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Shark (Carcharhinus perezi), cleaned by the goby (Elacatinus randalli), at Fernando de Noronha Archipelago, Western South Atlantic

Authors:
Ivan Sazima at University of Campinas
Ivan Sazima
Rodrigo Leão Moura at Federal University of Rio de Janeiro
Rodrigo Leão Moura
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Sharks are seldom recorded as associates of reef-based cleaner fishes. Here we report on juvenile Caribbean Reef Sharks, Carcharhinus perezi, associated with Yellownose Gobies, Elacatinus randalli, off northern Brazil. The sharks sought out cleaning stations tended by the gobies and posed on the bottom while being cleaned. The bottom-resting habit of C. perezi possibly facilitates cleaning interactions with the bottom-dwelling cleaner gobies.
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2000 by the American Society of Ichthyologists and Herpetologists
Copeia, 2000(1), pp. 297–299
Shark (Carcharhinus perezi), Cleaned by the Goby (Elacatinus randalli), at
Fernando de Noronha Archipelago, Western South Atlantic
I
VAN
S
AZIMA AND
R
ODRIGO
L. M
OURA
Sharks are seldom recorded as associates of reef-based cleaner fishes. Here we
report on juvenile Caribbean Reef Sharks, Carcharhinus perezi, associated with Yel-
lownose Gobies, Elacatinus randalli, off northern Brazil. The sharks sought out clean-
ing stations tended by the gobies and posed on the bottom while being cleaned. The
bottom-resting habit of C. perezi possibly facilitates cleaning interactions with the
bottom-dwelling cleaner gobies.
C
LEANING symbiosis among reef fishes is re-
garded as an interspecific, cooperative in-
teraction, in which a microcarnivore (cleaner)
seeks food from the body of other fishes (cli-
ents), that in this way rid themselves of ectopar-
asites and debris and receive tactile stimulation
(Losey, 1971, 1987). Sharks and rays are seldom
reported as clients of reef-based cleaner fishes
(Snelson et al., 1990). Although remoras (Eche-
neidae) occasionally feed on parasites of several
species of reef sharks and devil rays (Cressey
and Lachner, 1970; Clark, 1975), these fishes
live attached to their hosts instead of tending
cleaning stations. The few records of sharks at-
tended by reef-based cleaners are mostly short
accounts in popular books (Michael, 1993), vid-
eo records (Gruy, 1992), or aquarium observa-
tions (Keyes, 1982). Here we report on juvenile
Caribbean Reef Sharks, Carcharhinus perezi, seek-
ing out cleaning stations and posing on the bot-
tom while being cleaned by the Yellownose
Goby, Elacatinus randalli, and comment on the
cleaning association between bottom-resting
elasmobranchs and cleaner gobies.
M
ATERIALS AND
M
ETHODS
Study site.—Fernando de Noronha Archipelago
is situated at 03
8
50
9
S, 32
8
25
9
W, about 345 km
east off the coast of Brazil (for map and descrip-
tion, see Maida and Ferreira, 1997). Cleaning
symbiosis between yellownose gobies and Carib-
bean reef sharks was recorded at a leeward site,
Laje Dois Irma˜os, at a depth of 18–24 m. At this
site, rocks are covered by scleractinian corals,
mostly large Montastrea cavernosa heads, where
the gobies tend cleaning stations.
Methods.—Cleaning interactions between sharks
and gobies were photographed and video re-
corded in April 1994 in about 220 min of SCU-
BA diving over four days, and voucher speci-
mens were secured in August 1998. Records
concentrated on cleaning events, that is, the pe-
riod of association between cleaner and host
which begins with physical contact and ends
when the cleaner or the client retreats ( John-
son and Ruben, 1988). A voucher of the Carib-
bean shark is at MZUSP (52974, female, 975
mm TL) and those of the yellownose goby are
at ZUEC (3895, two specimens, 37.5 and 37.1
mm TL); institutional abbreviations follow Lev-
iton et al. (1985). Video-recorded cleaning
events are on file at ZUEC (tape 5).
R
ESULTS
Four juvenile individuals of the Caribbean
reef shark of about 80–120 cm TL (for length
of adults, see Gadig et al., 1996) were recorded
on cleaning stations tended by yellownose go-
bies on Montastrea coral heads or on rocky ledg-
es. The sharks landed on the sand/rubble bot-
tom within about 30 cm of the stations and were
cleaned by the gobies. A single shark was re-
corded at the cleaning station at a time, al-
though up to three individuals were observed
swimming within 20–30 m at the leeward site.
