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First Record of a Pearlfish, Carapus mourlani, Inhabiting the AplysiidOpisthobranch Mollusc Dolabella auricularia1

Peter W. Glynn,2,3 Ian C. Enochs,3 John E. McCosker,4 and Abigail N. Graefe5

Abstract: Adult individuals of the pearlfish Carapus mourlani (Petit, 1934) occurcommonly in the mantle cavity of the opisthobranch mollusc Dolabella auricu-laria (Lightfoot, 1786) in shallow marine waters of the Gulf of Chiriquı, PacificPanama. Nearly 30% of the molluscan hosts collected during the day on a coralreef contained one or two fish. Feeding observations of a captive fish as well asthe intact condition of the host’s ctenidium and other internal organs suggestthat C. mourlani is an inquiline commensal and not parasitic. Fish curl aroundthe ctenidium during the day and capture microcrustaceans when the fishemerge from their host at night to feed. From low-light infrared video record-ings, Carapus was observed to accurately grasp rapidly swimming amphipods innearly total darkness and ingest them. This symbiotic relationship appears tobenefit Carapus by allowing the fish to avoid predators during the day and toforage at night.

Carapid pearlfishes are free-living, com-mensal inquilines or parasitic (Trott 1981,Parmentier and Vandewalle 2005). Thosethat are inquiline commensals are reportedto occupy holothurians, sea stars, or bivalvemolluscs (Trott 1970, Markle and Olney1990, Paredes-Rios and Balart 1999). Theterminology adopted herein follows Castro(1988). Symbiosis is defined as a close hetero-specific association irrespective of harm orbenefit to the partners. Commensals are sym-bionts with no metabolic dependency (e.g.,food, growth factors) between the membersof the association. Inquilines refer to associ-

ates that shelter within (but not inside thebody cavity of ) the host. Some carapid spe-cies enter the coelom of their hosts, but thiswas not observed in Carapus mourlani in ourstudy.

It has also been suggested, but not demon-strated, that some carapids facultatively oc-cupy polychaete worm tubes (Williams andShipp 1982) and sponges (Ayling and Cox1982). Many ophidiiformes possess a propen-sity for finding shelter in a variety of inani-mate substrates and as such their hidingbehavior in a particular host can be describedas facultative rather than obligate (Svetovidov1961, Markle and Olney 1990). This is thefirst report of a pearlfish, Carapus mourlani(Petit, 1934), inhabiting the mantle cavityof a large opisthobranch mollusc, Dolabellaauricularia (Lightfoot, 1786), in the Gulf ofChiriquı, Panama.

Four species of carapids are recognizedfrom the eastern tropical Pacific (Markle andOlney 1990, Parmentier et al. 2006). Theyare Echiodon exilium (Rosenblatt, 1961), whichare free-living as adults; Carapus dubius (Put-nam, 1874), which inhabits bivalve molluscs;Carapus mourlani, an associate of sea starsand holothurians (Markle and Olney 1990);and Encheliophis vermicularis (Muller, 1842),an obligate parasite of the holothurian Actino-pyga lubrica (Sluiter).

Pacific Science (2008), vol. 62, no. 4:593–601: 2008 by University of Hawai‘i PressAll rights reserved

1 Support was provided by U.S. National ScienceFoundation grant OCE-0526361 and earlier awards.Manuscript accepted 26 October 2007.

2 Corresponding author (e-mail: pglynn@rsmas.miami.edu).

3 Division of Marine Biology and Fisheries, Rosen-stiel School of Marine and Atmospheric Science, Uni-versity of Miami, 4600 Rickenbacker Causeway, Miami,Florida 33149-1098.

