1. Introduction

Remora or diskfish species of the family Echeneidae can be found on a wide variety of hosts including teleost fishes, marine mammals, turtles, sharks, and even conspecifics [1, 2]. This relationship is widely known, but the costs and benefits of this interaction for the echeneids and their hosts remain poorly understood [1, 3–5]. The most-cited possible benefit for the host is cleaning through the removal of parasites and diseased or injured tissue [5–7], but little quantitative data is available to support this hypothesis. Echeneids are reported to feed—at least to some extent—on ectoparasites, but the relative importance of parasites as a food source varies with the echeneid species involved [2, 6].

This study presents data on echeneid and ectoparasite presence from two shark host species. We use these data to address two working hypotheses: (1) if certain echeneid species actively feed on ectoparasites found on the host’s skin, then shark individuals with ectoparasites would host echeneids with a greater frequency than individuals with no detectable parasites on their skin; and (2) the number of ectoparasites on sharks would be negatively correlated to the number of echeneids present.

2. Materials and Methods

Echeneid and ectoparasite presence was recorded for two shark host species: the whale shark Rhincodon typus, and the shortfin mako, Isurus oxyrinchus. Both species are known to host different echeneid species [2]. The first hypothesis was tested using data from both hosts, whereas the second hypothesis was tested using data from mako sharks only.

Digital photographs of free-swimming whale sharks were taken opportunistically between October 2005 and January 2007 off the coast of Tofo Beach, Southern Mozambique. Each photograph of sufficiently high quality was visually searched for echeneids. For sharks that we were able to examine comprehensively (head, caudal area, fins, dorsal, as well as lateral and ventral surfaces), each photograph was additionally searched for ectoparasites larger than about 1 cm length or width and their position on the shark’s body was recorded.

Mako sharks were captured by a Spanish commercial surface longline fishing vessel targeting swordfish, Xiphias gladius, in the South Pacific between December 2004 and March 2005. Hooked sharks were hoisted onto the deck, at which time echeneids would usually detach from the host and could be counted. Echeneids were photographed for later analysis and immediately returned to sea after detachment from the sharks. The external surfaces of the sharks were then visually examined for the presence of ectoparasites and the number and position of parasites were recorded for each shark.

The echeneid species attached to either host were identified from the best-quality photographs. These were enlarged, analysed for body proportions and shapes, scrutinised for diagnostic features, and checked against digital or digitalised photographs and drawings of all presently recognized echeneid species [8]. To determine parasite distribution on the whale and mako sharks, the host’s body was divided into “microhabitats.” Analyzed data are reported as means  ±  S.D.

3. Results

3.1. Whale Sharks

A total of 3606 photographs were taken during 309 whale shark encounters. Sharks had detectable associated echeneids in 47 cases. Two echeneid species were positively identified: Echeneis naucrates was present in 21 and Remora brachyptera in 5 cases. The remaining echeneids could not be reliably identified to species level based on the photographs. The number of echeneids on a single shark was estimated to be between 1 and about 35 individuals (free-swimming E. naucrates; Figure 1(a)). Whale sharks could be examined comprehensively in 54 cases (17.5%). Ectoparasites on these whale sharks were identified as representatives of the copepod family Pandaridae similar to those described in [9]. A percentage of 30.6% of whale sharks with detectable parasites also had associated echeneids (Figure 1(b)). Ectoparasites were most frequently found on the head (Figure 1(c)). Where both organisms were observed on the same whale shark host (), echeneids could be found on several body microhabitats, including free-swimming (=  microhabitat L) close to the shark’s body, but mostly (66.7%) on the head where also parasites were located (Figure 1(c)).

Figure 1: Whale sharks photographed off Tofo Beach, Mozambique, with (a) a group of free-swimming Echeneis naucrates (microhabitat L); (b) frequencies of presence of ectoparasites and echeneids on 54 comprehensively sampled whale sharks (E  =  echeneids; P  =  parasites); (c) frequency of ectoparasite presence per microhabitat observed on whale sharks with (white bars) and without (black bars) echeneids.

3.2. Shortfin Makos

A total of 224 shortfin makos were examined, of which 68 had a total number of 128 echeneids attached (). All echeneid individuals were positively identified as Remora osteochir and ectoparasites were identified as Pandaridae and Caligidae (Figures 2(a), 2(b)). The recorded number of visible ectoparasites on 175 sharks was 5036 (). Of these, average parasite load on sharks with echeneids attached (22.3%; Figure 2(c)) was about a half compared to mako sharks without echeneids attached ( versus 32  ±  35.8). Ectoparasites were found on all microhabitats (except free-swimming) with most sharks having parasites attached on C, D, and G, respectively, when no echeneids were present (Figure 2(d)). Individual sharks had parasites attached to an average number of 3.7 (±2.1) microhabitats. When both organisms were present on the shark, most hosts had ectoparasites attached to microhabitats D, G, and H (Figure 2(d)). In this case, individual sharks had parasites attached to an average number of 2.2 (S.D.  =  1.3) microhabitats. The number of ectoparasites on mako sharks decreased with an increasing number of attached echeneids (, Figure 3).

