Parasitic Copepods from Pelagic Sharks in Western Australia

BULLETIN OF MARINE SCIENCE, 65(3): 715–724, 1999

PARASITIC COPEPODS FROM PELAGIC SHARKS IN WESTERN AUSTRALIA

Dennyse R. Newbound and Brenton Knott

ABSTRACT This first attempt to elucidate elasmobranch-copepod associations from Western Aus- tralian waters revealed 17 species of commensal copepod from four species of pelagic shark (Galeocerdo cuvier, Carcharhinus obscurus, Carcharhinus plumbeus, and Carcharhinus amblyrhynchos). The copepods represented the families Pandaridae, Euphoridae, Eudactylinidae, Kroyeridae and Caligidae. Praniza stage gnathiids were also common and other symbionts comprised species of Hirudinea, an ostracod and a sphaeromatid isopod. A predominance of tiger sharks (G. cuvier) were caught throughout the study area, which extended from the Montebello Islands to Shark Bay. There was a bias toward female tiger and sandbar (C. plumbeus) sharks caught, and a difference in the infection of tiger sharks in the north and southern regions of the study area. Several hypotheses are suggested: population differentiation of the tiger sharks, population differentiation of the copepods or ecophysiological differences in the two regions. Two major patterns were identified in the distribution of the copepods on hosts: those which occur generally on the body surface of their hosts and had a geographical distribution throughout the entire study area, and those which have a specific body location and a more restricted geographic distribution. Nemesis robusta is the one exception to this rule, as it has a wide geographic distribution, yet is restricted in site of attachment.

Numerous associations between symbiotic copepods and teleost or elasmobranch fishes have been observed. While elasmobranch-symbiont interactions have been extensively recorded within some oceans, notably the North Atlantic (Cressey, 1967a; Kabata, 1979) and South Atlantic oceans (Rokicki and Bychawska, 1991), knowledge pertaining to ex- amples from other oceans is, by comparison, meagre. Elasmobranch-copepod interactions have never been specifically described for the waters along the Western Australian coast, and there is little known about the general pattern of such associations within the Indian Ocean (e.g., Cressey, 1967b). Studies of this nature within Australian waters are also limited (e.g., Cressey and Simpfendorfer, 1988), although Grutter (1994) described spatial and temporal patterns of ectoparasitic load on coral reef fishes from the Great Barrier Reef, Queensland. There is a wide variety of associations between copepods and their fish hosts. How- ever, little is known about these associations and their biological nature. Host-symbiont associations range from commensalism, where copepods have a life stage restricted to their host but there is little physiological dependence on the host, to parasitism, where there is significant metabolic dependence on the host. The extreme forms of parasitism are presumably a result of long term co-evolutionary events. This study provides the first description of copepod-elasmobranch faunal associations in Western Australian coastal waters and was derived from a biological survey of sharks between the Montebello Islands and Shark Bay undertaken by Fisheries Western Austra- lia in July 1997. The microhabitats occupied by the copepod fauna on shark hosts were examined. In contrast to those studies where the copepod specimens were dissociated

715 716 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 3, 1999 from the host before examination, this study had the advantage of observing both the hosts and the symbionts immediately following capture.

MATERIALS AND METHODS

The study site extended 700 km along the Western Australian coast, from west of the Montebello Islands (20°28'25S 115°24'24E) to west of the Peron Peninsula (25°51'75S 113°14'89E) (Fig. 1). The geographic distribution of shark capture shown in Figure 1 can be divided into two separate areas; north and south of an approximate midline (23°S latitude) through the travel route of the R/V FLINDERS. This provides a convenient reference from which it is possible to assess any bias in catch rates. Sharks were caught using set-line fishing with hooks set in the evenings, and retrieved the following morning. Sex, total length, (TL: measured snout to dorsal tip of caudal fin) fork length (FL: measured snout to fork in caudal fin) and sexual maturity were recorded for each shark. Sharks were examined immediately following retrieval. The dorsal and ventral body surfaces of each shark were examined, as were the surfaces of fins, tail and eyes. Incisions were made to extend the gill slits to allow a thorough examination of the gill filaments. The openings of the external nares were extended to enable examination of the internal nares. Parasites were located visually and removed with forceps, then stored in seawater. Specimens were examined under an Olympus field binocular microscope within 10 h of removal from the host, then transferred to a solution of either 10% neutral, saline buffered formalin; 80% ethanol or Karnovsky’s solution. For identification, parasites were dissected and examined under a Wild Leitz dissecting microscope and Olympus BH-2 compound microscope in either 80% alcohol or a 0.1M phosphate wash buffered solution, at pH 7.4. Identification was based on keys and descriptions in Yamaguti (1963), Cressey (1967a) and Kabata (1979). Prevalence (% fish infected) and mean intensity (mean number of a particular copepod species on each infected fish) were calculated (Margolis et al., 1982). Spearman Rank Correlations between copepod intensity and total length of host were calculated. Sex ratio and geographic differences in species composition were tested using Chi-squared goodness of fit analysis. A contin- gency Chi-square test was used to examine geographic differences with copepod infection. Pre- ferred associations with host species and locations on the host were noted. Other surface dwelling symbiotic taxa were noted.