4 California Academy of Sciences, San Francisco, Cal-ifornia 94118-4599.

5 Marine and Atmospheric Science Program, Univer-sity of Miami, Coral Gables, Florida 33124-0411.

Carapus mourlani was first reported fromthe eastern Pacific on the basis of specimensfound to inhabit the sea cucumber Isostichopusfuscus (Ludwig) off the Ecuador coast (Par-mentier et al. 2006). Twelve C. mourlaniwere found within the coelomic cavity, respi-ratory tree, or digestive tracts of the 4,345(0.28%) I. fuscus that were collected betweendepths of 5 and 60 m and examined. Carapusmourlani is widely distributed in the tropicalIndo-Pacific from East Africa to Hawai‘i andthroughout Micronesia. In the central towestern Indo-Pacific it is known to inhabitthe asteroids Culcita novaeguineae Muller &Troschel, Pentaceraster cumingi (Gray), Cho-riaster granulatus Lutken, and Acanthasterplanci (Linnaeus) and the holothurians Sticho-pus variegatus Semper, Stichopus chloronotusBrandt, Bohadschia argus Jager, Actinophyamuritiana (Quoy & Gaimard), and Holothuriascabra Jaeger (see Markle and Olney 1990).

materials and methods

Dolabella auricularia, a member of the opis-thobranch family Aplysiidae, is an uncom-monly large sea slug easily recognized by itstruncated posterior border, which forms asloping, disklike shield with elongated simplepapillae covering the dorsum (Camacho-Garcıa et al. 2005). Dolabella is the largest seahare present in the tropical Indian and Pacificoceans, reaching 0.5 m in length. It is widelydistributed from the Red Sea to the tropicaleastern Pacific, including the Hawaiian andGalapagos islands (Gosliner et al. 1996). Car-apus mourlani, family Carapidae, is a commonspecies and differs from other carapids in itsdentition, swimbladder morphology, and col-oration. It reaches 17 cm in total length(Markle and Olney 1990).

The majority of the symbionts were cap-tured during the day in 25- to 30-liter-volume mesh bags of Pocillopora spp. coralrubble anchored at 3–6 m depth on the sea-ward side of the Uva Island coral reef. Thecoral reef is on the west side (07� 49 0 N, 81�

46 0 W) of Uva Island in the Gulf of Chiri-quı, Pacific Panama (Figure 1). The bundlesof rubble were located about 5 m downslope

from the reef framework. Collections weremade from 2002 to 2005, the first 6 monthsafter emplacement of the rubble bags, thenat yearly intervals thereafter. Dolabella andCarapus were also collected at 4–6 m depthalong the south shore of the Uva Islandembayment when the opisthobranch hostemerged at night. The presence of Carapusinhabiting Dolabella was determined whenthe oxygen concentration declined and thefish exited the host. The emerging fish werethen quickly revived with frequent waterchanges and aeration. Symbionts employedin long-term observations were reintroducedto their hosts and maintained in flow-throughaquariums until shortly before departure toMiami, Florida. About 4 hr before the flight,symbiont-host pairs were placed in polyethyl-ene bags containing approximately 1 liter offiltered seawater and 2 liters of 100% oxygen.Bagged specimens were placed inside a largecooler and transported as cargo aboard aflight to Miami. Upon arrival, the symbiontswere immediately moved to flow-throughaquariums at the Rosenstiel Marine School,University of Miami.

Animals were maintained in powder-coated, metal screen–covered (to prevent es-cape) 40-liter aquariums supplied with sea-water from Biscayne Bay. Aquariums werekept in subdued lighting during the day andin darkness at night. Large rocks were placedin each aquarium to provide shelter for thecryptic habit of the molluscan hosts. Thehosts were fed several times a week withgreen filamentous (Derbesia sp.) and brownStypopodium zonale algae. The algae were col-lected from Biscayne Bay and containedabundant associated microfauna.

Observations on the exit and entrance be-havior of several fish were conducted duringthe day and night. Behavioral observationsin aquariums were obtained with a remote,night-vision, digital video recorder (DVR).An infrared (IR) LED (light-emitting diode)illuminator was positioned over an aquariumand programmed to turn on automatically atlow light levels, beginning before sundownand ending after sunrise. A low-light IR-sensitive bullet camera was connected to a

594 PACIFIC SCIENCE . October 2008

DVR (Archos 504) and was positioned to re-cord the symbionts. An aquarium divider wasused to constrain the symbionts within thefield of view. Video files were later uploadedto a computer and symbiont activity was sub-sequently observed.

