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  • 8/14/2019 Hindawi Publishing Corporation Research Letters in Ecology Volume 2008, Article

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    Hindawi Publishing CorporationResearch Letters in EcologyVolume 2008, Article ID 107576, 4 pagesdoi:10.1155/2008/107576

    Research Letter

    Is Host Ectoparasite Load Related to Echeneid Fish Presence?

    Gonzalo R. Mucientes,1 Nuno Queiroz,2, 3 Simon J. Pierce,4, 5 Ivan Sazima,6 and Juerg M. Brunnschweiler7

    1 Instituto de Investigaciones Marinas, IIM-CSIC, Eduardo Cabello 6, 36208 Vigo, Spain2 Centro de Investigacao em Biodiversidade e Recursos Geneticos (CIBIO), Campus Agrario de Vairao,

    Rua Padre Armando Quintas, 4485 Vairao, Portugal3Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, PL1 2PB, UK4 Foundation for the Protection of Marine Megafauna Tofo Beach, Mozambique5 School of Biomedical Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia6Museu de Zoologia, IB, Universidade Estadual de Campinas, 13083-970 Campinas, SP, Brazil7Swiss Federal Institute of Technology, Raemistrasse 101, 8092 Zurich, Switzerland

    Correspondence should be addressed to Juerg M. Brunnschweiler, [email protected]

    Received 15 September 2008; Accepted 4 December 2008

    Recommended by Mark Gibbons

    This study used field data of echeneid and ectoparasite associations with free-swimming whale sharks (Rhincodon typus) andcaptured mako sharks (Isurus oxyrinchus) to test whether (1) echeneid presence was positively correlated with ectoparasitepresence; and (2) the number of ectoparasites was negatively correlated with the number of echeneid fish. Data from whale andmako sharks do not support the first hypothesis whereas data from mako sharks yields support for the second hypothesis. Theresults indicate that echeneids do regulate the number of ectoparasites on at least some host species, but these benefits may becontingent on the echeneid species.

    Copyright 2008 Gonzalo R. Mucientes et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

    1. INTRODUCTION

    Remora or diskfish species of the family Echeneidae can befound 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 costsand benefits of this interaction for the echeneids and theirhosts remain poorly understood [1, 35]. The most-cited

    possible benefit for the host is cleaning through the removalof parasites and diseased or injured tissue [57], but littlequantitative data is available to support this hypothesis.Echeneids are reported to feedat least to some extentonectoparasites, but the relative importance of parasites as afood source varies with the echeneid species involved [2, 6].

    This study presents data on echeneid and ectoparasitepresence from two shark host species. We use these datato address two working hypotheses: (1) if certain echeneidspecies actively feed on ectoparasites found on the hostsskin, then shark individuals with ectoparasites would hostecheneids with a greater frequency than individuals with nodetectable parasites on their skin; and (2) the number of

    ectoparasites on sharks would be negatively correlated to thenumber of echeneids present.

    2. MATERIALS AND METHODS

    Echeneid and ectoparasite presence was recorded for twoshark host species: the whale shark Rhincodon typus, and theshortfin mako, Isurus oxyrinchus. Both species are known

    to host different echeneid species [2]. The first hypothesiswas tested using data from both hosts, whereas the secondhypothesis was tested using data from mako sharks only.

    Digital photographs of free-swimming whale sharks weretaken opportunistically between October 2005 and January2007 off the coast of Tofo Beach, Southern Mozambique.Each photograph of sufficiently high quality was visuallysearched for echeneids. For sharks that we were able toexamine comprehensively (head, caudal area, fins, dorsal, aswell as lateral and ventral surfaces), each photograph wasadditionally searched for ectoparasites larger than about 1 cmlength or width and their position on the sharks body wasrecorded.

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    Mako sharks were captured by a Spanish commercialsurface longline fishing vessel targeting swordfish, Xiphiasgladius, in the South Pacific between December 2004 andMarch 2005. Hooked sharks were hoisted onto the deck,at which time echeneids would usually detach from thehost and could be counted. Echeneids were photographed

    for later analysis and immediately returned to sea afterdetachment from the sharks. The external surfaces of thesharks were then visually examined for the presence ofectoparasites and the number and position of parasites wererecorded for each shark.

