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New Host and Geographical Distribution for the Pearlfish Carapus mourlani
(Carapidae) with a Discussion on its Biology
E
´
RIC PARMENTIER,ANNIE MERCIER, AND JEAN-FRANC¸ OIS HAMEL
Specimens of the pearlfish Carapus mourlani (Carapidae) were observed for the
first time in association with the sea cucumber Isostichopus fuscus (Holothuroidea:
Echinodermata) along the coast of Ecuador. Out of 4345 sea cucumbers collected from
various depths between 5 and 60 m, 12 harbored a pearlfish either in the coelomic
cavity, the respiratory tree, or the digestive tract, yielding a prevalence of ca. 0.0028.
The presence of C. mourlani appeared to be detrimental to the holothurian host in
some cases. Side effects resulting from coelomic cavity infections included less
advanced gonad maturity (reduced gonadal tubule diameter and length, lower ratio of
mature oocytes) and a significant proportion of necrotic and shriveled gonadal tubules,
devoid of gametes. Aside from discussing this evidence, the present paper briefly
describes the biology of the pearlfish, its relationship with the host, and its daily activity
cycle.
T
HE Carapini tribe comprises a group of
marine fishes that are distributed worldwide
between 40uN and 30uS but display a greater
diversity in tropical latitudes (Williams, 1984;
Markle and Olney, 1990; Nielsen et al., 1999).
The Carapini are currently divided into two
genera: Carapus and Encheliophis (Markle and
Olney, 1990; Parmentier et al., 2000a). Among
the seven known commensal species of Carapus,
four are associated with holothurians (C. acus, C.
bermudensis, C. boraborensis, and C. homei), one is
found in sea stars (C. mourlani), one is hosted by
bivalves (C. dubius), and the last one (C. sluiteri)
by ascidians (Markle and Olney, 1990; Parmen-
tier et al., 2000a; Eeckhaut et al., 2004). The five
species that belong to the genus Encheliophis are
parasites of holothurians (Parmentier et al.,
2000a; Parmentier and Das, 2004) although at
least two (E. gracilis and E. sagamianus) were also
found in sea stars (Arnold, 1956; Cheney, 1973;
Markle and Olney, 1990). Carapidae are known
to associate with preferred hosts (Trott and
Trott, 1972; Gustato et al., 1979), but they may
occur in uncharacteristic hosts as well (Smith,
1964; Trott, 1970). In captivity, some Carapidae
were observed to associate with holothurians in
which they had never been found before in the
wild, although they always selected their custom-
ary hosts when given a choice (Trott, 1970,
1981).
While the biology of some Carapidae has
received a certain degree of attention, the habits
and behavior of C. mourlani remain poorly
known. Carapus mourlani is commonly found in
the Indo-Pacific where it is described as a com-
mensal of sea stars such as Culcita sp. and
Acanthaster planci (Meyer-Rochow, 1977, 1979;
Trott, 1981). Carapus mourlani has been observed
to swim along the ambulacral groove of the sea
star Culcita before entering the stomach, tail first,
through the oral cavity and finally reaching the
coelomic cavity (E. Parmentier, pers. obs.). The
presence of a pearlfish is usually not believed to
be detrimental for hosts (Trott, 1981; Vanden-
Spiegel et al., 2000), which display very efficient
regeneration capabilities (Mary Bai, 1971; Hamel
and Mercier, 2000).
The prevalence of pearlfishes in given hosts
seems largely dependent on the host abundance
and distribution as well as on the occurrence of
pearlfish planktonic eggs and vexillifer larva
(Trott, 1981). The degree of infection varies
between 10% and 100% depending on the
species and geographical locations (Jangoux,
1987, 1990).
This paper reports the first occurrence of
a Carapini off the coast of Ecuador within a new
holothurian host. The specific goals of the
present study were to identify the species found
in Ecuador and describe the main aspects of its
biology.