The total body lengths (TL) of Carapuspreserved in 70% ethanol were measured tothe nearest millimeter. Live body lengthsand weights of 27 specimens of Dolabellawere obtained within a few hours after cap-ture. Length measurements were taken fromnaturally relaxed individuals and weightsfrom animals blotted for about 30 sec withabsorbent paper towel. A least squares regres-sion analysis was performed on these 27 indi-viduals. The weights of nine individuals wereestimated from their lengths according to theregression relationship noted.

Four individuals each of Dolabella and Car-apus preserved in 70% ethanol were dissectedto determine the condition of the ctenidia

and other organs, and gut contents, respec-tively. All of these specimens were living to-gether. Two of the opisthobranch hosts werefrom field-collected (March 2005) specimens.The remaining two hosts and four fish sym-bionts were collected 18–22 March 2006 atUva Island and remained together in aquari-ums for about 3 months. Specimens of C.mourlani are deposited in the IchthyologyDepartment of the California Academy ofSciences (cas), San Francisco, California, andthe Virginia Institute of Marine Sciences(vims), Glouster Point, Virginia. Includedare cas 225463 (85 mm TL); cas 225464(84 mm TL); cas 225465 (85 mm TL); cas225466 (68 mm TL); cas 225467 (77 mmTL); cas 225468 (73 mm TL); cas 225469(82 mm TL); cas 225471 (87 mm TL); cas225472 (76 mm TL); cas 225473 (87 mmTL); vims 12001 (TL not measurable); vims12002 (71 mm TL); vims 12003 (74 mmTL); and vims 12004 (71 mm TL).

Figure 1. Dolabella auricularia collection sites in the Gulf of Chiriquı, Panama. 1, Uva Island coral reef; 2, south shoreof Uva Island embayment; 3, Canal de Afuera Island; 4, north shore of Coiba Island; 5, Jicarita Island; 6, coral reef onunnamed island in the Secas Islands group.

Pearlfish Inhabits an Opisthobranch Mollusc . Glynn et al. 595

results

On the Uva Island coral reef, the overallmean prevalence of adult Carapus mourlaniwith Dolabella auricularia was 0.292 (Table 1;Figure 1, site 1). The prevalence of the sym-biosis was highest at the south end of the reef(0.419) compared with the north (0.067) andcentral (0.263) reef sectors. Most Dolabellaðn ¼ 8Þ hosted single individuals, but threedifferent hosts contained two fish each. Dola-bella collected at night (March 2005, 0100–0200 hours; March 2006, 2100–2200 hours)while grazing along the coral/rock bottom ofthe south shore embayment (Figure 1, site 2)exhibited a prevalence of 0.22 (4 Carapus/18Dolabella). Three C. mourlani were associatedwith nine Dolabella (prevalence ¼ 0.33) col-lected during the day from under pocilloporidblocks along the leeward side of Uva reef.The carapid inquiline was also found inhabit-ing D. auricularia by D. R. Robertson (pers.comm.) in 2003 at Canal de Afuera Islandand along the north shore of Coiba Island(Figure 1, sites 3, 4), and by Terence M. Gos-

liner at Isla Jicarita in 2003 (Figure 1, site 5).The presence of Carapus was determined byintroducing Quinate (active ingredient qui-naldine) to the mantle cavity. Six adult C.mourlani were found by Robertson inhabitingD. auricularia collected from under rock screewith a prevalence of @0.01. Finally, 22 Dola-bella were collected in March 2003 from un-der coral blocks at 1 m depth on a reef flatin the Secas Islands (Figure 1, site 6), butnone of these contained the inquiline. Onlytwo tenuis-stage larvae were found over thecourse of this study. They were collectedfrom Dolabella in rubble bags on March 2003from central and south Uva reef locations.

