BULLETIN OF MARINE SCIENCE. 32(3): 736-744, 1982 CORAL REEF PAPER

AN ASSOCIATION OF A POLYCHAETE, BRANCHIOSYLLIS EXILIS WITH AN OPHIUROID, ECHINATA, IN PANAMA

Gordon Hendler and David L. Meyer

ABSTRACT On the Caribbean coast of Panama Branchiosyl/is exi/is (Gravier) is associated with Ophio- coma echinata (Lamarck). They have not been found in symbiosis in other localities although both species are widespread. B. exifis was not collected on the ophiuroid species sympatric with O. echinata, but we speculate that it may associate with other hosts elsewhere in its range. Larger ophiuroids are more often infested than smaller specimens. In the majority of infestations a single polychaete is found near the mouth or on the arm on the ventral surface of the ophiuroid. The consistent occurrence of one polychaete per host may be an indication of aggression between individuals of B. exi/is. The polychaete freely enters and leaves the mouth of O. echinata and may steal food captured by the ophiuroid. The incidence of infestation varies at different collecting sites and seasonally at a single locality. It is possible that fluctuations in the incidence of infestation are related to seasonal stress and mortality of B. exilis, or are effected through changes in the density of the host population.

Some of the large and relatively sedentary species of the act as hosts for associated invertebrates. For example, Indo-Pacific species of Ophio- coma have as associates a tric1ad, pycnogonid, crab, and several species of poly- chaetes (Sloan et aI., 1979). Ophiocoma echinata from Cura

METHODS

This report is based on surveys carried out on the mainland of Panama and in the San BIas Ar- chipelago (Panama) from 1973 to 1980. Data on the freql,lency of infestation were gathered while collecting ophiuroids for a study of reproductive cycles (1972-1974), and occasional surveys thereafter provided additional information. Samples were collected by overturning coral rubble and coral slabs in shallow areas (1-3 m deep) of the sublittoral and the reef flat. This meant that only adult O. echinata were examined, since the smallest O. echinata occur in less accessible, cryptic habitats from the shallow reef flat to the deeper fore-reef zones, often in the interstices of colonies of calcareous algae and branching corals (unpub. obs.), Much of the research reported below was carried out at the Galeta Marine Laboratory (Smithsonian Tropical Research Institute) and additional observations on the incidence of the Ophiocoma-Branchiosy/lis association were made by the authors and their col- leagues at other sites in Panama, the Caribbean, and the Eastern Pacific.

736 HENDLER AND MEYER: POLYCHAETE·OPHIUROID ASSOCIATION 737

15

w ...~ 10 - NOT INFESTED • ""w u a: w C>.

1D 13 16 19 21 25 28 SIZE [mm DISC DIAMETER] Figure 1. (Left) Branchiasyllis exi/is. about 2 cm long, on the ventral surface of the arm of Ophia- coma echinata. Galeta Reef Flat, Caribbean, Panama. Figure 2. (Right) The size-frequency distribution of Ophiacama echinafa infested with Branchia- sy//is exi/is, superimposed on the distribution of uninfested O. echinata. Data from all samples of measured O. echinata inspected for B. exi/is in Panama are combined. N = 915.