Two sharks adopted a soliciting pose by lying
on their side (Fig. 1), whereas two other sharks
landed on the bottom and remained so during
the cleaning events. One to three cleaners
moved over the shark’s body and fins, and on
one cleaning event, a goby twice entered the
client’s gill slits and mouth. One cleaning event
lasted 182 sec, and three other events (that were
incomplete due to disturbance caused by the
observers) lasted 48, 52, and 67 sec, respectively.
While being cleaned, the sharks rhythmically
pumped water over the gills, opening and clos-
ing the mouth at a rate of 32–36 times/min (n
5
2). Clark (1975) comments on active pump-
ing in cave-resting sharks, but no rates are giv-
en.
On one occasion, a large (about 120 cm TL)
Green Moray Eel, Gymnothorax funebris, ap-
proached a shark being cleaned by two gobies
and nibbled at, as well as pushed on, the shark’s
298 COPEIA, 2000, NO. 1
Fig. 1. A juvenile Caribbean reef shark, Carcharhinus perezi, lying on its side while being cleaned by two
individuals of the yellownose goby, Elacatinus randalli. One goby is on the lower jaw and the other is near the
base of the right pectoral fin. Photo by D. Brisolla.
head five times. The shark remained stationary,
closing its nictitating membrane when the mo-
ray nibbled close to its eye. When one of the
gobies left the shark and began to clean the mo-
ray eel, the moray ceased its harassment and re-
mained close to the shark, each client attended
by one cleaner. After 40 sec, the goby on the
moray returned to the shark, and that on the
shark moved to the moray, both gobies cleaning
the two clients for additional 12 sec, when the
shark left the station.
At the study site, the Caribbean reef shark was
observed being cleaned only at the stations of
the yellownose goby (we recorded no other spe-
cies of cleaner goby at Fernando de Noronha
Archipelago). Thirty-four fish species were re-
corded as clients of this goby in the archipelago,
including a ray and another shark (see below).
D
ISCUSSION
In the tropical west Atlantic, gobies of the ge-
nus Elacatinus are known to clean a vast array
of reef fishes and even octopuses, which seek
their cleaning stations ( Johnson and Chase,
1982; Johnson and Ruben, 1988; Wicksten,
1998). However, we are unaware of any record
involving Atlantic Cleaner Gobies and Carchar-
hinid Sharks. The Pacific Redhead Goby, Ela-
catinus puncticulatus, is known to clean the
Whitetip Reef Shark, Triaenodon obesus, at Cocos
Island in Costa Rica (Michael, 1993). Judging
from the description of Michael (1993) and the
video record by Gruy (1992), the cleaning as-
sociation between T. obesus and E. puncticulatus
is similar to that recorded here for C. perezi and
E. randalli, except for the side-lying posture of
C. perezi.
Both C. perezi and T. obesus are carcharhinid
sharks noted for their behavior of resting on the
bottom in caves or crevices (Clark, 1975; Mi-
chael, 1993; Lieske and Myers, 1994), a habit
that possibly facilitates cleaning interactions
with the substratum-oriented Elacatinus gobies.
The bottom-dwelling Nurse Shark, Ginglymosto-
ma cirratum, and the Southern Stingray, Dasyatis
americana, were recently recorded being
cleaned by the yellownose goby at Fernando de
Noronha Archipelago, and we also observed a
Reef Stingray, Dasyatis macrophtalma, being
cleaned by the Barber Goby, E. figaro, at Abrol-
hos Archipelago off eastern Brazil (unpubl.
obs.). Because the onset of these events was not
observed, we are not sure whether these three
elasmobranchs actively sought cleaning service
or were merely resting close to a cleaning sta-
tion and the goby capitalized on this situation.
However, resting close to a cleaning station may
create a plausible scenario for the evolution of
cleaning symbiosis between sharks and gobies.
Cleaners sometimes inspect and clean nonpos-
ing fishes passing slowly or resting by their sta-
tions (pers. obs.), and these may learn to rec-
ognize cleaners as a source of rewarding tactile
stimulation (Losey and Margules, 1974). From
an initially loose contact between a resting elas-
mobranch and a station-based goby, a more
elaborate association may evolve with the sharks
seeking out, and posing at, the cleaning stations
as recorded herein for C. perezi.