Euapta godeffroyi (Semper), the only otherlarge abundant holothurian at the study site,did not host C. mourlani. Examination of60 individuals of E. godeffroyi collected fromrubble bags across the reef front during2002–2005 did not reveal associated carapids.Numerous specimens of Acanthaster planci,another potential host, were examined anddissected at the Uva reef and from other lo-calities in the Gulf of Chiriquı from 1970 to

TABLE 1

Numbers of Carapus mourlani Found in Association with Dolabella auricularia Collected from Rubble Bags at 4–6 mDepth on the Seaward Front of the Uva Island Coral Reef, 2002–2005

Location on Reefa Date No. Dolabella No. Carapus Car./Dol.b Mean Prevalence

North 19 Sept. 02 1 0 —1 0 —

7 Mar. 04 8 1 19 Mar. 05 1 0 —10 Mar. 05 4 0 — 0.067

Center 4 Mar. 03 1 1 14 1 13 0 —

15 Sept. 03 2 0 —10 Mar. 05 1 2 211 Mar. 05 4 1 112 Mar. 05 4 0 — 0.263

South 17 Sept. 02 5 1 19 Mar. 03 10 2 114 Sept. 03 1 1 113 Mar. 04 6 5 1, 2, 215 Mar. 05 2 0 —

7 4 ? 0.419Overall mean prevalence 0.292

a North, center, and south sectors of reef.b Denotes number of Carapus per host when inquiline was present.

596 PACIFIC SCIENCE . October 2008

2006. Carapus was not found in that specieseither.

Field observations of recently capturedfish showed them to enter the host’s mantlecavity headfirst through the anteriorly locatedinhalant siphon. However, on several occa-sions fish explored the inhalant siphon areaheadfirst then quickly inserted their tails andbacked in to the mantle cavity tail first. Thistail-first entry was executed quickly, in from2 to@25 seconds, by vigorous body wriggling(Figure 2). A few fish were observed to exittheir hosts headfirst from the exhalant siphon.In no instance did the activities of Carapuscause Dolabella to contract or release ink.Video records (n ¼ 13, @12 hr nocturnalobservations each) over a 4-month period(November–March) showed a hidden fish toemerge headfirst from the inhalant siphon

after sunset and enter the exhalant siphonheadfirst after varying times of free-swimming activity. The times outside thehost varied from 24 to 587 (9.8 hr) min. Ontwo occasions, fish exited and entered itshost twice. During 10 nocturnal video rec-ords over a 2.5-month period, Carapus failedto emerge from its host.

Fifteen C. mourlani collected from Dola-bella in rubble bags over the period 10–15March 2005 had ethanol-preserved mean (1sd) lengths and wet weights, respectively, of81.3 (6.9) mm and 0.83 (0.32) g. Total lengthsranged from 68 to 97 mm and weightsfrom 0.315 to 1.534 g. The Dolabella length-weight relationship for 27 individuals (Figure3) is expressed as the power function y ¼0:040X 3:271 ðr 2 ¼ 0:893Þ. Nine individualswith known lengths only are also plotted in

Figure 2. Head of Carapus mourlani protruding from inhalant siphon of Dolabella auricularia (arrow) recently collectedat the Uva Island coral reef, March 2004.

Pearlfish Inhabits an Opisthobranch Mollusc . Glynn et al. 597

Figure 3. Carapids occurred with Dolabellaover a wide range of host sizes, from 10 to20 cm in length. The smallest and largest Do-labella hosts contained two and one C. mour-lani, respectively. The two tenuis larvae were143 and 153 mm in length. Their specifichosts could not be identified.

Upon visual inspection of four dissectedDolabella that hosted carapids, none revealeddamage to tissues lining the mantle cavity ordamage to the ctenidium, digestive gland,gonad, and kidney (Figure 4). Another indi-cation that the host’s gonads were not im-paired is from reproductively active Dolabellaharboring the fish inquilines. On 13 March2004, six Dolabella hosting five carapids at thesouth end of Uva reef were aggregated andlaying large masses of eggs.