M
ATERIALS AND METHODS
Collection and observations.—Sea cucumbers (Iso-
stichopus fuscus) were routinely collected by
SCUBA divers between 5 and 60 m at several
sites along the coast of mainland Ecuador, from
fall 2000 to fall 2003, for the purpose of
aquaculture studies. During this time, a total of
12 pearlfishes were found inside the sea cucum-
bers, mostly in fall 2001 and exclusively in hosts
collected at 20 6 5 m near the villages of Punta
Ayangue (01u599330S and 80u459230W) and An-
concito (02u199600Sand80u529600W) in the
Guayas Province. The pearlfishes were either
Copeia, 2006(1), pp. 122–128
#
2006 by the American Society of Ichthyologists and Herpetologists
observed at the time of collection or during the
first night of their arrival at the laboratory. While
only one specimen, found on 12 September 2003
in Punta Ayangue, was preserved for taxonomical
analysis (SIO 04-163, 67 mm SL), all pearlfishes
found were of the same species, based on
thorough visual inspection and known occur-
rences of Carapini in the region. The sea
cucumbers, collected from two sites off the
village of Playas and one site near the city of
Machala, did not harbor any pearlfish.
Observations on the behavior of the sea
cucumber and the pearlfishes were carried in
nine round 20-ton tanks (ca. 4 m wide and 1.5 m
high, filled with ca. 35 cm of water). Adult sea
cucumbers (18–23 cm long, contracted length)
were distributed evenly with an average of 133
individuals per tank and fed daily by adding
grinded macrophytes and sedimented phyto-
plankton. They were provided with a flow of ca.
7000 L/h with natural variations of salinity, pH,
and temperature. The light intensity and photo-
period also fluctuated with the ambient condi-
tions (through a Plexiglas
TM
roof); sunset was
around 1845 h. The bottom of the tanks was
covered with ca. 30 cm of natural sand collected
from the field and a few fiberglass plates to
provide shelter to the sea cucumbers. Sea
cucumbers harboring a pearlfish were randomly
spread among the tanks; no more than 3–4
infected individuals were ever observed in a given
month. Monitoring began on the first day of
collection, from 30–45 min before sunset
through the early morning hours and for up to
14 consecutive nights, depending on the level of
activity noted. Observers used low intensity light
sources to confirm a specific observation when
necessary, otherwise using only natural lighting.
In the experiments designed to determine the
importance of light in the behavior of C.
mourlani, the tanks containing infected sea
cucumbers were either exposed to artificial
fluorescent lights (ca. 100 mmol m
22
s
21
in the
first five cm of water) or covered with opaque
plastic. Every simulation was repeated at least
three times in the night and day time and the
results compared to observations under the
normal day/night regime. After the general
observations were completed, the pearlfishes
were routinely separated from their host and
transferred to a 40 L aquarium offering environ-
mental conditions similar to the ones prevailing
in the larger tanks, to verify if the fishes could
survive away from their hosts.
All sea cucumbers that initially harbored
a pearlfish and those that were visited by one
during the experiments were identified and
eventually dissected. They were examined for
signs of morphological and tissue alteration.
Special attention was given to the two females
in which C. mourlani was present in the coelomic
cavity, as they displayed evident abnormalities.
Qualitative and quantitative measurements were
therefore taken in fresh gonad samples collected
from infected (n 5 2) and non-infected female
sea cucumbers (n 5 30). The dominant gameto-
genic stage of maturity was determined using the
classification of Hamel et al. (1993, 2001). The
following features were observed: 1) the pro-
portion of gonadal tubules displaying necrotic
sections (e.g., dehydrated and shriveled, darker
in color, irregular in shape and in diameter); 2)
the length, outer diameter, and lumen diameter
of 15 randomly collected gonadal tubules (in
infected individuals, data were collected sepa-
rately in necrotic and normal sections); 3) the
diameter and maturity level of 30 oocytes; 4) the
number of mature oocytes per cm in three
gonadal tubules.