An additional, seemingly favorable condition
for the association between sharks and gobies
may be the absence of another cleaner. Riding
remoras (Echeneidae) ocasionally clean reef
elasmobranchs (Cressey and Lachner, 1970; Mi-
chael, 1993) and may thoroughly clean sharks,
including C. perezi, while these rest on the bot-
tom in the reef habitat (Clark, 1975; pers. obs.).
Because remoras were not recorded on the ju-
venile Caribbean reef sharks we observed seek-
ing the cleaning stations, it seems plausible that
yellownose gobies are replacing, at least partial-
ly, the cleaner role of the remoras (Suckerfish,
Echeneis naucrates, were recorded on adult indi-
299SAZIMA AND MOURA—SHARK AND CLEANER GOBY ASSOCIATION
viduals of C. perezi near the study site). Also, no
remoras were recorded on Pacific Whitetip
Sharks cleaned by redhead gobies (Gruy, 1992;
Michael, 1993). Keyes (1982) comments on the
quick onset of cleaning symbiosis between cap-
tive sharks lacking associated remoras and the
Cleaner Wrasse Labroides dimidiatus.
A
CKNOWLEDGMENTS
We thank D. Brisolla, M. C. M. Rodrigues,
and C. Secchin for allowing use of their video
records and/or photographs; R. B. Francini-Fil-
ho, M. C. M. Rodrigues, and C. Sazima for help
with fieldwork; R. M. C. Castro for suggestions
on the manuscript; the Ibama for permission to
study and collect cleaner fishes and their clients
at the Parque Nacional Marinho de Fernando
de Noronha (permits MMA 09/97 and 06/98);
and the CNPq (grant 300992/79 to IS), FAPESP
(grants 98/03491-3 to RLM and 96/5238-8 to
IS), and Finep/Pronex (grant 058/97 to N. A.
Menezes) for essential financial support.
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(IS) D
EPARTAMENTO DE
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OOLOGIA AND
M
USEU
DE
H
ISTO
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N
ATURAL
,C
AIXA
P
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6109,
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NIVERSIDADE
E
STADUAL DE
C
AMPINAS
, 13083-
970 C
AMPINAS
,S
A
˜
O
P
AULO
,B
RASIL
;
AND
(RLM) S
EC¸A
˜
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USEU DE
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OOLO
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,U
NIVERSIDADE DE
S
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AULO
, 04299-970
S
A
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O
P
AULO
,S
A
˜
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P
AULO
,B
RASIL
. E-mail: (IS)
isazima@unicamp.br. Send reprint requests to
IS. Submitted: 2 Oct. 1998. Accepted: 7 June
1999. Section editor: S. T. Ross.
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Full-text available
  • Mar 2022
Ecologically or Biologically Significant Marine Areas (EBSAs) are rare, and highly important sites to the life history of a number of declining shark species are endangered by fishing. The high diversity of sharks caught by fisheries is difficult to monitor due to the scarcity of information on species-specific biological aspects (growth, maturity and fertility rate). There are two EBSAs off north-eastern Brazil, where key species are caught, more specifically the oceanic whitetip (Carcharhinus longimanus), mako (Isurus oxyrinchus), blue (Prionace glauca) and silky (Carcharhinus falciformis) sharks. Another 23 species displaying low frequency in catches have also been recorded, many of them considered threatened according to the IUCN Red List and the Brazilian Ministry of Environment. The main purpose of this study was to generate information about shark diversity and demonstrate the role of the two EBSAs in their conservation. After analysing fishing data collected from 2000 to 2011, maps were built to categorize shark species by phases of their ontogenetic development (neonate, young and adult) based on samples of C. falciformis (n = 330), C. longimanus (n = 440), I. oxyrinchus (n = 452) and P. glauca (n = 8,176). Shark stocks comprised mainly juveniles, which raises concerns since they are considered a crucial life stage for the sustainability of shark populations. Catch monitoring also highlighted that several of the species caught are threatened and their catch is either prohibited or limited according to the Brazilian laws and international rules in place. Action plans and enforcement of laws and rules are needed to deliver the protective measures needed for shark species in these EBSAs.