    The echeneid species attached to either host were identi-fied from the best-quality photographs. These were enlarged,analysed for body proportions and shapes, scrutinised fordiagnostic features, and checked against digital or digitalisedphotographs and drawings of all presently recognized ech-eneid species [8]. To determine parasite distribution on thewhale and mako sharks, the hosts body was divided intomicrohabitats. Analyzed data are reported as means S.D.

    3. RESULTS

    3.1. Whale sharks

    A total of 3606 photographs were taken during 309 whaleshark encounters. Sharks had detectable associated echeneidsin 47 cases. Two echeneid species were positively identified:Echeneis naucrates was present in 21 and Remora brachypterain 5 cases. The remaining echeneids could not be reliablyidentified to species level based on the photographs. Thenumber of echeneids on a single shark was estimated tobe 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 thesewhale sharks were identified as representatives of the cope-pod family Pandaridae similar to those described in [9]. Apercentage of 30.6% of whale sharks with detectable parasitesalso had associated echeneids (Figure 1(b)). Ectoparasiteswere most frequently found on the head (Figure 1(c)). Whereboth organisms were observed on the same whale sharkhost (n = 15), echeneids could be found on several bodymicrohabitats, including free-swimming (= microhabitat L)close to the sharks body, but mostly (66.7%) on the headwhere also parasites were located (Figure 1(c)).

    3.2. Shortfin makos

    A total of 224 shortfin makos were examined, of which 68had a total number of 128 echeneids attached (1.9 1.3).All echeneid individuals were positively identified as Remoraosteochir and ectoparasites were identified as Pandaridaeand Caligidae (Figures 2(a), 2(b)). The recorded number ofvisible ectoparasites on 175 sharks was 5036 (28.1 33.5).Of these, average parasite load on sharks with echeneidsattached (22.3%; Figure 2(c)) was about a half compared tomako sharks without echeneids attached (17.5 34.5 versus32 35.8). Ectoparasites were found on all microhabitats(except free-swimming) with most sharks having parasitesattached on C, D, and G, respectively, when no echeneids

    (a)

    E and PP onlyE onlyNo E and P0

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

    were present (Figure 2(d)). Individual sharks had parasitesattached to an average number of 3.7 (2.1) microhabitats.When both organisms were present on the shark, mosthosts had ectoparasites attached to microhabitats D, G,and H (Figure 2(d)). In this case, individual sharks hadparasites attached to an average number of 2.2 (S.D. = 1.3)microhabitats. The number of ectoparasites on mako sharksdecreased with an increasing number of attached echeneids(P < .05, Figure 3).

    4. DISCUSSION

    Our data from whale and mako sharks do not lend conclusivesupport to the first hypothesis (Figures 1(b), 2(c)) whichis based on the assumptions that parasites are the primarydriver of echeneid host selection and/or that echeneids areable to assess host parasite loads. However, it is possiblethat echeneids choose hosts opportunistically and feed onectoparasites nonselectively. With no data to test the twoabove-mentioned assumptions but data from mako sharksthat support the second hypothesis (Figure 3), our resultsindicate that echeneids do regulate ectoparasite numbersatleast to some extent and probably dependent on the echeneidand ectoparasite species involved (see below)and therebyreduce the number of the latter on the hosts body.

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    Gonzalo R. Mucientes et al. 3

    (a)

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    E and PP onlyE onlyNo E and P0

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

    Ectoparasites were most commonly observed in a singlemicrohabitat on whale sharks and in multiple microhabitatson 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 toadverse abiotic or biotic factors including predation byfishes [11]. However, in whale sharks, echeneids were alsofound most likely on the head when ectoparasites werepresent at the same time, which indicates that this particularmicrohabitat offered no protection from potential echeneidpredation.

    Both Xiphias gladius and Isurus oxyrinchus are knownhosts for Remora osteochiralthough the latter association hasbeen documented only once in the literature [2]. OToole[2] regards this echeneid species to be a pelagic obligaterestricted to a small group of hosts, mostly billfishes. Diet

    76543210

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

    data indicate that R. osteochir regularly feeds on differentspecies of parasitic copepods [6, 12]. For whale sharks in this

    study, both species of echeneids reported were not previouslylisted to be associated with this particular host species [2].About one third of the whale sharks that were infectedwith pandarid copepods also had associated echeneids. Thiscould be related to the prevalence ofE. naucrates, for whichparasites are not an important food ([2, 6, 13] but see [4, 7]).Additionally, most individuals were free-swimming underthe ventral surfaces of whale sharks while observed, whichcould indicate that these echeneids were not actively feedingat the time of our observations although there is a possibilitythat they were ram-feeding on plankton. For R. brachyptera,parasites are generally considered a moderately importantfood item [2, 10, 14].