RESULTS The syllid polychaetes identified as Branchiosyllis exi/is found on Ophiocoma echinata are usually about 1.5 to 2 cm long, with overall black pigmentation (Fig. 1). The segments of the polychaete each have a thin white border such that on close examination the polychaete displays light striations. This pattern of pig- mentation makes it difficult to distinguish specimens of B. exi/is against the black, brown, and white body of O. echinata. The effectiveness of the polychaete's camouflage is heightened by its usual location on the black and white banded arms of the ophiuroid between colonnades of black and white striped spines and rapidly moving white tube feet (Fig. 1). Adult B. exi/is were found exclusively on O. echinata although 10 to 15 species of large ophiuroids were routinely collected in habitats occupied by the infested O. echinata populations. In fact, two of the common sympatric ophiuroids were congeners of O. echinata, namely O. wendti Muller and Troschel similar in size and color to O. echinata, and the smaller green-brown species, O. pumila Liitken. Surveys at other localities to determine the incidence of Branchiosyllis infestation showed that 118 O. wendti and 10 O. pumila collected were free of B. exilis while 39.1% of 838 O. echinata examined carried B. exi/is (Table 1). Over 100 additional specimens of O. wendti and O. pumila were inspected for another study and B. exi/is was never seen on either species. Additionally, hundreds of Ophiocoma aethiops Lutken and Ophiocoma alexandri Lyman were collected on the Pacific coast of Panama (at the study sites described in Hendler, 1979). Polychaetes were not found on those species, although B. exilis was re- ported from the region (Pauchald, 1977). B. exilis was not collected on O. echinata from other sites in the Caribbean. Samples of O. echinata from Cura~ao, Nassau, and Virgin Gorda (small because the species was uncommon at the sampling localities) showed no infestation by 738 BULLETIN OF MARINE SCIENCE. VOL. 32, NO.3, 1982

Table I. The numbers of three sympatric Ophiocoma species infested (with) or not infested (without) by the polychaete, Branchiosyllis exilis, at different collecting sites along the Caribbean coast of Panama

O. echinata O. wendt; O. pumila Locality (Panama) Date Without With Without With Without With

Galeta 24 X 1977 175 106 37 0 4 0 Galeta 21 IX 1978 170 93 45 0 5 0 Galeta 5 X 1980 27 23 5 0 I 0 Punta Guapa 29 V 1976 18 13 5 0 Largo Remo I IX 1974 69 78 II 0 Largo Remo 23 VIII 1977 36 2 5 0 Maria Chiquita 3 IV 1976 14 II 4 0 Achutupo, San BIas 25 VII 1977 I 1 4 0 Korbiski, San Bias 25 IX 1980 0 I 2 0

B. exi/is, More intensive surveys in Florida and along the Belize Barrier Reef (conducted from the U.S. National Museum Carrie Bow Cay Laboratory) and personal communications with Ms. Elizabeth Sides and Mr. Richard Bray who have carefully studied large numbers of O. echinata and other ophiuroids from Jamaica and Barbados indicate that B. exilis is not found on O. echinata on those islands (Table 2). B. exilis occurs on the arms or disc of its host. Unless disturbed, the polychaete moves along the ventral arm plates (that pave the oral surface of the ophiuroid arm) between alternating rows of arm spines and tube feet (Fig. 1). The poly- chaetes are also found partially or wholly within the oral cavity of the ophiuroid and they presumably enter the host's stomach. On occasions when the location of the polychaete could be found immediately upon collecting an ophiuroid, B. exilis occurred more frequently on the arms of the ophiuroid than on the disc (Table 3). The polychaetes generally occupied the thick, proximal portion of the ophiuroid arm, on the ventral (oral) surface. Polychaetes on the disc of the ophiu- roid were usually on the radial area at the base of the arm and the oral frame, rather than on the interradial or dorsal (aboral) areas of the disc. About 22% of the polychaetes surveyed were observed in the oral area, usually with a portion of their body hidden within the mouth of the ophiuroid (Table 3). On Ophiocoma, B. exi/is was difficult to secure with forceps but could be removed by vigorously shaking the ophiuroid in seawater. When disturbed (prod- ded with forceps) the polychaetes retreated between the arm spines, moved across the dorsal (aboral) surface of the ophiuroid arm, or moved onto the disc and possibly inside one of the host's bursae. Interestingly, when pursued the polychaetes did not take refuge in the oral cavity of the host even though they were capable of moving in and out of the ophiuroid's mouth. To find the relationship between the size of the host and the incidence of infestation, a series of O. echinata were inspected for B. exilis and measured. The superimposed size-frequency plots of infested and non-infested ophiuroids (Fig. 2) show a relatively greater incidence of infestation in the larger ophiuroid size classes. As expected, a regression of infestation (expressed as the percentage of infestation for each size class in Fig. 2) related to host size (Fig. 3) is significant (P < 0.05). The coefficient of determination (r2) indicates that 61% of the varia- tion in the percentage of infestation is a function of host size. Most infested ophiuroids carried but a single individual of B. exi/is. In a sample of 552 O. echinata, 8% of the ophiuroids hosted 2 polychaetes and only 3 spec- HENDLER AND MEYER: POLYCHAETE-OPHIUROID ASSOCIATION 739