Taxonomic investigation.—Counts and measure-
ments followed the methods of Williams and
Shipp (1982) and Markle and Olney (1990). A
Wild M10 binocular microscope, combined to
a camera lucida, was used. Measurements were
made to the nearest 0.1 mm with a caliper. The
specimen from Ecuador available for the de-
scription was stained with alizarin (Taylor and
Van Dyke, 1985) and compared to other stained
specimens of the Carapini (Carapus boraborensis,
C. homei, C. dubius, C. mourlani, C. acus, Enchelio-
phis gracilis, and E. vermicularis) from the private
collection of the laboratory of Functional and
Evolutive Morphology of the University of Lie`ge,
Belgium.
R
ESULTS
Description.—The following description is restrict-
ed to the characters that allowed the identifica-
tion of the Ecuadorian specimen. Outer cardi-
form teeth are present at the anterior end of the
premaxilla, and small conical teeth are organized
in two rows along this bone. The dentary displays
a row of large external conical teeth and three to
five rows of smaller conical teeth. The vomer has
three large prominent teeth. The first cerato-
branchial displays three well-developed bran-
chiospines, with two rows of small conical teeth.
The specimen also has a central constriction of
the swim bladder at the 9
th
vertebra, 15 precaudal
vertebrae, and 19 rays in the pectoral fin.
Biological aspects.—A total of 12 pearlfishes were
found individually in separate hosts: five in Punta
Ayangue samples and seven in Anconcito sam-
PARMENTIER ET AL.—CARAPUS MOURLANI 123
ples, out of 4345 sea cucumbers collected at
those sites over a period of three years. Two
gravid females were observed, and no juvenile
was ever found, giving a male to female ratio of
2 : 10. Although they were kept for variable
lengths of time, all sea cucumbers were eventu-
ally dissected. The prevalence of I. fuscus infected
by C. mourlani in the Punta Ayangue-Anconcito
region was therefore 12 : 4345, or ca. 0.0028.
However, pearlfishes were never observed in
thousands of other sea cucumbers collected at
three other sites during the same period.
Monitoring of the behavior of C. mourlani in
captivity showed that they remained inside their
host during the day. They first started to come
out around 1930 h (ca. 45 min after sunset),
although they usually only exposed half of their
body in a back and forth motion. As darkness
settled (ca. 2000 h), the pearlfishes left their
hosts and swam freely for periods varying from 30
to 95 min before sheltering again for period of
32 to 55 min and heading out once more. The
cycle was usually repeated several times each
night (between two to four times, depending of
the individual). The same individual was often
found to swim out of its host several nights in
a row, for up to 12 consecutive nights in one case.
Some fishes remained active until 0100 h with
a peak of activity noted just after emergence from
the host. A tendency to swim actively, explore
shelters and crevices, and probe the anal
opening of several sea cucumbers was observed.
In fact, the same fish rarely came back to its
original host after foraging. Carapus mourlani
were found to graze on various substrates
comprising the fouling layers of the tanks and
fiberglass plates, mainly on a mixture of hydro-
zoans, worms, crustaceans, and various other
sessile benthic invertebrates as well as on the
surface of sea cucumbers. Artificial light (ca.
100 mmol m
22
s
21
) prevented the pearlfishes
from swimming out of the hosts at sunset. When
light was switched off again, it generally took
under 10 min for most pearlfishes to exit the
holothurians. Conversely, when darkness was
simulated during daytime, the foraging behavior
of C. mourlani was induced within a period of ca.
45 min. Pearlfishes did not survive more than ca.
six days in the absence of their host, at least in
the conditions provided during the study.
Inspection of the originally infected sea
cucumbers revealed that four of the specimens
of C. mourlani lived in the last third of the
digestive tract, six of them colonized the re-
spiratory tree, and two dwelled in the coelomic
cavity of I. fuscus. Hosts harboring a pearlfish in
the intestine or respiratory tree did not present
any deformity or internal injury. However, the
two cases of coelomic cavity infection were
characterized by the presence of multiple open-
ings along the respiratory tree epithelium.