On several consecutive nights (4–13March 2007), the infrared video recordingsshowed C. mourlani feeding on swimmingcrustaceans that had emerged from a rock

covered with the brown alga Stypopodium zo-nale. Amphipods, 4–6 mm in body length,were captured as they swam rapidly upwardfrom the algal substrate. The carapid quicklysensed the location of the amphipod in nearlytotal darkness, from distances of 2 to 4 cm. Insome instances, detection seemed to involvethe swimming motion of the prey becausethe fish was oriented in the opposite direc-tion. Adult carapids such as C. mourlani havea moderately developed lateral line and ce-phalic pore system that would allow the de-tection of such prey movements. The fishgrasped each amphipod and crushed andswallowed body parts. On a few occasions,amphipods were captured, momentarilychewed, and then rejected. Other swimmingcrustaceans (ostracods and mysids) also weredetected, captured, and ingested. Multiplefeedings per night were observed. One nighta carapid captured and ingested five crusta-ceans.

Figure 3. Body length and mass relationship of live Dolabella auricularia collected at the Uva Island coral reefðn ¼ 36Þ. Solid symbols denote Dolabella hosts with Carapus mourlani. The number 2 identifies hosts that containedtwo fish symbionts.

598 PACIFIC SCIENCE . October 2008

Examination of the adult buccal cavity re-vealed well-developed dentition with numer-ous backward-directed, needlelike teeth onthe upper and lower jaws. The two or threeteeth anteriorly on the vomer are stout andlarge, and located along the midline of theroof of the mouth. The same arrangementof teeth was present but less well developedin the tenuis larval stage.

discussion

The presence of two fish per host is not un-common among carapid symbioses. As manyas 15 and 19 Carapus mourlani, respectively,were reported in single individuals of a holo-thurian and an asteroid species (Meyer-Rochow 1977). At least one of the fish waspresent in the holothurian’s coelom. It is like-ly that the paired C. mourlani found in Dola-bella in our study were of the opposite sex,although this was not verified (Trott 1981).

The relatively large and nearly totally en-closed mantle cavity of Dolabella renders thisa suitable resting space for Carapus. The con-

stant supply of inhalant water that irrigatesthe single ctenidium, over which Carapus iscoiled, ensures a sufficiently oxygenated me-dium. Besides benefiting from the shelterprovided by Dolabella, it is possible that thehost’s grazing activities on algal substratesexpose mobile microfauna that can then bemore readily detected and consumed by thepearlfish. This would be ecologically equiva-lent to hamlets that follow parrotfish andsurgeonfish schools, feeding on invertebratesand fishes flushed from algal turfs by thegrazing herbivores (Ogden and Buckman1973). Meyer-Rochow (1979) suggested thatsome hosts of C. mourlani may offer a sourceof prey. For example, the cushion sea starCulcita, a common host of pearlfish in thecentral and West Pacific, generally sheltersshrimp that may be consumed by Carapus.No invertebrate commensals were observedon Dolabella.

Another possible advantage of Carapussheltering in Dolabella is the ability of thisherbivore host to sequester noxious second-ary metabolites from its algal diet. The con-

Figure 4. Dissected mantle cavity of Dolabella showing exposed, undamaged ctenidium. A Carapus sheltered in thisaquarium-confined host for about 3 months.

Pearlfish Inhabits an Opisthobranch Mollusc . Glynn et al. 599

centration of unpalatable chemicals wouldlikely render Dolabella less likely to be con-sumed by potential reef predators. Penningset al. (1999) demonstrated from feeding as-says on reefs at Guam that the skin, eggs,and digestive glands of D. auricularia wereunpalatable to reef fishes. The opistho-branch’s ink also likely plays a role in chemi-cal defense, due to the concentration of adietary-derived red algal pigment (aplysiovio-lin). The unpalatable nature of the host’s tis-sues might also discourage feeding by the fishsymbiont.

