Parasitology Research

, 105:479

Diversity and ecological remarks of ectocommensals and ectoparasites (Annelida, Crustacea, Mollusca) of echinoids (Echinoidea: Mellitidae) in the Sea of Cortez, Mexico

  • Ernesto Campos
  • Alma Rosa de Campos
  • Jesús Angel de León-González
Original Paper

DOI: 10.1007/s00436-009-1419-8

Cite this article as:
Campos, E., de Campos, A.R. & de León-González, J.A. Parasitol Res (2009) 105: 479. doi:10.1007/s00436-009-1419-8

Abstract

The diversity of symbiotic invertebrates on intertidal and shallow water echinoids of the northwestern Gulf of California was studied. Five ectosymbionts were found: three pinnotherid crabs, Dissodactylus lockingtoni Glassell (1935), Dissodactylus nitidus Smith (1870), and Dissodactylus xanthusi Glassell (1936); one eulimid gastropod, Turveria encopendema Berry (1956); and one polychaete, Struwela sp. We discovered seasonal fluctuation in D. nitidus Smith (1870) and D. xanthusi Glassell (1936), which result in these species being undetectable during the winter season when the temperature in the head of the Gulf of California drops to 14–18°C; the rest of the species are permanent residents in this area. An updated list of all external macrosymbionts of echinoids of the Mexican Pacific is presented.

Introduction

The Sea of Cortez (Gulf of California) is considered one of the five more diverse seas of the world with more than 5,000 species of macroinvertebrates described, largely free-living forms (see, Brusca and Findley 2005). Ongoing studies on the diversity of symbiotic invertebrates of the northwestern Gulf of California permitted us to collect intertidal and shallow water echinoid species of the genera Mellita and Encope to record their ectocommensal and ectoparasite invertebrates. A total of five species were found living on the sand dollar tests: three pinnotherid crabs of the genus Dissodactylus Smith 1870; Dissodactylus lockingtoni Glassell 1935, Dissodactylus nitidus Smith 1870, and Dissodactylus xanthusi Glassell 1936; one eulimid gastropod, Turveria encopendema Berry 1956; and one polychaete, Struwela sp. Each species has been illustrated, taxonomically diagnosed, and some remarks on the host–symbiont relationship are included. In addition, we have compiled a complete list of all ectosymbionts of echinoids of the Mexican Pacific.

Materials and methods

All the echinoid species were collected in sandy beaches of the port of San Felipe, Baja California, and vicinity of the west coast of the Gulf of California, México. During low tides, Mellita granti Mortensen 1948 was manually collected on the upper mesolittoral, while Encope grandis L. Agassiz 1841 and E. micropora L. Agassiz 1841 were collected in shallow subtidal water (30–90 cm depths). Each sand dollar was inspected, adult symbionts were located and identified, their position on the oral and aboral area of the host was recorded, and any visible damage to the sand dollar attributable to the symbionts was documented. Each sand dollar and their symbionts were placed in individual plastic bags, labeled, and frozen. All material was preserved in 80% ethanol for further laboratory study. Voucher specimens of both ectosymbionts and hosts have been deposited in the Laboratorio de Sistemática de Invertebrados of the Universidad Autónoma de Baja California (Ensenada, Baja California, México), the Colección Poliquetológica of the Universidad Autónoma de Nuevo León (Monterrey, Nuevo León, México), the Colección Nacional de Crustáceos and the Colección Nacional de Equinodermos both of the Universidad Nacional Autónoma de México (México, Distrito Federal), and the Zoological Museum of Hamburg (Hamburg, Germany). Original descriptions, redescriptions, or specialized key for identification provided by Glassell (1935, 1936), Berry (1956), Hartmann-Schröder (1959), Caso (1980), Griffith (1987), Campos and Griffith (1990), Harold and Telford (1990), and Warén (1992) were used to identify the studied species and compile a list of all the macroinvertebrate ectosymbionts of echinoids of the Mexican Pacific.