Necrotic or shriveled tissues were observed along
the respiratory tree and gonad, and evidence of
irritation of the body wall muscles bands and of
the cloaca were visible. Furthermore, the gonad
development of these two female hosts was
clearly less advanced than that of non-infected
sea cucumbers collected simultaneously
(Table 1). The infections of C. mourlani were
noticed in I. fuscus that had been collected
between two and five days before the monthly
spawning date depending on the month. During
that period, .90% of the sea cucumbers were
ready to spawn and displayed gonadal tubules
filled with mature gametes. However, individuals
hosting a pearlfish in the coelomic cavity were
predominantly in the ‘‘growth stage,’’ which is
characterized by less abundant and less devel-
oped gametes with poor vitelline reserves. More-
over, the proportion of necrotic tubule sections,
which were devoid of gametes, was clearly higher
(ca. 34%) in infected sea cucumbers than in non-
infected ones (ca. 4%). Finally, the gonadal
tubules of infected individuals were shorter and
smaller; they had less gametes per centimeter
and a strikingly thinner lumen (Table 1).
D
ISCUSSION
Identification of SIO 04-163.—Carapus lacks pelvic
fins and fangs and diastemas on the premaxilla
and dentary. The premaxilla bears cardiform
teeth, two or three enlarged teeth on its anterior
part, and at least two rows of small conical teeth
along its length, whereas the dentary has one row
of enlarged conical teeth and several rows of
small internal teeth (Parmentier et al., 2000a).
Therefore, the SIO 04-163 specimen definitely
belongs to the genus of Carapus. It can further be
classified as C. mourlani on the basis of the
combination of the following characters: swim
bladder constriction at the ninth vertebra, three
prominent teeth on the vomer, 15 precaudal
vertebrae, 19 rays in the pectoral fin, and two
rows of teeth on the branchiospines of the first
ceratobranchial (Petit, 1934; Markle and Olney,
1990; Parmentier et al., 2002a).
Biological aspects.—Frequency of infection of
holothurians by Carapidae vary between locali-
ties. Out of 257 specimens of Bohadschia argus
collected in French Polynesia, 84% contained
pearlfishes: C. homei in 39.3% of the cases and C.
boraborensis in 59.2% (Parmentier and Vande-
walle, 2005). VandenSpiegel and Jangoux (1989)
reported similar data. Tyler et al. (1992) and
124 COPEIA, 2006, NO. 1
Smith et al. (1981) noted a frequency of in-
fection of 21% by C. bermudensis in Bahamas and
of 8 to 13% by C. acus in the Mediterranean Sea
(Kloss and Pfeiffer, 2000). However, the occur-
rences of C. acus apply only to hosts sampled at
ca.40m;nopearlfishwaseverfoundin
holothurians collected from shallower depths in
Corsica (E. Parmentier, pers. obs.). The preva-
lence found in the present study (ca. 0.0028) is
probably the lowest ever recorded. The fact that
Carapidae appear to be restricted to certain
depths, as observed in the Mediterranean and in
the present study, may partly account for this very
low incidence since the 4345 sea cucumbers were
collected between ca. 5 and 60 m throughout the
study. However, this value does not take into
account the thousands of other I. fuscus collected
elsewhere along the Ecuadorian coast, which
were never reported to host a pearlfish.
Despite the low frequency of infection, two
gravid pearlfish females were found, which raises
questions regarding the recruitment and overall
reproductive success of the population of C.
mourlani found in I. fuscus. Investigation of other
potential Ecuadorian hosts such as sea stars (e.g.,
Oreaster occidentalis, Heliaster multiradiata) could
shed some light on the situation.
To our knowledge, no study has ever been
conducted to evaluate the impact of pearlfishes
on their hosts. Adverse effects can be expected in
the case of species of Encheliophis which feed on
the host’s gonads (Murdy and Cowan, 1980;
Trott, 1981; Parmentier and Das, 2004). Howev-
er, C. mourlani are commensals that feed outside
of their hosts (Parmentier and Das, 2004). The
present work is the first to suggest possible
detrimental effects of a Carapus on holothurians.
