Access. This is an open Downloaded collections access from article of not distributed Brill.com only copepods 12/12/2023 under 03 the terms:03:35PM three to a class and 12 to a genus. There are but also of their invertebrate of hosts the, CC-BY as well 4.0 as License. https://creativecommons.org/licenses/by/4.0/

Copepod family Host family Host class or type

Asterocheridae Actiniidae Ant Agelasidae Dem Axinellidae Dem Briareidae Ant Callyspongiidae Dem Cidaridae Ech Comatulidae Cri Diadematidae Ech Echinometridae Ech Iotrochotidae Dem Meandrinidae Ant Merulinidae Ant Montastraeidae Ant Niphatidae Dem Ophiomyxidae Oph Ophiotrichidae Oph Phymanthidae Ant Plexauridae Ant Ricordeidae Ant Stichodactylidae Ant Toxopneustidae Ech

Cancerillidae Amphiuridae Oph Ophiocomidae Oph

Clausidiidae Ophiocomidae Oph

Corallovexiidae Acroporidae Ant Meandrinidae Ant Merulinidae Ant Montastraeidae Ant Faviidae Ant

Entomolepididae Chondrillidae Dem

Lamippidae Briareidae Ant Gorgoniidae Ant Plexauridae Ant Primnoidae Ant

Lichomolgidae Holothuriidae Hol Stichopodidae Hol

Macrochironidae Echinometridae Ech Renillidae Ant Toxopneustidae Ech

Micropontiidae Brissidae Downloaded from Brill.com Ech 12/12/2023 03:03:35PM via Open Access. This is an open access article distributed under the terms of the CC-BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

* Abbreviations: Ant – Anthozoa, Cri – Crinoidea, Dem – Demospongiae Ech – Echinoidea, Hol – Holothuroidea,

Hom – Homoscleromorpha, Oph – Ophiuroidea, Po – Porifera.

morphological and molecular studies of this dae and Meandrinidae (updated classification material (Rocha et al., 2014). The DNA-barcod- in Hoeksema & Cairns, 2019), respectively; 36

ing of the hosts, photographing of hosts alive and 16 of these records pertain to the endounderwater, and photographing of host skel- parasitic copepod symbionts belonging to the etons along with basic locality data are impor- family Corallovexiidae . Most records from tant for both identification and maintaining holothurians from the families Holothuriinformation about each copepod host and the idae and Stichopodidae (75 and 35 records), establishment of base line information about from ophiuroids the families Ophiocomi-

their distributions (Hoeksema et al., 2011). dae and Ophiotrichidae (29 and 19 records)

In total, there are 253, 197 and 81 records of are most common, from sea cucumbers the copepods found associated with echinoderms, family Stichopodidae (35 records) is well cnidarians and sponges,respectively( figs.1–3 View FIGURE 1 View FIGURE 2 View FIGURE 3 ). represented, alcyonaceans the family Plex- Forty-seven and 20 records of copepods are auridae (29), and corallimorpharians (four linked to the scleractinian coral families via Open Favii- Access records. This is)an also open Downloaded are access represented from article Brill. distributed com(table 12/12 3 /2023) under. Many 03 the:03:35 terms PM of the CC-BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

Copepod species / Ecoregion Bahamian Bermuda Eastern Floridian Greater Southern Southwestern Western Caribbean Antilles Caribbean Caribbean Caribbean

Acanthomolgus aequiseta Stock, 1975

Acanthomolgus affinis Stock, 1975

Acanthomolgus bayeri Humes, 1973

Acanthomolgus bilobipes Humes & Stock, 1973 Acanthomolgus dionyx Stock, 1975

Acanthomolgus gorgoniae Humes, 1973 Acanthomolgus intermedius Stock, 1975 Acanthomolgus longidactylus Stock, 1975 Acanthomolgus longifurca Stock, 1975

Acanthomolgus mononyx Stock, 1975

Acanthomolgus muriceanus Humes, 1973 Acanthomolgus seticornis Stock, 1975

Acanthomolgus triangulipes Stock, 1975 Acanthomolgus verrucipes Humes, 1973

Aspidomolgus stoichactinus Humes, 1969 × Asterocheres sp.