Results

Phylum: Annelida

Class: Polychaeta

Family: incertae sedis

Genus: Struwela Hartman-Schröder 1959

Diagnosis: small worm parasitic on sand dollars (Fig. 3f), body flattened ventrally, with numerous segments, first 17 with marked dorsal transverse dark brown bands. Prostomium wider than longer, with a pair of unsegmented frontal antennae (Figs. 1a, b and 2a, b). Without palpi. Peristomium formed by two segments, with tentacular cirri similar to antennae (Figs. 1a, b and 2a, b). Parapodia (Figs. 1d and 2e) formed by bilobate lobe and simple postsetal one; dorsal and ventral cirri segmented, the ventral one larger. Chaetae of two types: long curved pseudocompound hooks on lateroventral side of peristomium (Figs. 1b, c and 2a, c); and compound falcigers (Figs. 1d–f and 2e, f). Pygidium divided dorsally (Figs. 2d and 4f).
Fig. 1

Struwela sp.: a anterior end, dorsal view; b anterior end, frontal view; c anterior pseudocompound hooks; d middle segment of body, dorsal view; e bidentate compound falciger. S. noodti (paratype): f bidentate compound falcigers. Measures: a, b = 0.1 mm; c, ef = 15 µ; d = 50 µ

Fig. 2

S. noodti Hartman-Schröder 1959: a anterior end dorsal view; b anterior end ventral view; c anterior pseudocompound hooks; d posterior end dorsal view; e parapodium, with falciger blades similar in shape and size; f falciger, articulated and terminally bifid (all after Hartman-Schröder 1959)

Species: Struwela sp.

Diagnosis: small worm, body flattened ventrally, with numerous segments, first 17 with marked dorsal transverse dark brown bands. Prostomium wider than longer, with a pair of unsegmented frontal antennae (Fig. 1a, b). Without palpi, eyes not seen. Peristomium formed by two segments, with six tentacular cirri similar to the antennae; anterior pair dorsolateral, a dorsal pair between both segments, and a ventrolateral pair. On the second peristomial segment a small, dorsolateral and papiliform cirri are observed. Parapodia (Fig. 1d) formed by bilobate lobe and simple postsetal one; dorsal and ventral cirri segmented, the ventral one larger. Chaetae of two types: long, curved, pseudocompound hooks on lateroventral side of peristomium (Fig. 1b, c); and compound falcigers, with blade of variable size (Fig. 1d, e). Pygidium is collar-shaped, divided dorsally.

Distribution: only known from the northwestern Gulf of California, México.

Material examined: 20 specimens, Campo el Pescador, San Felipe, Baja California, México (=BCMex), 30°53′33″ N, 114°51′09.3″ W, 24 October 1988, on M. granti; 41 specimens, Baja California, 22 June 1994; ten specimens, Rancho Punta Estrella, San Felipe, BCMex, 31°04′11″ N, 104°50′22″ W, September 1995 on E. grandis, four specimens, same locality, 27 September 2005, on M. granti.

Additional material studied: Struwela noodti Hartman-Schröder 1959, Paratypes Zoological Museum of Hamburg, ZMH-P-14195, La Herradura, El Salvador, Central America, on Mellita longifissa.

Remarks: because the material of the Gulf of California features the presence of a dorsal and ventral tentacular cirri (Fig. 2a, b), a group of modified hooks that extend beyond the margin of the prostomium on the first and second segment of the body (Fig. 2b, c) and a pygidium dorsally divided (Fig. 2d) it was originally assigned to S. noodti Hartman-Schröder 1959 (Figs. 1f and 2a–f). This species is known only for its type locality, El Salvador, Central America, harbored on M. longifissa, a sand dollar species that ranges from Central Mexico and west coast of Baja California peninsula at San Juanico, Baja California Sur to Panama (Harold and Telford 1990; Campos et al. 1992). A detailed examination of our material and its comparison with paratypes of S. noodti revealed differences that suggest it is a different species, but closer to S. noodti.The main distinction was found in the relative length of the falciger blade. Specimens of the Gulf of California have the falciger blades variable in length (short and long) in each parapodia (Fig. 1d, e), while in S. noodti the falciger blade has a similar length and shape in each parapodia (Fig. 1f and 2e, f). We consider the specimens of the Gulf of California to belong to a new species that will be described elsewhere.