Figure 2: (a) A live Remora osteochir from a mako shark; (b) ectoparasites (Pandaridae) attached to microhabitat C close to the pelvic fins of a male mako shark; (c) frequencies of presence of ectoparasites and echeneids on mako sharks (E  =  echeneids; P  =  parasites); (d) frequency of ectoparasite presence per microhabitat observed on mako sharks with (white bars) and without (black bars) R. osteochir attached.

Figure 3: Average number (+ S.D.) of ectoparasites on mako sharks with between 0 and 5 R. osteochir attached to the same individual. Only two individuals with  >5 echeneids attached to their bodies were captured. E echeneids; P parasites.

4. Discussion

Our data from whale and mako sharks do not lend conclusive support to the first hypothesis (Figures 1(b), 2(c)) which is based on the assumptions that parasites are the primary driver of echeneid host selection and/or that echeneids are able to assess host parasite loads. However, it is possible that echeneids choose hosts opportunistically and feed on ectoparasites nonselectively. With no data to test the two above-mentioned assumptions but data from mako sharks that support the second hypothesis (Figure 3), our results indicate that echeneids do regulate ectoparasite numbers—at least to some extent and probably dependent on the echeneid and ectoparasite species involved (see below)—and thereby reduce the number of the latter on the host’s body.

Ectoparasites were most commonly observed in a single microhabitat on whale sharks and in multiple microhabitats on mako sharks. Copepods are known to prefer specific locations on the bodies of their elasmobranch hosts [10], which has been hypothesised to decrease the exposure to adverse abiotic or biotic factors including predation by fishes [11]. However, in whale sharks, echeneids were also found most likely on the head when ectoparasites were present at the same time, which indicates that this particular microhabitat offered no protection from potential echeneid predation.

Both Xiphias gladius and Isurus oxyrinchus are known hosts for Remora osteochir although the latter association has been documented only once in the literature [2]. O’Toole [2] regards this echeneid species to be a pelagic obligate restricted to a small group of hosts, mostly billfishes. Diet data indicate that R. osteochir regularly feeds on different species of parasitic copepods [6, 12]. For whale sharks in this study, both species of echeneids reported were not previously listed to be associated with this particular host species [2]. About one third of the whale sharks that were infected with pandarid copepods also had associated echeneids. This could be related to the prevalence of E. naucrates, for which parasites are not an important food ([2, 6, 13] but see [4, 7]). Additionally, most individuals were free-swimming under the ventral surfaces of whale sharks while observed, which could indicate that these echeneids were not actively feeding at the time of our observations although there is a possibility that they were ram-feeding on plankton. For R. brachyptera, parasites are generally considered a moderately important food item [2, 10, 14].

A number of methodological limitations are evident in our study. For example, we were only able to sample a relatively small number of free-ranging whale sharks conclusively (covering the entire body surface) and only were able to detect large ectoparasites on photographs. We might also have missed smaller echeneid species and/or individuals that would feed on parasites in the mouth or gill chambers of whale sharks. These constraints likely result in underestimating the actual ectoparasite and echeneid load. Furthermore, we were not able to quantify the degree of echeneid detachment and/or microhabitat changes (if any actually occur) for hooked mako sharks while still in the sea. Future studies looking at the degree of importance of ectoparasites to different echeneid species should also look at their gut contents. We nevertheless are confident that our study adds a novel approach to the understanding of the little known and elusive host-echeneid association and underpins the need for observational data from free-ranging animals that can be combined with information collected on commercial fishing vessels.

Acknowledgments

Thanks to Instituto Español de Oceanografía (Coruña) and Andrés Paz and crew of the vessel “Maicoa Dos” for assistance and collaboration with mako shark fieldwork. Andrea Marshall and Tofo Scuba assisted with whale shark fieldwork. J. M. Brunnschweiler is supported by the Save Our Seas Foundation, the Shark Foundation Switzerland, Project AWARE (UK) and he acknowledges the Swiss National Science Foundation Grant no. 11 9305/1 for partial funding during the preparation phase of this manuscript. I. Sazima thanks the CNPq for essential financial support. N. Queiroz was funded by Fundação para a Ciência e a Tecnologia (FCT) Grant SFRH/BD/21354/2005. S. J. Pierce is supported by Casa Barry Lodge, Project AWARE (UK), PADI Foundation, and the Save Our Seas Foundation. Fran Saborido and Juan Santos are gratefully acknowledged for technical assistance and advice. The valuable comments from two anonymous referees that substantially improved this manuscript are greatly appreciated.