A study conducted in the South MoluccanSea, based on gut analyses of adult C. mour-lani associated with echinoderms (asteroidsand holothurians), demonstrated that de-capod crustaceans, probably polychaetous an-nelid worms, and small fishes were consumedby the symbiont (Meyer-Rochow 1979). An-other line of evidence, from the stable isoto-pic composition of adult muscle tissue of C.mourlani living in the coelomic cavity of acushion sea star in French Polynesia, supportsthe earlier findings of a nonparasitic associa-tion (Parmentier and Das 2004). Our results,of nocturnal feeding on crustaceans and noapparent damage to the opisthobranch host’sinternal organs, also support those studies.Two tenuis-stage larvae were found with Do-labella, but we were not able to determinetheir feeding habits. Jangoux (1974) notedthat the young stages of C. homei (Richard-son) are more inclined to parasitism thanadults, consuming the gonadal tissues of theirasteroid hosts. This claim is suspect, however,because his description of the fish is incor-rect, and C. homei does not inhabit asteroidsand is not parasitic.

Acanthaster planci occurs at the Uva reef,sometimes at relatively high population den-sities (25–30 individuals ha�1) but has notbeen observed hosting C. mourlani as in thewestern Pacific (Cheney 1973). On Guam, A.planci is probably not a major host of Carapusbecause only around 1% of 450 sea starscontained the inquiline. The only large holo-thurian present at the Uva reef is Euapta god-effroyi, but C. mourlani has not been found toinhabit this species either. It is possible thatthe sticky body wall and tentacles of E. godef-

froyi, due to the presence of anchor ossicles,would offer an entanglement hazard to Cara-pus.

The ability of Carapus mourlani to feedunder subdued light conditions demonstratesa capacity to detect and capture rapidly mov-ing prey at night. Meyer-Rochow and Tiang(1978) showed that the eyes of C. mourlaniare fully functional and concluded (p. 583)‘‘that the eye of C. mourlani is basically aphotoreceptor designed for vision in a darkenvironment characterized by high sensitivityand poor resolution, but that its visual perfor-mance drops with age.’’ It is also possible thatthe swimming activities and pressure changesgenerated by potential prey serve to alert C.mourlani of a feeding opportunity.

Considering the nocturnal feeding behav-ior, visual sensitivity under low-light condi-tions (Meyer-Rochow and Tiang 1978), andthe adaptations of the buccal apparatus forfeeding, it is likely that the diurnal associationof Carapus mourlani with a variety of hostsevolved in response to avoid visual preda-tors. Based on the structural and behavioralspecializations in feeding, adult C. mourlanican be justifiably placed among graspinghunters.

acknowledgments

John E. Olney kindly identified the carapidspecies. We thank Tyler B. Smith and JuanL. Mate for photographic help, and C. M.Eakin, Vincent Flynn, Peggy Fong, GenaHockensmith, Derek Manzello, and MattWhartian for field and laboratory assistance.The feeding and maintenance of animals wasperformed by Tara Dolan, Carla Fernandez,Tally Holcombe, Daniel Holstein, LindsayJones, Margarita Kruyff, Megan Porter, andErin Reilly. Jonathan Walkenstein (Non-linear Dynamics Laboratory, University ofMiami) and Aaron Jozsef offered technicaladvice on the IR illuminator and camera de-sign. Information on Carapus mourlani collec-tions from Panama were provided by D. R.Robertson and Terence M. Gosliner. Permis-sion to work and collect specimens in theCoiba National Park was authorized by theAutoridad Nacional del Ambiente (ANAM),

600 PACIFIC SCIENCE . October 2008

Republic of Panama. Scientific export per-mits were granted through the Ministerio deDesarrollo Agropecuario (MIDA) permit nos.46099 and 72423, and SEX/A-23-05 andSEX/AP-2-06 (ANAM). The SmithsonianTropical Research Institute also provided lab-oratory and logistical support.