    A number of methodological limitations are evidentin our study. For example, we were only able to samplea relatively small number of free-ranging whale sharksconclusively (covering the entire body surface) and onlywere able to detect large ectoparasites on photographs. Wemight also have missed smaller echeneid species and/orindividuals that would feed on parasites in the mouth or gillchambers of whale sharks. These constraints likely result inunderestimating the actual ectoparasite and echeneid load.Furthermore, we were not able to quantify the degree ofecheneid detachment and/or microhabitat changes (if anyactually occur) for hooked mako sharks while still in thesea. Future studies looking at the degree of importance of

    ectoparasites to different echeneid species should also lookat their gut contents. We nevertheless are confident thatour study adds a novel approach to the understanding ofthe little known and elusive host-echeneid association andunderpins the need for observational data from free-ranginganimals that can be combined with information collected oncommercial fishing vessels.

    ACKNOWLEDGMENTS

    Thanks to Instituto Espanol de Oceanografa (Coruna)and Andres Paz and crew of the vessel Maicoa Dos forassistance and collaboration with mako shark fieldwork.

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    Andrea Marshall and Tofo Scuba assisted with whale sharkfieldwork. J. M. Brunnschweiler is supported by the Save OurSeas Foundation, the Shark Foundation Switzerland, ProjectAWARE (UK) and he acknowledges the Swiss NationalScience Foundation Grant no. 11 9305/1 for partial fundingduring the preparation phase of this manuscript. I. Sazima

    thanks the CNPq for essential financial support. N. Queirozwas funded by Fundacao para a Ciencia e a Tecnologia (FCT)Grant SFRH/BD/21354/2005. S. J. Pierce is supported byCasa Barry Lodge, Project AWARE (UK), PADI Foundation,and the Save Our Seas Foundation. Fran Saborido and JuanSantos are gratefully acknowledged for technical assistanceand advice. The valuable comments from two anonymousreferees that substantially improved this manuscript aregreatly appreciated.

    REFERENCES

    [1] J. M. Brunnschweiler and I. Sazima, A new and unexpected

    host for the sharksucker (Echeneis naucrates) with a briefreview of the echeneidhost interaction, JMBA2 BiodiversityRecords, 2006, http://www.mba.ac.uk/jmba/pdf/5434.pdf.

    [2] B. OToole, Phylogeny of the species of the superfamilyEcheneoidea (Perciformes: Carangoidei: Echeneidae, Rachy-centridae, and Coryphaenidae), with an interpretation ofecheneid hitchhiking behaviour, Canadian Journal of Zoology,vol. 80, no. 4, pp. 596623, 2002.

    [3] J. M. Brunnschweiler, Sharksuckershark interaction in twocarcharhinid species, Marine Ecology, vol. 27, no. 1, pp. 8994, 2006.

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    [7] I. Sazima, R. L. Moura, and M. C. M. Rodrigues, A juvenilesharksucker, Echeneis naucrates (Echeneidae), acting as astation-based cleaner fish, Cybium, vol. 23, no. 4, pp. 377380, 1999.

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    [10] J. N. Caira and C. J. Healy, Elasmobranchs as hosts ofmetazoan parasites, in Biology of Sharks and their Relatives,J. C. Carrier, J. A. Musick, and M. R. Heithaus, Eds., pp. 523551, CRC Press, Boca Raton, Fla, USA, 2004.

    [11] K. Buchmann and T. Lindenstrm, Interactions betweenmonogenean parasites and their fish hosts, International

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    [13] L. Szidat and A. Nani, Las remoras del Atlantico austral conun estudio de su nutricion natural y de sus parasitos, Revistadel Instituto Nacional de Investigacion de las Ciencias Naturales(Ciencias Zoologicas), vol. 2, pp. 385417, 1951.

    [14] D. W. Strasburg, Notes on the diet and correlating structuresof some central Pacific echeneid fishes, Copeia, vol. 3, pp.244248, 1959.