Hindawi Publishing Corporation
Research Letters in Ecology
Volume 2008, Article ID 107576, 4 pages
doi: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, Spain
de Investigação em Biodiversidade e Recursos Genéticos (CIBIO), Campus Agrário de Vairão,
Rua Padre Armando Quintas, 4485 Vairão, Portugal
3 Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, PL1 2PB, UK
4 Foundation for the Protection of Marine Megafauna Tofo Beach, Mozambique
5 School of Biomedical Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia
6 Museu de Zoologia, IB, Universidade Estadual de Campinas, 13083-970 Campinas, SP, Brazil
7 Swiss Federal Institute of Technology, Raemistrasse 101, 8092 Zurich, Switzerland
2 Centro
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) and
captured mako sharks (Isurus oxyrinchus) to test whether (1) echeneid presence was positively correlated with ectoparasite
presence; and (2) the number of ectoparasites was negatively correlated with the number of echeneid fish. Data from whale and
mako sharks do not support the first hypothesis whereas data from mako sharks yields support for the second hypothesis. The
results indicate that echeneids do regulate the number of ectoparasites on at least some host species, but these benefits may be
contingent on the echeneid species.
Copyright © 2008 Gonzalo R. Mucientes et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
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.
2
Research Letters in Ecology
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.
Frequency (%)
No E and P
RESULTS
100
80
60
40
20
0
L
A
P only
E and P
H
D
B
C
I
A
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 (n = 15), 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)).
E only
(b)
Frequency (%)
3.
(a)
100
80
60
40
20
0
B C
F
G
J
E
K
D E F G H
Microhabitat
I
J
K
L
(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.
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
(P < .05, Figure 3).
4.
DISCUSSION
3.2. Shortfin makos
A total of 224 shortfin makos were examined, of which 68
had a total number of 128 echeneids attached (1.9 ± 1.3).
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 (28.1 ± 33.5).
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 (17.5 ± 34.5 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
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.
Gonzalo R. Mucientes et al.
3
Number of P
40
30
20
10
(a)
0
0
Frequency (%)
100
80
60
40
20
0
E only
P only
E and P
Frequency (%)
(c)
100
80
60
40
20
0
A
L
A
D
C
B
I
B C
H
F
G
J K
2
3
4
5
Number of E
6
7
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.
(b)
No E and P
1
E
D E F G H
Microhabitat
I
J
K
L
(d)
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.
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 Oceanografı́a (Coruña)
and Andrés Paz and crew of the vessel “Maicoa Dos” for
assistance and collaboration with mako shark fieldwork.
4
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.
REFERENCES
[1] J. M. Brunnschweiler and I. Sazima, “A new and unexpected
host for the sharksucker (Echeneis naucrates) with a brief
review of the echeneid—host interaction,” JMBA2 Biodiversity
Records, 2006, http://www.mba.ac.uk/jmba/pdf/5434.pdf.
[2] B. O’Toole, “Phylogeny of the species of the superfamily
Echeneoidea (Perciformes: Carangoidei: Echeneidae, Rachycentridae, and Coryphaenidae), with an interpretation of
echeneid hitchhiking behaviour,” Canadian Journal of Zoology,
vol. 80, no. 4, pp. 596–623, 2002.
[3] J. M. Brunnschweiler, “Sharksucker—shark interaction in two
carcharhinid species,” Marine Ecology, vol. 27, no. 1, pp. 89–
94, 2006.
[4] I. Sazima and A. Grossman, “Turtle riders: remoras on marine
turtles in Southwest Atlantic,” Neotropical Ichthyology, vol. 4,
no. 1, pp. 123–126, 2006.
[5] J. M. Silva Jr. and I. Sazima, “Whalesuckers on spinner
dolphins: an underwater view,” JMBA2 Biodiversity Records,
2006, http://www.mba.ac.uk/jmba/pdf/5201.pdf.
[6] R. F. Cressey and E. A. Lachner, “The parasitic copepod diet
and life history of diskfishes (Echeneidae),” Copeia, vol. 2, pp.
310–318, 1970.
[7] I. Sazima, R. L. Moura, and M. C. M. Rodrigues, “A juvenile
sharksucker, Echeneis naucrates (Echeneidae), acting as a
station-based cleaner fish,” Cybium, vol. 23, no. 4, pp. 377–
380, 1999.
[8] I. Sazima, “Species records, mistaken identifications, and their
further use: the case of the diskfish Echeneis naucrates on a
spinner dolphin,” Neotropical Ichthyology, vol. 4, no. 4, pp.
457–460, 2006.
[9] B. M. Norman, D. R. Newbound, and B. Knott, “A new species
of Pandaridae (Copepoda), from the whale shark Rhincodon
typus (Smith),” Journal of Natural History, vol. 34, no. 3, pp.
355–366, 2000.
[10] J. N. Caira and C. J. Healy, “Elasmobranchs as hosts of
metazoan parasites,” in Biology of Sharks and their Relatives,
J. C. Carrier, J. A. Musick, and M. R. Heithaus, Eds., pp. 523–
551, CRC Press, Boca Raton, Fla, USA, 2004.
[11] K. Buchmann and T. Lindenstrøm, “Interactions between
monogenean parasites and their fish hosts,” International
Journal for Parasitology, vol. 32, no. 3, pp. 309–319, 2002.
[12] T. Vaske Jr., “Alimentação de rêmora Remora osteochir
(Cuvier, 1929), e peixe-piloto Naucrates ductor (Linnaeus,
1758), no sul do Brasil,” Revista Brasileira de Biologia, vol. 55,
pp. 315–321, 1995.
Research Letters in Ecology
[13] L. Szidat and A. Nani, “Las remoras del Atlantico austral con
un estudio de su nutricion natural y de sus parasitos,” Revista
del Instituto Nacional de Investigacion de las Ciencias Naturales
(Ciencias Zoologicas), vol. 2, pp. 385–417, 1951.
[14] D. W. Strasburg, “Notes on the diet and correlating structures
of some central Pacific echeneid fishes,” Copeia, vol. 3, pp.
244–248, 1959.