The two hosts in which C. mourlani were found
inside the coelomic cavity showed evidence of
tissue alterations and less advanced gametogenic
levels of maturity compared to other infected
and non-infected sea cucumbers collected in the
same location and to transient hosts visited by
pearlfishes during the experiments. Previous
studies have shown that the reproductive cycle
of populations of I. fuscus is generally character-
ized by a well synchronized gonad development
and monthly spawning (Mercier et al., 2004). By
tearing the respiratory tree to reach the coelomic
cavity, the pearlfish would allow sea water to
penetrate as well, therefore modifying the
composition of the perivisceral coelomic fluid,
which has been identified as a key element in the
reproductive cycle of echinoderms (e.g., Hines et
al., 1992; Barker and Xu, 1993; Mercier and
Hamel, 2002).
Carapidae usually occur in the respiratory tree
or coelomic cavity of holothurian hosts (Trott,
1970; VandenSpiegel and Jangoux, 1989; Markle
and Olney, 1990). The presence of specimens of
C. mourlani in the digestive tract remains anec-
dotal and is considered unusual. In this study,
the presence of a pearlfish in the digestive tract
was always consistent with the absence of in-
testinal contents and might therefore represent
a laboratory artifact. In the field, I. fuscus usually
feed continuously during the night, so they
should almost always present some sort of
intestinal contents, whereas diurnal inactivity
reduces intestinal transit and the intestine
usually remains at least partly full until the next
feeding period (Mercier et al., 1999, 2004).
Sheltering of pearlfishes in the respiratory tree
remains the most consistent observation and it
appears to be the most suited place for the fish to
dwell (i.e., allowing gill oxygenation through
periodic water exchange).
The activity of C. mourlani monitored during
this study was clearly nocturnal. This behavior
agrees with the notion that the eyes of C. mourlani
share certain characteristics with those of cave-
dwelling organisms, such as photoreceptors with
TABLE 1. GONAD MATURITY AND MORPHOMETRIC MEASUREMENTS OF Isostichopus fuscus. Comparison between non-
infected individuals (n 5 30) and infected individuals hosting a pearlfish in the coelomic cavity (n 5 2). Values are
expressed as mean 6 confidence interval (95%).
Dominant gametogenic stage
Non-infected
Infected
Normal tubules Necrotic tubules
Mature Growth No gametes present
Mean 6 CI n Mean 6 CI n Mean 6 CI n
Gonadal tubule length (mm) 95.6 6 0.8 450 82.3 6 1.6 30 61.1 6 7.6 30
Gonadal tubule diameter (mm) 3.7 6 0.5 450 2.8 6 0.3 30 2.1 6 0.2 30
Lumen diameter (mm) 1.9 6 0.2 450 1.1 6 0.3 30 0.1 6 0.08 30
Oocyte diameter (mm) 110.7 6 3.1 900 55.2 6 7.5 60 – –
No. of oocytes per cm of gonadal
tubule
334.4 618.9 90 202.7 6 31.4 6 – –
PARMENTIER ET AL.—CARAPUS MOURLANI 125
high levels of sensitivity and poor resolution
(Meyer-Rochow and Tiang, 1978). The fact that
the pearlfishes were found to leave their host
almost every night while in captivity is not
necessarily an indication of their normal behav-
ior. Indeed, other evidence suggests that wild
pearlfishes may remain in the same host for
a while. For instance, less advanced gametogenic
levels of maturity and gonadal tissue deteriora-
tion were recorded in sea cucumbers that hosted
a pearlfish in their coelomic cavity. Since gonad
development cannot be altered within one or two
days (Hamel and Mercier, 1996, 1999), and the
pearlfish-to-host ratio does not seem sufficient to
allow repeated infections, the delayed gonad
development should be induced by long-term
infection. Moreover, based on otolith (sagittae)
observations, Parmentier et al. (2002b) proposed
that C. boraborensis and C. homei had resting and
active periods, with a duration that depended on
the energy provided by the ingested prey. In C.
bermudensis, a feeding periodicity ranging from
15 to 24 days on average was estimated (Smith et
al., 1981). The nightly activity recorded in the
tanks could therefore be linked to the abun-
dance of copepods and other invertebrates that
live on the outer surface of holothurians.