Pleijel (1998) pointed out that, because “there are no characters to support a hesionid affinity,” the genus Struwela does not fit in the family Hesionidae. Pleijel and Rouse (2004) considered Struwela a Phyllodocida, but placing its family status as incertae sedis (see also, Salazar-Vallejo and Orenzans 2006).

Phylum: Mollusca

Class: Gastropoda

Family: Eulimidae

Genus: Turveria Berry 1956

Diagnosis: medium-sized (4–6 mm) eulimnid parasitic on sand dollars (Fig. 4f), with a rather short and broad, conical shell with a reddish brown color pattern (Fig. 3a, d). Surface covered by a very fine but distinct sculpture of axial lines. Aperture small and narrow with the line collumnela-parietal wall almost straight. Outer lip slightly sinuate below the suture (after Warén 1991).
Fig 3

T. encopendema Berry 1956: a front view; d side view; height = 4.82 mm. T. pallida Warén (1992): b front view = 4.96 mm, c side view = 4.88 mm (b and c after Warén 1992)

T. encopendema Berry 1956

Diagnosis: shell minute, ovate-conic spire, lanceolate, whorls moderately convex, solid, surface bright, semitransparent, smooth except for microscopical fine spiral and incremental striae. Protoconch subcylindric, colorless, forming a small papilliform apical prolongation; aperture oblique, narrowing pyriform, rounded and produced in front. The color is waxy white with a narrow, yellowish brown subsutural band.

Previous distribution and host: outer strand of Cholla Cove, Bahia de Adair, Sonora, Mexico; on E. grandis L. Agassiz and E. californica Verrill 1870.

Material examined: 20 specimens, Rancho Punta Estrella, San Felipe, BCMex (new locality record), 31°04′11″ N, 104°50′22″ W, July–September 1995 on E. grandis L. Agassiz; four specimens, same locality, 27 September 2005, on M. granti (new host record).

Remarks: two eulimid species of the genus Turveria (Fig. 3) have been recorded in the Gulf of California, T. encopendema Berry, 1956 and T. pallida Warén (1992) [Willard Island, Bahía San Luis Gonzaga, BCMex to Bahía Concepción, Baja California Sur, México]. These species have been found on the same host, E. grandis; however, T. encopendema had been reported on E. californica Verrill also. The specimens herein reported were compared with the original description of both species and they agree very well with the diagnostic features of T. encopendema as noted by Berry (1956). Our specimens have an ovate-conical spire, whorls moderately convex and its color is waxy white with a narrow subsutural yellowish brown band, which may continue around the body-whorl as a conspicuous warm brown band (Fig. 3a, d). Warén (1992) pointed out that T. pallida differs from T. encopendema by having a regularly conical spire, flatter whorls and less vivid color patterns (Fig. 3b, c). Despite both species being very similar, the convex (T. encopendema, Fig. 3a, d) versus flatter (T. pallida, Fig. 3b, c) whorls seems to be a distinctive character to separate these sympatric species.

T. encopendema was recorded both on the oral and aboral area of E. grandis (Fig. 4a) and M. granti (Fig. 4b) but never observed on E. micropora L. Agassiz (40 specimens examined). No external damage attributable to this species was observed on the oral or aboral surface of the host although this eulimid is considered as a parasitic species (Berry 1956; Warén 1992).
Fig. 4

aE. grandis L. Agassiz, oral view, mesial length = 76.5 mm; bM. granti Harold and Telford 1990, oral view, mesial length = 44.2 mm; cE. grandis L. Agassiz, close up of anus damaged by the adult female of D. lockingtoni, mesial length = 72 mm; dD. lockingtoni Glassell 1935, juvenile in lateral lunule, carapace width = 2.8 mm; eT. encopendema Berry 1956 on aboral surface of M. granti Mortensen, height = 4.9 mm; fStruwela sp., on aboral surface of M. granti, body length = 2.5 mm. Arrows indicate the damage caused by D. lockingtoni by removing the spines of hosts

