# Is Host Ectoparasite Load Related to Echeneid Fish Presence?

Authors: Gonzalo R. Mucientes; Nuno Queiroz; Simon J. Pierce; Ivan Sazima; Juerg M. Brunnschweiler
Journal: Research Letters in Ecology
 (2008)

---

## Abstract

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.


---

## Body

## 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 sharkRhincodon 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 (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)).Whale
sharks photographed off Tofo Beach, Mozambique, with (a) a group of
free-swimmingEcheneis 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.
(a)(b)(c)


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


## 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)).Whale
sharks photographed off Tofo Beach, Mozambique, with (a) a group of
free-swimmingEcheneis 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.
(a)(b)(c)


## 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 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).(a) A liveRemora 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.
(a)(b)(c)(d)Figure 3
Average
number (+ S.D.) of ectoparasites on mako sharks with between 0 and 5R. 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 (Figures1(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.BothXiphias 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.



---

*Source: 107576-2009-01-08.xml*