Table 2. Incidence of infestation with Branchiosyllis exilis and relative abundance of Ophiocoma echinata (expressed as a percentage of the number of all species of ophiuroids collected) at all sites sampled for B. exilis

o. echinara No. Worms/Ophiuroid Percentage Locality Date N abundance Infestation

Galeta, Panama 9"24' 18"N, 79°51'52"W 1972-1980 960 40.6-41.9 42.2 365 37 3 Navy Site, Galeta, Panama 9°24'26"N,79"52'21"W 4 X 1974 27 - * 51.9 14 0 0 Punta Guapa, Panama 9"23'54"N, 79°51'20''W 29 V 1976 31 41.9 13 0 0 Largo Remo, Panama 9"24' 12"N, 79°50'57"W I IX 1974 147 53.1 73 5 0 23 VIII 1971 38 5.3 2 0 0 Maria Chiquita, Panama 9"26'55"N,79°45'51"W 3 IV 1976 25 44.0 10 0 Portobelo, Panama 9"33'29"N, 78°40'43"W 22 IX 1974 76 45.1 32.9 22 3 0 Salar, San BIas, Panama 9°30'27"N,78°48'27"W 9 XI 1974 7 15.2 29.6 2 0 0 Achutupu, San Bias, Panama 9"33'35"N, 78°52'40"W 25 VII 1977 2 1.6 50.0 0 0 Korbiski, San BIas, Panama 9"32'54"N, 78°51'43"W 25 IX 1980 1.4 100.0 0 0 Carrie Bow Cay, Belize W48.1 'N, 88°04.8'W 22 III 1979 50 0 0 0 0 I IV 1980 175 35.4 0 0 0 0 Looe Key, Florida, U.S.A. 24°33'00"N,81°24'30''W 12 IX 1981 60 0 0 0 0 Paradise Island, Nassau 25°05.I'N,77°18.0'W 31 III 1978 27 0 0 0 0 Piscadera Baai, Curapo 12°07'31"N, 68°58'03.3"W 27 IX 1976 15 0 0 0 0 South Sound, Virgin Gorda, BVI 18°29.0'N,64°23.0'W 15 I 1981 25 0 0 0 0

• Data unavailable.

imens in the sample each carried 3 associated polychaetes (Table 2). Unfortu- nately, the sizes and positions of the polychaetes in these cases of multiple in- festation were not recorded. Although O. echinata from 5 to 29-mm disc diameter were infested with B. exilis, only specimens 14-mm disc diameter and larger carried more than one polychaete. Thus, there is a tendency for multiple infes- tations to be restricted to the larger ophiuroids. At the primary study site (Galeta, Panama) O. echinata was reported in max- imum densities of 20 individuals per m2 (Birkeland et al., 1976) and we found that the overall incidence of infestation was 42.2%. A series of other sites in Panama was surveyed for O. echinata and B. exilis, and where the relative abundance of 740 BULLETIN OF MARINE SCIENCE. VOL. 32. NO.3, 1982

Table 3. Location of Branchiosy/lis exi/is found on Ophiocoma echinata discs, arms, and oral area immediately upon collection of the ophiuroid

Number of Branchiosyllis exilis Collected on:

Locality (Panama) Date Ann Disc Disc and Arm· Mouth

Galeta 24 X 1977 53 34 16 21 IX 1978 40 31 23 5 X 1980 9 5 9 Punta Guapa 29 V 1976 7 4 2 Navy Site, Galeta 4 X 1974 13 1 Largo Remo 1 IX 1974 56 22 Portobelo 22 IX 1974 22 3 Percentage 46.8 31.8 77.8* 21.7 Percentage of total 78.3t 21.7

* Figure for samples where counts on ann and disc were combined. t Figure for all specimens on either arm or disc.