Phylum: Arthropoda

Subphylum: Crustacea

Family: Pinnotheridae

Genus: Dissodactylus Smith 1870

Diagnosis: carapace subpentagonal, with anterolateral margins disjunt (Fig. 5a–c). Endopod of third maxilliped with the palp stouter and longer than the widest part of the ischium-merus, exopod without flagellum (Fig. 5g–i). Walking legs with dactyli bifid (Fig. 5j–l). Male abdomen with somites first and second and third through sixth fused, telson triangular; female abdomen with six somites and telson well separated.
Fig. 5

a, d, g, jD. lockingtoni Glassell 1935; b, e, h, kD. nitidus Smith 1870; c, f, i, lD. xanthusi Glassell 1936: ac caparace dorsal view; df first sternite; gi third maxilliped; jl third walking leg (after Griffith 1987, slightly retouched). Scale bar = 1 mm

Species: Dissodactylus lockingtoni Glassell 1935

Diagnosis: carapace width to length ratio less than 1.2, covered with minute granules, not-shiny (Fig. 5b). Middle region of first sternal segment tongue-like, extended beneath buccal region (Fig. 5e); Distal region of the ischium-merus of outer maxilliped rounded and bearing a robust palp with rounded segments; dactyl of maxilliped palp small but evident (Fig. 5h); ambulatory legs stout, dactylus of first three ambulatory legs bifurcate for at least one fourth length (Fig. 5k).

Distribution: San Felipe and Punta Peñasco, head of the Gulf of California to Punta Arenas, Beach, Costa Rica, Central America (Pohle and Marques 1995). On E. californica Verril, E. grandis L. Agassiz, E. micropora L Agassiz, M. longifissa Michelin, M. granti Mortensen (Campos et al. 1992; Pohle 1994).

Material examined: +100 males, +100 females, Campo El Pescador San Felipe, BCMex, 30°53′33″ N, 114°51′09.3″ W, October 1988 to September 1989, on M. granti [\ly prevalence, n = 100–110, varied from 4% (winter; only adults) to 91% (summer; megalopae, juveniles and adults)]; 30 males, 30 females, Rancho Punta Estrella, San Felipe, BCMex, 31°04′11″ N, 104°50′22″ W, July–September 1995, on M. granti, E. grandis and E. micropora.

Remarks: D. lockingtoni is the commonest symbiont crab of sand dollars and a permanent resident in the head of the Gulf of California. This species is a symbiont of species of Encope and Mellita (Fig. 4d). Observations throughout a year allow us to discover the changing residence of D. lockingtoni on the aboral and oral surfaces of the sand dollar during the postlarval ontogeny. The invasive megalopae and juveniles always reside on the aboral surface of their host species. Subadult males and females, and adult males live on the lateral lunules on the oral surface of the sand dollar, while adult females always reside between the anus and the anal lunule. In all cases, the crab damages its host by removing the spines in a section not more than twice the crab dimensions (Fig. 4a–c arrow). Furthermore, it is remarkable that adult females frequently cut around the anus of their hosts and regularly were observed transporting feces to their buccal cavity (Fig. 4c arrow). These observations suggest that adult females of D. lockingtoni are capable of being coprophagous.

Species: Dissodactylus nitidus Smith 1870

Diagnosis: carapace width to length ratio less than 1.2, smooth and shiny (Fig. 5a). Middle region of first sternal segment tongue-like, extended beneath buccal region (Fig. 5d); Distal region of the ischium-merus of outer maxilliped square and bearing a robust palp with squared segments, dactyl of maxilliped palp vestigial, microscopic (Fig. 5g); cheliped with a dense tuft of setae on ventral margin of propodus; ambulatory legs long and slender; dactylus of first three ambulatory legs bifurcate for at least one fourth length (Fig. 5j).

Distribution and hosts: from the head of the Gulf of California and west coast of Baja California Sur at Abreojos point, to west of Matacaballa, Bay of Senchura, Peru (Griffith 1987; this work). On Encope spp. (Griffith 1987); Glassell (1935) did not record any host species for this species as noted by Griffith (1987).