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Behavior of cleaners and their client fishes at Bonaire, Netherlands Antilles
Article
Full-text available
  • Jan 1998
Forty-one species of 20 families of fishes were observed being cleaned at Bonaire by two species of decapod crustaceans and four species of fishes. Of 525 observations of fishes being cleaned (clients), over 60% involved species of the Serranidae, Scaridae and one species of Pomacentridae (Chromis multilineata). Gobies (Gobiosoma spp.) and Pederson's cleaner shrimp (Periclimenes pedersoni) were the most frequent cleaners of all three groups of clients. Only P. pedersoni performed a display that may have attracted clients. Cleaner species except Thalassoma bifasciatum cleaned the mouth and gills of clients, as well as the rest of the body. Clients approached cleaners, presented part of their body to the cleaner, opened their mouth or flared their gills, remained relatively motionless, and then twitched their tail and body and swam away. Unlike other clients, species of the Serranidae rarely assumed a vertical posture during cleaning. Chromis spp. and Clepticus parrai formed tight ball-like formations around cleaners. The behaviour of cleaner fishes and shrimp at Bonaire was more similar to that reported for eastern Pacific species than that of Labroides spp. of the Indo-Pacific area.
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Cleaning behavior ofBodianus rufus, Thalassoma bifasciatum, Gobiosoma evelynae, andPericlimenes pedersoni along a depth gradient at Salt River Submarine Canyon, St. Croix
Article
Full-text available
  • Nov 1988
Cleaning activity at specific cleaning stations was monitored over a depth range of 15–45 m at Salt River Submarine Canyon, St. Croix using the HYDROLAB underwater habitat. We observed over 4600 cleaning events involving 32 host species. Cleaners included the fishesGobiosoma evelynae (cleaning goby), juvenileBodianus rufus (Spanish hogfish) and juvenileThalassoma bifasciatum (bluehead wrasse) and the shrimpPericlimenes pedersoni, often active simultaneously at the same stations. Although cleaning was observed to depths of 30 m, the greatest density of cleaning fishes occurred at a sharp break in the bottom contour at 15 m.Clepticus parrae was the dominant fish cleaned by fishes (80% of events), and the graysby,Petrometopon cruentatum, was most frequently cleaned byPericlimenes. Cleaning was initiated byGobiosoma at 0600 to 0630 h and continued throughout the day as intense bouts of cleaning activity were interspersed with periods of relative calm.Bodianus patrolled areas of several meters and would sometimes rise over a meter above the substrate to initiate cleaning. In contrast, gobies were much more restricted in both lateral and vertical movements.Gobiosoma andBodianus cleaned 3104 and 1346 hosts during the study compared to only 207 forThalassoma. This study of a deeper reef area shows significantly more cleaning activity byBodianus and much less byThalassoma than has been reported from other studies in shallower water
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The Parasitic Copepod Diet and Life History of Diskfishes (Echeneidae)
Article
  • Jun 1970
  • COPEIA
Stomach contents from 401 individuals representing six species of echeneids were examined. Parasitic copepods are an important part of the diet of echeneid fishes. Parasitic copepods were present in 70% of the stomachs of Remora remora containing food and in four other species to a lesser, but significant extent. The growth stage of the life history of the echeneid during which it feeds on parasites varies among species. In R. remora the younger individuals are more active as parasite pickers whereas in R. osteochir older specimens are more active. Life history information resulting from extensive collection data is included in the discussion of each of the six species considered.
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Southern Stingray, Dasyatis americana: Host for a Symbiotic Cleaner Wrasse
Article
  • Dec 1990
  • COPEIA
The southern stingray, Dasyatis americana, served as host for the bluehead wrasse, Thalassoma bifasciatum, in a symbiotic cleaning relationship at a site near Bimini, Bahamas. Rays were cleaned either while swimming slowly around a cleaning station or when they settled to the bottom and assumed a peculiar, stereotyped pose. Cleaning bouts lasted from less than a minute to 26 min. Both sexes of rays were cleaned and one individual was cleaned four times over 2 d. A trematode ectoparasite was found on the stingrays, but they were not heavily infested and only occasionally had wounds.
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Cleaning Symbiosis Provides a Positive Reinforcer for Fish
Article
  • May 1974
Chaetodon auriga, a conun7won marine fish in Hawaii, can be conditioned by presentation of a moving model of a cleaner fish as a positive reinforcement on an instrumental schedule. Reinforcement is probably through tactile stimulation and might help to shape the response of fish to cleaners. Tactile stimulilation night serve as a valuable reinforcer in studies of fish learning.
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