RESULTS

Seventy-eight sharks belonging to five species: tiger shark, Galeocerdo cuvier (Peron and Le Sueur, 1822); dusky shark, Carcharhinus obscurus (Le Sueur, 1818); sandbar shark, Carcharhinus plumbeus (Nardo, 1827); grey reef shark, Carcharhinus amblyrhynchos (Bleeker, 1856); and scalloped hammerhead shark, Sphyrna lewini (Griffith and Smith, 1834) were examined. The three most commonly caught shark species did not exhibit any obvious trends in spatial distribution, ranging throughout the study area, from 20°S latitude to 25°30'S (Fig. 1). With regard to the small-scale distribution of sharks, the highest diversity was observed to the west of Barrow Island. The two coastal grids (22°30'S 114°E and 24°30’S 113°30'E) exhibit a predominance of sandbar sharks, while there is an absence of this species in Shark Bay, and to the west of Thevenard Island. The Shark Bay region appears to be dominated by tiger sharks. There was no significant difference, as judged by goodness of fit Chi-squared analysis, between the total numbers of sharks caught in the northern and southern regions for tiger sharks, dusky sharks and sandbar sharks. More females than males were caught for both sandbar and tiger sharks. NEWBOUND AND KNOTT: COPEPOD DISTRIBUTION ON SHARKS IN WESTERN AUSTRALIA 717

Figure 1. Distribution and composition of shark species caught along the north-west coast of Western Australia, showing capture per quadrat (30' dimensions). Inset: the study area of the north-west coast of Western Australia.

G. cuvier captured in the southern region were more commonly infected with copepods. There was no significant difference in infection proportions on male and female tiger sharks. A significant correlation was observed between length of the host and the number of copepod species found on tiger sharks using the fork length of both tiger sharks (n = 28, 718 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 3, 1999

Z = 2.314, P =0 .0207), but not total length (TL and number of species: n = 28, Z = 2.421, P = 0.155), and dusky sharks (n = 10, Z = −2.335, P = 0.019). No significant correlation was observed between host length and the abundance of copepods on each host for any of the shark species. All sharks were captured in shallow water (9–72 m depth) with G. cuvier extending more frequently into very shallow water (<20m) than any of the either species caught. No trends were evident in the data with regard to copepod species or rate of infections with depth. Seventeen species of parasitic Copepoda were collected from elasmobranch hosts. Fifty- eight of the 78 (74.4%) sharks examined were infested with Copepoda (Table 1). Within the majority of the grids, there was a high diversity of commensal and parasitic copepods. Two grids; the grid to the east of the Montebello Island, and the grid to the west of Thevenard Island showed a species diversity lower than other grids. While the lowered diversity to the west of Thevenard Island may be linked to the absence of sandbar sharks caught, there was no noticable difference in the composition of host species to the east of the Montebello Islands. Three large-scale patterns of spatial distribution for copepods were observed (Table 1) along the coast of Western Australia (Fig. 2). Some species were distributed throughout the entire study area, for example Alebion carchariae; some species were restricted to the northern study area, for example Eudactylina acuta; and other species were only collected from Exmouth Gulf to Shark Bay. Eight copepod species exhibited a distinct host preference, being observed on a single shark species (Table 1). G. cuvier was infected by a broad range of parasitic and commensal copepods. While A. carchariae were prevalent on all three of the commonly caught host species, C. plumbeus was the most common host, with the highest prevalence (66.7%) and mean intensity. G. cuvier appears to be the most common host for Nesippus crypturus, with a prevalence of 59.5%, compared to 11.1% for C. plumbeus. The mean intensity was 53.3 individuals per host for G. cuvier, as compared to 12.5 individuals per C. plumbeus. Several other symbionts were observed on the sharks (Table 2). Praniza (larvae) of gnathiid isopods were commonly found on the gills of C. plumbeus, C. obscurus, C. amblyrhynchos and G. cuvier. Praniza were found on sharks throughout the study site. Other ectoparasites occurred infrequently on shark hosts.