Asterocheres antillensis Varela, 2010

Asterocheres bahamensis Kim, 2010 × Asterocheres crinoidicola Humes, 2000

Asterocheres cubensis Varela, 2010

Asterocheres espinosai Varela, Ortiz & Lalana, 2007 Asterocheres fernandezmilerai Varela, 2010 Asterocheres garridoi Varela et al., 2007

Asterocheres kimi Varela, 2012

Asterocheres lalanai Varela, 2013

× × × × ×

× ×

× × × × × × ×

× ×

× × × × × × ×

× ×

Copepod species / Ecoregion Bahamian Bermuda Eastern Floridian Greater Southern Southwestern Western Caribbean Antilles Caribbean Caribbean Caribbean

Asterocheres maxillatus Stock, 1987

Asterocheres reginae Boxshall & Huys, 1994 Asterocheres oricurvus Kim, 2010

Asterocheres peniculatus Kim, 2010 × Asterocheres plumosus Kim, 2010 × Asterocheres reginae Boxshall & Huys, 1994 Asterocheres simulans (T. Scott, 1898)

Asterocheres trisetatus Kim, 2010 × Asterocheres unioviger Kim, 2010 × Asteropontella foliata Stock, 1989

Asteropontius capillatus Kim, 2010

Asteropontius iuxtus Stock, 1989

Asteropontius longipalpus Stock, 1975

Asteropontius mycetophylliae Varela, Ortiz & Lalana, 2005 , 2005

Asteropontius parvipalpus Stock, 1975 × Asteropontius proximus Stock, 1987

Asteropontius ungellatus Stock, 1975

Asteropontopsis faviae Stock, 1987

Calonastes imparipes Humes & Goenaga, 1978 Caribeopsyllus sp. A

Caribeopsyllus chawayi Suárez-Morales, 1998 Caribulus sculptus (Humes, 1969) × Chelacheres longipalpus Stock & Humes, 1995 × Chelacheres optans Stock & Humes, 1995

× ×

× × ×

× ×

× × ×

× ×

Collocheres lunulifer Humes, 1998

Corallonoxia baki Stock, 1975

Corallonoxia longicauda Stock, 1975

Corallovexia brevibrachium Stock, 1975

Corallovexia dorsospinosa minor Stock, 1975 Corallovexia dorsospinosa Stock, 1975

Corallovexia kristenseni Stock, 1975

Corallovexia longibrachium Stock, 1975

Corallovexia mediobrachium Stock, 1975

Corallovexia mixtibrachium Stock, 1975

Corallovexia similis Stock, 1975

Corallovexia ventrospinosa Stock, 1975

Critomolgus sp.

Critomolgus astrophyticus (Humes & Stock, 1973) Critomolgus titillans (Humes, 1982)

Diogenella deichmannae Humes & Ho, 1970 Diogenella impar Humes & Ho, 1970

Diogenella seticauda Stock, 1968

Diogenella spinicauda Stock, 1968 × Diogenidium deforme Stock, 1968 × Diogenidium nasutum Edwards, 1891 × Diogenidium spinulosum Stock, 1968

Diogenidium tectum Humes & Ho, 1971 × Enalcyonium sp.

Enalcyonium euniceae Stock, 1973

Enalcyonium nudum Stock, 1973

Enalcyonium ramosum Stock, 1973

Enalcyonium variicauda Stock, 1973

Eupolymniphilus occidentalis Kim, 2009

× × ×

× × × × × × × × × × ×

Copepod species / Ecoregion Bahamian Bermuda Eastern Floridian Greater Southern Southwestern Western Caribbean Antilles Caribbean Caribbean Caribbean

Hemicyclops columnaris Humes, 1984 × Hermacheres diploriae Stock, 1987

Hermacheres montastreae Stock, 1987

Hetairosynella aculeata Kim, 2010 × Hetairosynella angulata Kim, 2010

Hetairosynella bifurcata Kim, 2010

Kimcheres fastigatus (Kim, 2010)