Material examined: 20 males, 20 females, Rancho Punta Estrella, San Felipe, BCMex, 31°04′11″ N, 104°50′22″ W, July–September 1995, on E. grandis L. Agassiz and E. micropora L. Agassiz.

Remarks: D. nitidus is a very active crab, light brown colored with scattered red spots on their legs. It is a rare species in San Felipe, Baja California and vicinity and occurs during the summer months only. It inhabits subtidally on the oral surface of E. grandis and E. micropora and was never observed on the intertidal M. granti. No damage attributable to adult crabs of this species was observed on the aboral surface of the host.

Species: Dissodactylus xanthusi Glassell 1936

Diagnosis: carapace width to length ratio greater than 1.2; middle region of first sternal segment non tongue-like (Fig. 5c); distal region of the ischium-merus of outer maxilliped rounded and bearing a robust palp with subsquare segments; dactyl of maxilliped palp small but evident (Fig. 5i); ambulatory legs slender; dactylus of first three ambulatory legs bifurcate for at least one fourth length (Fig. 5l).

Distribution and hosts: San Felipe and Punta Peñasco Gulf of California on E. grandis L. Agassiz, E. micropora L. Agassiz, and M. longifissa Michelin, (Pohle 1994) [this is a questionable record, since the only species of Mellita hitherto known in the head of the Gulf of California is M. granti Harold and Telford 1990, see Campos et al. 1992]; Venado Beach, Panama, on Encope stokesi L. Agassiz, (Dexter 1977).

Material examined: 30 males, 30 females, Rancho Punta Estrella, San Felipe, BCMex, 31°04′11″ N, 104°50′22″ W, July–September 1995, on E. grandis L. Agassiz, E. micropora L. Agassiz.

Remarks: in the San Felipe area, D. xanthusi is a seasonal crab which, like D. nitidus, occurs during the summer months when the shallow water temperature reaches about 26–30°C. Both species gradually disappear during the autumn to be undetectable during the winter months when the temperature of surface water in the port of San Felipe and the surrounding area drop to 14–18°C. D. xanthusi occurs subtidally, on the anterior margin of the aboral surface of E. grandis and E. micropora, but was never observed on M. granti. When the sand dollar was removed from the sand and it was dorsoventrally rotated, the crab walked quickly around the aboral surface and from this area to the oral face. No damage attributable to adult crabs of this species was observed on the aboral surface of the host. This crab ranges from a chocolate brown to a dark purple color in life, which is distinctive to identify adults in the field.

Discussion

Five intertidal and shallow water invertebrate species were found as presumed ectoparasites of six species of echinoids of the family Mellitidae (Encope and Mellita). Although an individual host may have only one symbiotic species on its body, it is not uncommon, during the summer season, to observe all the five species cohabiting on a same host. Because the parasitic species studied have been recorded on several host species, they should be considered generalists (see Table 1). With exception of subadults and adults of D. lockingtoni that prefer to live in the lunules on the oral surface and individuals of T. encopendema, which were observed in both the oral and aboral surfaces, the rest of the species seem to prefer to reside on the aboral surface of their hosts. Struwela sp., D. nitidus, and D. xanthusi are very active species in contrast to D. lockingtoni and T. encopendema which normally lie motionless on the host. Crabs of the genus Dissodactylus were the most diverse group; nevertheless, D. nitidus and D. xanthusi are seasonal species in the head of the Gulf of California, disappearing during the winter season when the temperature drops to 14–18°C (see, Campos 2007). The rest of the species are permanent residents and the parasitic polychaete, Struwela sp., seems to be endemic for this area. In addition to the studied species, the parasitic eulimnid T. pallida Warén 1992 and the pea crabs, D. glasselli Rioja 1944 (Playa Norte, Mazatlan, Sinaloa and Playa de San Benito, near Tapachula, Chiapas, México and Puerto El Triunfo, El Salvador, Central America, see Hendrickx 2008) and Clypeasterophilus ususfructus (Griffith 1987) (Cape San Miguel and off Río El Fuerte, Sinaloa, Gulf of California, México to Bahía Santa Elena, Ecuador, see Hendrickx 1990; Campos and Griffith 1990) have been recorded as presumed ectoparasites of sand dollars in the subtropical and tropical Mexican Pacific (see Table 1). Regarding the symbiotic status of the studied species, we consider the eulimnid, T. encopendema a true parasite, but it is not clear if the worm Struwela sp. and the crabs D. nitidus and D. xanthusi are fully parasitic species feeding exclusively on the fluids or tissue of their host or only complement their nourishment by ingesting some tissue of their host periodically. On the other hand, the symbiotic status of D. lockingtoni is somewhat controversial and seems to be transitional between commensalism–parasitism with an apparent specialization to coprophagy in adult females, which might be related with its sexual maturation (ovogenesis). The interaction among these five species of invertebrates when they co-occur in the same host is totally unknown.
Table 1