O. echinata in relation to the occurrence of other ophiuroid species could be determined there seemed to be no correlation between the dominance of O. echinata and the frequency of infestation (Table 2). In different populations, infestation ranged from 5.3 to 100%, but some of the higher values are clearly artifacts of insufficient sample sizes. Fluctuations of the incidence of infestation at a single site, such as the shift from 5.3 to 53.1% at Largo Remo Island (Table 2), show that there may be con- siderable changes in population density between years. At Galeta the degree of infestation varied over time between 20 and 90%. B. exi/is was found on O. echinata throughout the year at the Galeta site (Fig. 4), but infestation was greatest from November to March, during the dry season, and the period of lowest infes- tation bracketed the local rainy season. Samples for the same months in different years proved that there was an impressive fidelity of the year to year counts to a regular, seasonal trend (Fig. 4).

90 21 N'22 50 80 19 17 '"••••... 70 16 17 ~'" 40 ...'" 15 30 '"... ~ 60 ~ ... • 10 ••• 50 50 ~ 3D CD 16 ... 19 CD .. 15~ 281 ~ 40 19 .. 263 •... • ... 15 18 ~ 20 17 ~ 30 15 16 u • Y=2o.84 + 0.92X ac: ...... 16 ... 20 ••.• 10 N=9 r = 0.18 10

1 1 13 19 25 31 JFMAMIJAS 0 NO SIZE [mm DISC DIAMETER) 1973 74 73 74 73 74 73 74 73 74 73 74 73 7374 7378 73 77 8072 7372 73

Figure 3. (Left) Relationship between the size of Ophiocoma echinata and the incidence of infes- tation with Branchiosyllis exilis. Based on values of the mean incidence of infestation for each of the size classes in Fig. 2. Figure 4. (Right) Seasonal fluctuations in the percentage of Ophiocoma echinata infested with Bran- chiosyflis exilis at Galeta, Panama. HENDLER AND MEYER: POLYCHAETE-OPHIUROID ASSOCIATION 741

Table 4. A comparison of the population density of Ophiocoma echinata and the duration of low water exposures of the middle zone of the reef flat during exceptional low tides at Galeta, Panama

Month (1976) F M A M A S 0 N D

Number of O. echinata per 20 m' 16 17 33 -* 31 33 37 40 38 Hr exposure per mot II 5 10 74 10 23 0 43 0 2 0 0

.• Data unavailable. t From Hendler (1977a).

A census of O. echinata from a 20 m2 transect at Galeta made several years after the seasonal survey for B. exilis did not show any fluctuations in the density of the ophiuroid population with dry/rainy seasons or with devastating exposures of the reef flat during extreme low tides (Table 4). However, along the same 20- m2 transect, 22 O. echinata were counted in August 1973 and 50 in August 1974 when the incidence of infestation was respectively 29 and 50%.