Lamippina aequalis Stock, 1973

Linaresia bouligandi Stock, 1979

Macrochiron echinicolum Humes & Stock, 1973 × Macrochiron sargassi Sars, 1916

Magnippe caputmedusae Stock, 1978

Meandromyzon coronatum Stock, 1989

Meomicola amplectans Stock, Humes & Gooding ,

1963

Micropontius glaber Stock, Humes & Gooding, 1963 Nanaspis exigua Stock, Humes & Gooding, 1962 Nanaspis media Stock, Humes & Gooding, 1962 Nanaspis pollens Stock, Humes & Gooding, 1962 × Nanaspis truncata Stock, Humes & Gooding, 1962 Neoasterocheres humesi (Varela, 2012)

Onychocheres alatus Stock & Gooding, 1986 Ophiopsyllus latus Humes & Hendler, 1999 Ophiopsyllus reductus Stock, Humes & Gooding ,

1963

× × × ×

× × ×

× × × × × × × ×

× ×

× × Ophiurocheres bellulus Humes, 1998 ×

Orecturus antillensis Varela, 2011 ×

Orecturus ortizi Varela & Lalana, 2007 ×

Paramolgus antillianus Stock, 1975 ×

Parmulella emarginata Stock, 1992 ×

Parmulodes verrucosa Wilson C.B., 1944 × × × Parophiopsyllus ligatus Humes & Hendler, 1972 ×

Peltomyzon rostratum Stock, 1975 ×

Presynaptiphilus amphiopli Humes & Hendler, 1972 ×

Pseudanthessius acutus Kim, 2009 ×

Pseudanthessius deficiens Stock, Humes & Gooding , × × × 1963

Pseudanthessius exilicornis Stock & Humes, 1995 ×

Pseudanthessius pectinifer Stock, Humes & ×

Gooding, 1964

Pseudanthessius pectinifer Stock, Humes & ×

Gooding, 1964

Ridgewayia fosshageni Humes & Smith, 1974 ×

Scottocheres elongatus (Scott T. & Scott A., 1894) ×

Setacheres paraboecki (Johnsson, 1998) ×

Sphaerippe caligicola Grygier, 1980 ×

Sphaerippe sp. × Stenomyzon edentatum Kim, 2010 ×

1 – Ivanenko, 2016, 2 – Bayer, 1961, 3 – Alvarado, 2011, 4 – Pawson et al., 2009, 5 – Perez et al., 2017

(25 of 81) records of copepods found on un- families of stony corals only. Three families identified sponges. ( Lamippidae , Pseudanthessiidae , and Synap- Cyclopoida , representing mainly poecilo- tiphilidae) are found associated with four host stomatoids, with 317 records for 59 species is families; Macrochironidae and Nanaspididae the most diverse order of copepods found in are found with three host families; Cancerilsymbiosis with corals, sponges and echino- lidae and Lichomolgidae are found with two derms; Siphonostomatoida with 170 records host families; seven families ( Clausidiidae ,

of 55 species is the next ( figs. 1–3 View FIGURE 1 View FIGURE 2 View FIGURE 3 , table 4). The Entomolepididae , Micropontiidae, Pseudoorder Calanoida is represented by the only cyclopidae, Sabelliphilidae , Synaptiphilidae , known symbiotic calanoid copepod Ridgeway - and Thaumatopsyllidae ) are restricted to only ia fosshageni found associated with an actini- one family of invertebrate hosts ( table 5). The arian at the Atlantic coast of Panama (Humes remarkable absence on Caribbean host cor-

& Smith, 1974). The absence in the literature of als for copepods of the families Anchimolgi-

any records of symbiotic harpacticoids is con- dae (124 species in 32 genera) and Xarifidae tradicted by the results recently obtained from (96 species in 6 genera) so far only found on samples of undescribed harpacticoids repre- Indo-Pacific scleractinians (Stock, 1988), is senting the family Laophontidae (see Yeom confirmed by literature data and results of our et al., 2018). Siphonostomatoid copepods of recent sampling (Cheng et al., 2016; Hoekse-

the diverse but poorly investigated family As- ma et al., 2017b; table 1). To explain this distriterocheridae and poecilostomatoid cyclopoids bution a study of phylogenetic relationships representing endoparasitic Corallovexiidae of Corallovexiidae with other families of the have the greatest diversity of associations and order and the additional search for endopar-