External macroparasites of echinoids of the Mexican Pacific

Symbiont

Host

Echinodermata: Clypeasteroidea

Mellitidae

Clypeasteridae

Gastropoda

SR

EC

EG

EM

ES

MG

ML

CS

CE

 Family Eulimidae

         

 Turveria encopederma Berry 1956

A–O

  

   

 Turveria pallida Warén 1992a

A?

 

      

Polychaeta

         

 Family uncertain

         

 Struwela sp.

A

 

 

  

 Struwela noodti Hartmann-Schröder 1959

A

     

  

Crustacea

         

 Family Pinnotheridae

         

 Clypeasterophilus ususfructus Griffith 1987b

A?

      

√?

 Dissodactylus glasselli Rioja 1944b

A?

    

  

 Dissodactylus lockingtoni Glassell 1935

A–O

 

  

 Dissodactylus nitidus Smith 1870

A

  

  

 Dissodactylus xanthusi Glassell 1936

A

 

 

  

List compiled from Berry (1956), Hartmann-Schröder (1959), Dexter (1977), Griffith (1987), Campos and Griffith (1990), Hendrickx (1990, 2008), Campos et al. (1992), Warén (1992), Pohle and Marques (1995), and this study

CS Clypeaster europacificus H.L. Clark 1914, CE C. speciosus Verrill 1870, EC E. californica Verrill 1870, EG E. grandis L. Agassiz 1841, EM E. micropora L. Agassiz 1841, ES E. stokesi (Dexter 1977), MG M. granti Mortensen 1948, ML M. longifissa Michelin 1858, SR site of residence, A aboral, O oral

aSpecies not collected in the present study

bSpecimens from the Colección Nacional de Crustáceos of the Universidad Nacional Autónoma de México

Acknowledgements

We are indebted to Lobo Orensanz and Sergio I. Salazar-Vallejo for their aid with the literature, SEM photographs, and taxonomic discussion on Struwela species; Andrés Warén who kindly provided us with the unavailable literature and confirmed the identity of T. encopendema Berry, 1956. The authors deeply appreciate the following persons and institutions for lending the voucher specimens and for the working facilities: Fernando Alvarez and José Luis Villalobos, Colección Nacional de Crustáceos, Instituto de Biologia, Universidad Nacional Autónoma de México, Mexico, Distrito Federal (EM); Alfredo Laguarda and Francisco Solís Marín, Colección Nacional de Equinodermos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Distrito Federal, México (CNE); Michel E. Hendrickx, Colección de Macroinvertebrados, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlán, Sinaloa, México (EMU); and Angelika Brandt, Zoological Museum, Hamburg, Germany. This work was partially funded by a grant from CONACyT S52903-Q (México) “Sistemática, relaciones filogenéticas y evolución de los géneros Americanos de la subfamilia Pinnotherinae (Crustacea, Brachyura, Pinnotheridae)”. The senior author is a scholarship holder of the Consejo Nacional de Ciencia y Tecnología (CONACyT), México and a postgraduate student at the Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León, México.

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Ernesto Campos
    • 1
  • Alma Rosa de Campos
    • 1
  • Jesús Angel de León-González
    • 2
  1. 1.Facultad de CienciasUniversidad Autónoma de Baja CaliforniaEnsenadaMéxico
  2. 2.Facultad de Ciencias BiológicasUANLSan Nicolás de los GarzaMéxico

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