DISCUSSION Branchiosyllis exi/is has been reported in the Caribbean, the Eastern Pacific, and Hawaii (Fauchald, 1977; Hartmann-Schroder, 1978). Populations of the poly- chaete, or segments of populations, are free-living although Hartmann-Schroder (1978) did report it "among" (zwischen) ophiuroids. Therefore, at present the association of B. exi/is with O. echinata can be regarded as facultative. Further systematic investigations of B. exi/is could indicate that certain forms with con- stant color patterns, associated with specific hosts or habitats, are taxonomically distinct; in that case, the association discussed here might be viewed as obliga- tory. The pigmentation of B. exilis on O. echinata is darker than the fuscous col- oration reported for free-living individuals (Fauchald, 1977). However, it should be noted that the pigmentation of commensal polychaetes may vary on different hosts (Millot, 1953; Devaney, 1967; Gibbs, 1969). The unpublished results of a series of experiments performed by one of us (Hendler, in prep.) indicate that B. exi/is displays active recognition of its host and seeks out O. echinata in preference to other Ophiocoma species. This ability to detect and seek the host species has been used to distinguish commensal or parasitic symbiosis from fortuitous interspecific associations (Davenport, 1953; Clark, 1956). Although we have referred to the relationship between B. exilis and O. echinata using the neutral term "association," there is reason to suspect that the poly- chaete acts as a parasite in that it profits at the expense of its host (sensu Jennings, 1974). B. exilis has been found in the oral cavity of O. echinata, and as noted above it does not seek that area for shelter. Rather, it is possible that it steals food from the alimentary tract of its host. Moreover, the polychaete generally rests on the proximal portion of the ventral surface of its host's arms where it is directly in the path of food boluses passed by the tube feet to the mouth of the ophiuroid. Were the polychaetes present on the arms of the ophiuroid solely for physical protection, they might be expected to occur between the arm spines on the lateral surface of the arm as often as in the food canal on the ventral surface of the arm, but that is not the case, supporting the hypothesis that the polychaetes are "stealing" from their hosts. Clark (1956) noted that other syllid 742 BULLETIN OF MARINE SCIENCE, VOL. 32, NO, 3, 1982 species are associated with ascidians, nemerteans, polychaetes, and , and Paris (1955) concluded that symbiotic syllids are more often parasites than com- mensals. Interestingly, polychaetes associated with asteroids have been reported to enter the stomach of their hosts unharmed and in fact, experimental observations re- vealed one species that is resistant to digestion even when sealed inside the stomach of its host. In this example it is noteworthy too that the asteroid species captures and digests other species of polychaetes (Davenport, 1966), O. echinata has attributes that make it a favorable host for B. exilis. It is not a predator (and thus might not be expected to ingest a polychaete associate) but rather feeds on a broad size range of plant and materials and detritus (unpub. obs.). O. echinata is a relatively large and sedentary ophiuroid found from the shallowest reef areas to the deep fore-reef zones and it is one of the most common Caribbean ophiuroid species. It has been reported as a major macroinvertebrate constituent of the reef fauna in Florida (Kissling and Taylor, 1977) and Barbados (Bray, 1975) as well as in Belize and Panama (unpub. obs.), and its geographic range extends from Bermuda to Brazil (Clark, 1933).The direct relationship between host size and both the incidence of infestation and multiple infestation supports the possibility that the large size of an ophiuroid species such as O. echinata is a factor in the formation of a successful association. It seems enigmatic that despite the extensive geographic ranges of both species, B. exilis has been found associated with O. echinata only along the coast of Panama. Surveys in the Bahamas, British Virgin Islands, Jamaica, Belize, and Cura~ao have failed to detect infestations of Branchiosyllis (Table 2). The near absence of other commensal organisms on O. echinata suggests that the associ- ation with B. exi/is is not limited by competitive exclusion. The wide range of habitats occupied by the polychaete in Panama indicates that it is not restricted in its distribution through a paucity of suitable habitats. We would stress that in parts of its range B. exi/is may associate with hosts other than O. echinata. It is also possible that color morphs (identifiable as B. exi/is) from different habitats will eventually be recognized as distinct substrate-specific or host-specific taxa. The association of B. exilis and O. echinata is somewhat similar to that of the polynoid Gyptis ophiocomae Storch and Niggemann, with the ophiuroid Ophio- coma scolopendrina (Lamarck). G. ophiocomae has been found only in the Red Sea but its host ranges from the Indian Ocean across the Indo-Pacific region and Australia to Hawaii (Storch and Niggemann, 1967; James and Pearse, 1969; Clark and Rowe, 1971). In contrast another ophiuroid-associated polychaete, Holole- pidella nigropunctata (Horst), has been collected on four species of Ophiocoma from Aldabra, the Great Barrier Reef, the Marshall and Solomon Islands and Hawaii, as well as on Macrophiothrix belli (Doderlein), M. hirsuta (Muller and Troschel), Ophiarthrum elegans Peters, on the asteroids Acanthaster planci (L.) and Pentagonaster regulus (MUller and Troschel), and on the echinoid Diadema savignyi Michelin (Devaney, 1967; Gibbs, 1971; Gibbs et al., 1976; Sloan et at., 1979). B. exilis resembles H. nigropunctata in that it tends to occur singly on its host. Devaney (1967) discovered a mechanism for the one-per-host distribution of H. nigropunctata, in the tendency for the worms to attack each other when two or more polychaetes were confined together. Analogous experiments and related studies are needed to understand this and other aspects of the biology of B. exilis and its host. Unfortunately, we can suggest no convincing explanation for the variability in the incidence of infestation between sampling sites. Another observation begging an explanation is the seasonal occurrence of B. HENDLERANDMEYER:POLYCHAETE-OPHIUROIDASSOCIATION 743 exilis that was detected at Galeta, Panama. The decreased incidence of infestation during the rainy season could be the result of seasonal changes of salinity and other environmental parameters or annual fluctuations in the mortality of the polychaetes resulting from the seasonal, low-tide emergence of the reef flat. Such periods of exposure result in mass mortalities of marine shallow-water species in Panama and elsewhere in the Caribbean (Glynn, 1968; Hendler, 1977a; b). It is also possible that the size of the B. exilis population is constant and that the percentage of infestation is a function of fluctuations in the density of the host's population. In any case, the positive correlation between host density and the incidence of infestation in evidence at Galeta in 1974, could not be linked to seasonal effects such as reef flat exposures. Unfortunately, the relationship be- tween the abundance of O. echinata and B. exilis cannot be distinguished using the data available. Therefore, additional research is required to test alternative hypotheses for the population fluctuations of B. exilis.