Although stomach contents were not examined
during this study, previous data have shown that
shrimp, decapods, annelids, and small fish form
the usual diet of C. mourlani (Meyer-Rochow,
1979; Parmentier and Das, 2004).
The identification of a new holothurian host
for C. mourlani in Ecuador seems to support the
observation that this species can shelter in sea
cucumbers that are not hosting other Carapidae
(Markle and Olney, 1990). In parts of the world
where sympatric Carapus species occur, C. mour-
lani isfoundinseastarssuchasCu lcita
novaeguineae, C. schmidelliana, Acanthaster planci,
and Choriaster granulatus (Eeckhaut et al., 2004).
On the west coast of Central America, C. dubius
generally shelters in bivalves (Castro-Aguirre et
al., 1996; Paredes-Rios and Balart, 1999; Parmen-
tier et al., 2000b), whereas E. vermicularis favors
sea cucumbers (Markle and Olney, 1990) al-
though they have never been reported in I. fuscus
so far.
M
ATERIAL EXAMINED
Institutional abbreviations as follows: SIO 5
Scripps Institution of Oceanography; PCL 5
Private Collection of the Laboratory of Function-
al and Evolutive Morphology in Lie`ge (Belgium).
Carapus mourlani. SIO 04-163, 67 mm TL,
Ecuadorian coast, Punta Ayangue, 01u599330S,
80u459230W; PCL, 75 mm TL, French Polynesia,
Moorea (1 specimen), 70–110 mm TL, Madagas-
car, Tulear (3 specimens). C. boraborensis. PCL,
130–180 mm TL, French Polynesia, Moorea (3
specimens). C. homei. PCL, 80–125 mm TL,
French Polynesia, Moorea (2 specimens). C.
dubius. PCL, 92–120 mm TL, Gulf of California,
Bay of la Paz, Esperitu Santo Island (2 speci-
mens). C. acus. PCL, 74–125 mm TL, Bay of
Calvi, Corsica (4 specimens). Encheliophis vermi-
cularis. VIMS 09600, 123–148mm TL, New
Caledonia (2 specimens). E. gracilis. PCL, 135–
196 mm TL, French Polynesia, Moorea (2 speci-
mens).
A
CKNOWLEDGMENTS
We would like to thank R. Ycaza and his team
at Plasfel Especies Bioacuaticas for their precious
assistance with the collection of sea cucumbers
and pearlfishes along the coast of Ecuador. We
are also grateful to P. Vandewalle, M. Chardon,
and I. Eeckhaut who made helpful comments on
an earlier version of the manuscript. All collect-
ing and handling of specimens was in accordance
with policies and recommendations of University
of Lie`ge.
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(EP) UNIVERSITE
´
DE LIE
`
GE,LABORATOIRE DE
MORPHOLOGIE FONCTIONNELLE ET EVOLUTIVE,
I
NSTITUT DE CHIMIE,BA
ˆ
TIMENT B6, 4000 LIE
`
GE,
B
ELGIUM ;(AM)OCEAN SCIENCES CENTRE
(OSC), MEMORIAL UNIVERSITY OF NEWFOUND-
LAND
,ST.JOHN’S (NEWFOUNDLAND)CANADA
A1C 5S7 ; AND (JFH) SOCIETY FOR THE EXPLO-
RATION AND
VALUING OF THE ENVIRONMENT
(SEVE), 21 PHILS HILL ROAD (NEWFOUNDLAND)
C
ANADA A1M 2B7. E-mail: (EP) E.Parmentier@
ulg.ac.be; (AM) amercier@mun.ca; and (JFH)
jfhamel@mun.ca. Send reprint requests to P.
Submitted: 20 Feb. 2005. Accepted: 18 Aug.
2005. Section editor: D. Buth.
128 COPEIA, 2006, NO. 1