the highest number of host families ( table 5). asitic copepods living in Indo-Pacific stony Asterocheridae are found living on inverte- corals is needed. This proposed study should brates belonging to 22 families of cnidarians, includemethodsthatenabledissolutiononlyof echinoderms and sponges; Rhynchomolgidae soft coral tissue while the chitinous exoskel-

are recorded from eight families of anthozoans etons of microscopic crustaceans to remain and echinoderms; Corallovexiidae from five intact. Downloaded from Brill.com 12/12/2023 03:03:35PM via Open Access. This is an open access article distributed under the terms of the CC-BY 4.0 License. https://creativecommons.org/licenses/by/4.0/ Fifty of 115 species of symbiotic copepods six. The sea cucumber Holothuria arenicola are mentioned in literature only once; 83 of hosts six species of copepods ( table 2). Three 115 species of copepods are reported from only scleractinian and two holoturian species host one species or one genus of the host. Only 13 five copepod species. The sea urchin Meoma species are reported in symbiosis with repre- ventricosa and the sea cucumber Actinopyga sentatives of different families. Four species agassizii host four copepod species; three cor-

of copepods, the poecilostomatoids Eupolym- als and one sponge host three species each; niphilus occidentalis ( fig. 1g View FIGURE 1 ), Hemicyclops co- 18 host species have been recorded with two lumnaris, Pseudanthessius deficiens ( fig. 1e View FIGURE 1 ) associated species of symbiotic copepods. Nu- and the siphonostomatoid Nanaspis pollens merous findings of different species of symbi- (fig, 3e) are found in symbiosis with represen- otic copepods on the same hosts as well as the tatives of different classes. Of these species presence on these hosts of other symbionts only Hemicyclops columnaris is found associ- (shrimps, polychaetes, decapods, amphipods, ated with invertebrates representing differ- fish etc.) shows little knowledge of species reent phyla: echinoderms, corals, sponges and lationships in the symbiotic complexes (Stella arthropods. The finding on sponge and on a et al., 2011; Hoeksema et al., 2012).

compound ascidian of the copepod Eupolym- Copepod crustaceans living in symbiosis niphilus occidentalis (family Sabelliphilidae ) with the Caribbean reef invertebrates express typically living on tubicolous polychaetes re- diverse body shapes (cyclopiform, spherical, quires additional confirmation (Kim, 2009). flattened etc.), remarkably different body siz- Only two species of copepods are reported liv- es ranging from 0.25 mm (such as Collocheres ing on different classes: Pseudanthessius defi- lunulifer ) to 4.75 mm (such as Corallovexia ciens is found on three species of echinoderms ventrospinosa ), and various types of feeding to holothurians and echinoids; Nanaspis pol- apparatuses as well as host utilizations. Anallens is found on holothurians and ophiurioids. ysis of literature and sorting of samples shows Thus, most species of symbiotic copepods are a different, and sometimes very large number found associated with invertebrate hosts be- of individual copepods living on a single host.

longing to a single genus or only one family. The most numerous are the poorly studied These finding suggest the need to study the ef- asterocherid copepods living on and in difect of host specificity more extensively. Simi- verse sponges: in one sample on one sponge lar studies of host switching events may show thousands of individual copepods belonging that this phenomenon has occurred several to several species (Schirl, 1973; Ivanenko & times during in the evolution of symbiotic co- Smurov, 1997; Ivanenko, 1998; Klinger et al., pepods, as it has among decapod crustacean 2019; present study). The diversity, host specitaxa (Fransen & Hoeksema, 2014; Brinkmann ficity and phylogenetic relationships of these

& Fransen, 2016; García-Hernández et al., copepods with other siphonostomatoid cope- 2016; Horká et al., 2016; Hoeksema & Fransen, pods, especially species found in association 2017; Hoeksema et al., 2018). The very nature with Caribbean stony corals are among the of the specificity of copepods to the host or to most interesting unexplored topics in coral the group of hosts requires a thorough sam- reef ecology.

pling program as well as the use of molecular The symbiotic copepods are characterized methods (Ivanenko et al., 2018). by different ways of attachment to their host The number of copepod species found (loosely associated with or aggregating on on a single host species varies from one to the host’s Downloaded surface, from tightly Brill.com attached12/12/to 2023the03host:03:35PM via Open Access. This is an open access article distributed under the terms of the CC-BY 4.0 License. https://creativecommons.org/licenses/by/4.0/ by claw-like appendages, inducing a gall-like species of octocorals, 3% of echinoderms and structure, or residing inside of intestine, body of less than 1% species of sponges ( table 7).