ACKNOWLEDGMENTS

We are particularly indebted to Dr. K. Fauchald (National Museum of Natural History) for iden- tifying our material of Branchiosy//is exi/is, and for commenting on its systematic status. For their assistance in collecting samples used in this study we are grateful to the survey team supported by EPA Contract #]4-12-874 to the Smithsonian Tropical Research Institute, namely Drs. C. Birkeland and A. Reimer, Mrs. I. Tumlin and C. Buford, Mr. J. Stames, and also to Ms. K. Dunlap, J. Lee, B. Littman, and S. Williams. We thank the Kuna people of Panama for their permission to do research in the San BIas Islands. We wish to express our appreciation to the Smithsonian Tropical Research Institute for the use of the Galeta Marine Laboratory facilities and our thanks to Capt. J. Bryan, master of the R/V STENELLAand Mr. T. Borges for logistic support. For information on the occur- rence of B. exi/is on O. echinata we are indebted to Ms. E. Sides (Discovery Bay Marine Laboratory), Mr. R. Bray (University of Cincinnati), Ms. J. Clark and Dr. D. Pawson (National Museum of Natural History). Suggestions from Dr. D. Pawson, Ms. M. Downey and an anonymous reviewer improved the manuscript. Research at the Carrie Bow Cay Laboratory, Belize, was carried out under auspices of an Exxon Grant to Dr. K. Ruetzler (National Museum of Natural History), and travel to Panama and Belize was supported by the Research Fund of the Secretary, Smithsonian Institution.

L[TERA TURE C[TED

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DATE ACCEPTED: September 30, 1981.

ADDRESSES:(G.H.) Smithsonian Oceanographic Sorting Center, Smithsonian Institution, Washing- ton, D.C. 20560; (D.L.M.) Department of Geology, University of Cincinnati, Cincinnati, Ohio 4522/.