Literature Cited

Ayling, T., and G. J. Cox. 1982. Collins guideto the sea fishes of New Zealand. WilliamCollins Publishers Ltd., Auckland, NewZealand.

Camacho-Garcıa, Y., T. M. Gosliner, and A.Valdes. 2005. Field guide to the sea slugsof the tropical eastern Pacific. CaliforniaAcademy of Sciences, San Francisco.

Castro, P. 1988. Animal symbiosis in coralreef communities: A review. Symbiosis5:161–184.

Cheney, D. P. 1973. Pearlfish (Carapidae) inAcanthaster planci (L.). Micronesica 9:159.

Gosliner, T. M., D. W. Behrens, and G. C.Williams. 1996. Coral reef animals of theIndo-Pacific. Sea Challengers, Monterey,California.

Jangoux, M. 1974. Sur l’‘‘association’’ entrecertaines asteries (echinodermata) et despoissons Carapidae. Rev. Zool. Afr.88:789–795.

Markle, D. F., and J. E. Olney. 1990. System-atics of the pearlfishes (Pisces: Carapidae).Bull. Mar. Sci. 47:269–410.

Meyer-Rochow, V. B. 1977. Comparisonbetween 15 Carapus mourlani in a singleholothurian and 19 C. mourlani from star-fish. Copeia 1977:582–584.

———. 1979. Stomach and gut content ofCarapus mourlani from starfish and a holo-thurian. Ann. Zool. Fenn. 16:287–289.

Meyer-Rochow, V. B., and M. K. Tiang.1978. Visual behavior, eye and retina ofthe parasitic fish Carapus mourlani. Biol.Bull. (Woods Hole) 155:576–585.

Ogden, J. C., and N. S. Buckman. 1973.

Movements, foraging groups, and diurnalmigrations of the striped parrotfish Scaruscroicensis Bloch (Scaridae). Ecology 54:589–596.

Paredes-Rios, G. A., and E. F. Balart. 1999.Corroboration of the bivalve, Pinna rugosa,as host of the Pacific pearlfish, Enchelio-phis dubius (Ophidiiformes: Carapidae), inthe Gulf of California, Mexico. Copeia1999:521–522.

Parmentier, E., and K. Das. 2004. Commen-sal vs. parasitic relationship between Cara-pini fish and their host: Some furtherinsight through d13C and d15N measure-ments. J. Exp. Mar. Biol. Ecol. 310:47–58.

Parmentier, E., A. Mercier, and J. Hamel.2006. New host and geographical distribu-tion for the pearlfish Carapus mourlani(Carapidae) with a discussion of its biol-ogy. Copeia 2006:122–128.

Parmentier, E., and P. Vandewalle. 2005.Further insight on the Carapini-holothurian relationships. Mar. Biol.(Berl.) 146:445–465.

Pennings, S. C., V. J. Paul, D. C. Dunbar, M.T. Hamann, W. A. Lumbang, B. Novack,and R. S. Jacobs. 1999. Unpalatable com-pounds in the marine gastropod Dolabellaauricularia: Distribution and effect ondiet. J. Chem. Ecol. 25:735–755.

Svetovidov, A. N. 1961. On European speciesof the family Ophidiidae and on the func-tional importance of the structure specific-ity of their fish sound. Vopr. Ikhtiol. 17:3–13.

Trott, L. B. 1970. Contributions to the biol-ogy of carapid fishes (Paracanthopterygii:Gadiformes). Univ. Calif. Publ. Zool.89:1–60.

———. 1981. A general review of the pearl-fishes (Pisces, Carapidae). Bull. Mar. Sci.31:623–629.

Williams, J. T., and R. L. Shipp. 1982. A newspecies of the genus Echiodon (Pisces: Car-apidae) from the eastern Gulf of Mexico.Copeia 1982:845–851.

Pearlfish Inhabits an Opisthobranch Mollusc . Glynn et al. 601