DISCUSSION

This is the first description of elasmobranch-copepod associations in a biogeographi- cal context, from Australian waters. The seventeen taxa of copepod represent eight genera which are restricted to elasmobranch hosts (Yamaguti, 1963), with only Caligus better known from teleosts than elasmobranchs (Kabata, 1979). None of the species display extreme morphological specialisation for parasitism, but there is evidence of trends in relationships between niche width (as measured by the points of attachment to the host) and extent of geographical range. Two categories were identified: those copepods which occur generally on the body surface and have a geographical distribution throughout the entire study area (e.g., A. carchariae); and those which have a specific body location and a more restricted geographic distribution (e.g., N. crypturus, E. acuta and Caligus sp. nov.) (Table 1). Nemesis robusta defines a third category; it was widespread in geographic NEWBOUND AND KNOTT: COPEPOD DISTRIBUTION ON SHARKS IN WESTERN AUSTRALIA 719

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Figure 2. Distribution and composition of copepod species commensal or parasitic on sharks along the north-west coast of Western Australia, showing species collected per quadrat (30' dimensions). distribution, yet restricted in site of attachment. Insufficient data were available to elucidate the underlying causal processes generating these patterns. It may be relevant to ob- serve that the sampling areas north of Exmouth Gulf occur in water outside the Leeuwin Current; those south of Exmouth Gulf may come under the influence of the temperature NEWBOUND AND KNOTT: COPEPOD DISTRIBUTION ON SHARKS IN WESTERN AUSTRALIA 721

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and salinity conditions of the Leeuwin Current, and consequently associated fauna expe- rience quite different ecophysiological conditions. These categories may reflect the nature of the trophic relationships between the symbiont and its host. Copepods of the genus Pandarus, for example, are generally located on the body surface and fins of elasmobranchs (Yamaguti, 1963). Although Pandarus is usually regarded as an ectoparasite (Kabata, 1979), Pandarus sp. removed from the surface of the whale shark, Rhincodon typus at Ningaloo Reef, Western Australia are prob- ably commensal (Norman and Newbound, unpubl. observ.). In such a system, the shark may simply function as an unspecialised substrate on which micro-organisms grow; the association is not based on any specialised requirements. The attachment site of members of the genus Pandarus in this study was also consistent with copepods grazing on microbiota on the skin of the shark. The unspecialised nature of copepods grazing on shark skin is also indicated by the observation that most shark hosts had very low numbers of Pandarus specimens but usually had a species richness that approached the total abundance of copepods for each shark. The rhomboidal arrangement of Pandarus satyrus (Benz, 1981; Rokicki and Bychawska, 1991) which is believed to strengthen the attachment to the host, was not observed for any of the Pandarus species in this study. Instead, all Pandarus specimens were attached singularly and oriented with the cephalothorax facing towards the front of the shark. Copepods that had a specific body location and a more restricted geographic distribution are likely to reflect a specialized association with their hosts. The site of attachment of Caligus sp. (exclusively on the surface of the eye) and N. robusta, E. acuta and Kroyeria spp. (only within the gill filaments) is indicative of a narrow attachment niche for these species. However, the attachment site for some copepods may differ between different host species. Nesippus crypturus was found in the buccal cavity and extending out toward the inner gills on C. plumbeus, but the predominant site of attachment in G. cuvier was the nasal cavity. This apparent niche shift did not appear to result from competitive displacement, as has been suggested for niche shifts observed in other parasitic copepods (Hewitt, 1979), as neither location was occupied by any other species of copepod. The difference in location may reflect a difference in the site of resource availability for each shark species. For example, the internal nares of G. cuvier provided a larger space and contained a mucilaginous substance. Rokicki and Bychawska (1991) recorded Kroyeria 722 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 3, 1999