cavity, or the host tissues). They also show They are found on 4% of potential hosts marked variation in the number of embryos of the Caribbean invertebrates which corpresent in the egg-sacs (from one embryo, as responds with previous data on symbiotic in Peltomyzon rostratum , to 50 embryos, as in copepods (Humes, 1994). The literature and Caribulus sculptus ) or numerous embryos laid samples analyses indicate a poor knowledge in copepod-induced galls. The symbiotic co- of the diversity and distribution of symbiotic pepods have different types of lecithotrophic copepods living on different hosts in various and planktotrophic naupliar stages, some of ecoregions, and a particularly poor knowlwhich, like Thaumatopsyllidae , are parasitic edge of copepods living on corals and sponges in the stomach of its host brittle star ( fig. 2e View FIGURE 2 ; (Boxshall & Huys, 1994; García-Hernández Hendler & Kim, 2010). et al., 2019; present study) with unknown but Most of the ecological observations of the potentially high impact on their host and reef Caribbean symbiotic copepods are short com- community (Ho, 2001; Berkenbusch & Rowments added to the taxonomic descriptions den, 2003; Hatcher et al., 2012; Shelyakin et al.,

and describe behavioral features and/or loca- 2018; Zeppilli et al., 2015, 2018).

tion on the host. Exceptions are the study of

Ophiopsyllus reductus parasitizing on shallowwater ophiuroids (Emson & Mladenov, 1987; Acknowledgements

Emson et al., 1985), the ecological observations of the endoparasitic copepods of the family The preparation of the database, sampling in Corallovexiidae living in stony corals (Butter, Cuba and processing of the paper were sup-

1979; Herriott & Immermann, 1979), the stud- ported by the Russian Foundation for Basic ies of the life cycle and ecology of copepods Research (grant 18-54-34007). The data on of the family Thaumatopsyllidae parasitizing samples from St. Eustatius (2015) and Curaliving in the ophiuroids at naupliar stages and çao (2017) were obtained with support of a having non-feeding adult and subadult cope- Temminck-Fellowships to VNI by Naturalis podid stages (Suarez-Morales & Castellanos, Biodiversity Center. BWH and VNI want to 1998; Suarez-Morales & Tovar, 2004; Hendler thank staffs of the Caribbean Netherlands Sci-

& Kim, 2010; Ferrari et al., 2010; Ferrari & von ence Institute (CNSI) at St. Eustatius and the Vaupel Klein, 2019), and the experiments on Carmabi Research Station at Curaçao for hoscalanoid copepods that were discovered in a pitality and assistance. Sorting of samples and host-specific association with only one spe- identification of copepods were conducted cies of actinarian (Humes & Smith, 1974). Re- with partial support of the Russian Founda-

cent field trips to sample Caribbean symbiotic tion for Basic Research (grant 18-04-01192).

copepods lead to the discovery of new species Jaaziel Emmanuel Garcia-Hernandez (Uni-

of highly transformed gall-inducing copepods versity of Puerto Rico at Mayagüez) provided of the genus Sphaerippe ( Lamippidae ) caus- identification of sponges collected during ing the Multiple Purple Spot Syndrome previ- the field trips; Frank Ferrari commented on a ously found in Gorgonia ventalina (Ivanenko draft of the manuscript; Maickel Armenteros et al., 2017; Tracy et al., 2018). (University of Havana) hosted VNI and OAK

The Caribbean symbiotic copepods are during the field trip to Cuba.

found on 47% species of scleractinians, 9% Downloaded from Brill.com 12/12/2023 03:03:35PM via Open Access. This is an open access article distributed under the terms of the CC-BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

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RECEIVED: 29 APRIL 2019 | REVISED AND

ACCEPTED: 2 JULY 2019

EDITOR: R.W.M. VAN SOEST

Kingdom	Animalia
Phylum	Cnidaria
Class	Anthozoa
Order	Scleractinia
Family	Merulinidae
Genus	Orbicella