carchariaeglauca from the nasal cavity and Benz (1986) from “the excurrent water chan- nels between the gill filaments”. Kroyeria species observed on G. cuvier in this study were only found in the gill cavity. While similar species of sharks (three) and copepods (six) were reported in the Indian Ocean by Cressey (1967b) to those reported in this paper, there is little overlap in the specific associations between host and parasite. The only association observed in both studies is that which exists between N. crypturus and G. cuvier. The elasmobranch-copepod associations recorded here are also comparable in part with data provided by Rokicki and Bychawska (1991) in the Atlantic Ocean. The copepods on C. obscurus in both oceans were restricted to the genera Pandarus and Alebion. Indeed, the two Pandarus species from C. obscurus in this study (P. cranchii and P. smithii) were the same two species as listed by Rokicki and Bychawska (1991). However, there is no similarity in the copepod species assemblage on C. plumbeus between the two studies. Although a wide range of copepods have previously been found on Sphyrna lewini (Lewis, 1966; Cressey, 1967a; Benz, 1986; Rokicki and Bychawska, 1991), no copepods were found on the single speci- men caught in this study. It will be important to determine whether such differences in the copepod fauna can be used as biological tags to distinguish shark populations, as has been suggested by Lester (1990). Gnathiid praniza larvae are ectoparasitic on fish (Green, 1961, Naylor, 1972, Grutter, 1994) and in this study were found in the gill cavity, having a gut distended with blood. Leeches were also distended, and firmly attached to gill filaments. Ostracods have been recorded as scavengers/micropredators on fish (Stepien and Brusca, 1985), with Bennett et al., (1997) providing evidence of Sheina orri (Cyprinidae) parasitic on the gills of the epaulette shark (Hemiscyllium ocellatum). The trophic status of the sphaeromatid isopod is unknown. The lack of keys for identifying male copepods, particularly of the genus Pandarus (Nogaus), to species poses a problem for studies of this kind. As extensive keys for the identification of male Pandarus are not available, it has typically been assumed that the coexistence of a male and female copepod on the same host suggested that both individuals were of the same species (Yamaguti, 1963). However, as males were found on the same host as a number of female individuals of differing species, it was not possible in this study to make a reliable association. Male members of Alebion were only found occurring with female members of A. carchariae, suggesting the males were also of this species. However, two male morphs were observed, possibly representing two different species or two different developmental stages. As a result of this uncertainty, the males were treated as two species. While this increased the species richness of copepods on the sharks, it would have decreased the mean intensity values for A. carchariae. Since the study was restricted to shallow water (<75m) environments and did not bridge a main zoogeographic discontinuity, we expected to find a uniformity between type, sex and infection of the shark hosts throughout the area. The greater numbers of tiger sharks caught presumably reflected the abundance of the species in this region. The bias towards female sharks is not surprising, as sexual segregation has been observed for a number of elasmobranch species (Klimley, 1987; Stevens and McLoughlin, 1991; Wetherbee, 1996). A bias towards females sandbar and tiger sharks was recorded from sharks caught in the northern regions of Australia (Stevens and McLoughlin, 1991), while Joung and Chen (1995) found a 1:1 sexual ratio of sandbar sharks. As suggested by these authors, sexual NEWBOUND AND KNOTT: COPEPOD DISTRIBUTION ON SHARKS IN WESTERN AUSTRALIA 723 segregation may occur as a result of intra- or interspecific competition, migration or increasing female fitness for reproduction (Klimley, 1987). While other studies have reported an increased copepod load with increased host size (e.g., Bortone et al., 1978; Payne, 1986), this study did not find an increase in abundance of parasites. However an increase in the diversity of copepods with increasing lengths of tiger sharks and dusky sharks was observed. It is possible that competition for space (i.e., competitive displacement on smaller hosts) is a factor, or that colonisation rates are so low that only older (larger) sharks accumulate large numbers of species. A species (of copepod)—area (size of individual shark) relationship could reflect some purely passive mechanism for this pattern. The factors which control the difference in infection of tiger sharks in the northern and southern areas with no difference in numbers of hosts caught remain unknown. Several hypotheses are plausible: a population differentiation of the tiger sharks (i.e., two separate tiger shark populations); population differentiation of the copepods; or ecophysiological (temperature and salinity) differences generated by the Leeuwin Current. Although a 700 km transect is a large sample size, it nevertheless represents less than 6% of the Western Australian coastline and did not cross a major climatic or biogeo- graphic boundary. It will be important in future studies of copepod-shark evolution to cover a broader geographic area as well as determine whether the categories of copepod distribution are evident in benthic shark species.

ACKNOWLEDGMENTS

We thank C. Simpfendorfer, the Shark section of Fisheries Western Australia and the crew of the R/V FLINDERS for their continued assistance in gaining access to sharks, and the Department of Zoology, The University of Western Australia for funding this project. We also thank C. Simpfendorfer, R. Black and M. Heupel for their comments on the manuscript and T. Stewart for his assistance with the figures.

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DATE SUBMITTED: August 25, 1998. DATE ACCEPTED: February 16, 1999.

ADDRESS: Department of Zoology, The University of Western Australia, Nedlands, 6907 Australia.