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Marine Biodiversity
ISSN 1867-1616
Mar Biodiv
DOI 10.1007/s12526-016-0454-9
Herbivorous fishes Siganus rivulatus
(Siganidae) and Zebrasoma desjardinii
(Acanthuridae) feed on Ctenophora and
Scyphozoa in the Red Sea
Arthur R.Bos, Edwin Cruz-Rivera &
Ashraf M.Sanad
1 23
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SHORT COMMUNICATION
Herbivorous fishes Siganus rivulatus (Siganidae) and Zebrasoma
desjardinii (Acanthuridae) feed on Ctenophora and Scyphozoa
in the Red Sea
Arthur R. Bos
1,2,3
& Edwin Cruz-Rivera
4
& Ashraf M. Sanad
2,5
Received: 8 October 2015 /Revised: 9 January 2016 /Accepted: 24 January 2016
#
Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2016
Abstract Individuals of the rabbitfish Siganus rivulatus
(Siganidae) and surgeonfish Zebrasoma desjardinii
(Acanthuridae) were observed feeding on ctenophores and
scyphozoans in the northern Red Sea during late spring and
early summer seasons betwe en 2 010 and 2015. Siganus
rivulatus and Z. desjardinii, considered nominally herbivo-
rous, preyed on relatively large ctenophores until disintegra-
tion, and on the moon jellyfish Aurelia aurita (Scyphozoa)
until they sank to the bottom. Siganus rivulatus was the most
dominant predatory fish feeding on gelatinous zooplankton
(37 % of attacks on ctenophores and 51 % of attacks on A.
aurita). Furthermore, prey individuals were usually
approached by two or more fish simultaneously. Eleven addi-
tional fish species fed on gelatinous zooplankton, with
Chaetodon fasciatus (Chaetodontidae) accounting for 27 and
12 % of the attacks on ctenophores and A. aurita,respectively,
and Z. desjardinii for 17 and 24 % of the attacks. Other fishes
attacked gelatinous zooplankton in ≤6 % of the observations.
This study constitutes the first record of S. rivulatus and Z.
desjardinii preying on ctenophores and also confirms prelim-
inary observations of S. rivulatus feeding on scyphozoans.
Although herbivorous fishes may accidentally ingest small
invertebrates while feeding on algae, the deliberate feeding
on gelatinous zooplankton observed for S. rivulatus and Z.
desjardinii suggests that their trophic role should be
reevaluated.
Keywords Aurelia aurita
.
Chaetodontidae
.
Cnidaria
.
Gelatinous zooplankton
.
Herbivory
Introduction
Siganid fishes, distributed in the Indo-Pacific and Red Sea, are
herbivorous during their entire life cycles. Siganids preferably
feed on selected algae, cyanobacteria, and seagrasses, but may
temporarily shift their diet to less palatable algae when pre-
ferre d food items are seasonally scarce (Tsud a and Bryan
1973;vonWesternhagen1973; Lundberg and Lipkin 1979).
The diet of Siganus rivulatus Forsskål & Niebuhr, 1775 has
been well studied in the north-western corner of its geograph-
ical range, because first, successful migration from the Red
Sea to the Mediterranean Sea has triggered researchers study-
ing ecological impacts of this invading herbivore (e.g.,
Lundberg and Golani 1995; Shakman et al. 2009;Salaetal.
2011), and second, S. rivulatus is a fast-growing species with
high potential for aquaculture (Bariche 2006; Afeworki et al.
2013).
Herbivorous fishes, such as representatives of the
Acanthuridae, Scaridae and Siganidae, accomplish an impor-
tant ecological function in coral reefs by removing algae.
Communicated by R. Thiel
Electronic supplementary material The online version of this article
(doi:10.1007/s12526-016-0454-9) contains supplementary material,
which is available to authorized users.
* Arthur R. Bos
arthurrbos@yahoo.com
1
Department of Biology, American University in Cairo, P.O. Box 74,
New Cairo 11835, Egypt
2
John D. Gerhart Field Station, American University in Cairo,
El-Gouna, Egypt
3
Naturalis Biodiversity Center, P.O. Box 9517, 2300
RA Leiden, The Netherlands
4
Department of Biological Sciences, University of the Virgin Islands,
#2 John Brewers Bay, St. Thomas, USVI 00802, USA
5
Dive Pro Academy, P.O. Box 94, Sahl Hasheesh, Hurghada, Egypt
Mar Biodiv
DOI 10.1007/s12526-016-0454-9
Author's personal copy
Through top– down con trol (Fox and Bellwood 2007;
Mantyka and Bellwood 2007), these herbivores prevent corals
from being overgrown by algae and create space for settling
coral larvae (Brandl and Bellwood 2014). Phylogenetically
distinct herbivorous fish taxa show various feeding modes
and preferences in algal diets, but all Siganus and
Zebrasoma species are consistently considered nominally her-
bivorous (Gerking 1994; Choat et al. 2002).
Although not well studied, large gelatinous zooplankton
are part of the diet of pelagic fishes especially during spring
seasons when other food sources are scarce (Mianzan et al.
1996; Purcell and Arai 2001; Milisenda et al. 2014). The ma-
jority of these pelagic fishes are zooplanktivorous or piscivo-
rous and well adapted to feeding on animal tissue. Although
generally considered a food source of low quality for fishes,
some marine gelatinous taxa may provide as much energy as
other prey species (Arai 2005). In that context, Arai (2005)
distinguished fish species as being either generalists or coe-
lenterate specialists. Also, apex predators have been reported
to feed on gelatinous plankton (Cardona et al. 2012), but ref-
erence to herbivores feeding on this resource was not
provided.
While the idea that herbivorous fishes supplement their
diets with animal matter is not new (White 1993; Gerking
1994), surprisingly few observations have demonstrated ac-
tive ingestion of animal foods other than occasional phytal
epifauna. Accidental ingestion of small invertebrates while
feeding on algae has been reported (Foud a and El-Sayed
1994;Bariche2006), but herbivores deliberately selecting an-
imal prey has seldom been observed. Yet, gut content analyses
have demonstrated that certain species of fishes considered
herbivores can ingest considerable amounts of animal material
(Choat et al. 2002). Blooms of jellyfish and ctenophores occur
throughout the Red Sea (Alamaru et al. 2009; Cruz-Rivera and
El-Regal 2015) and provide a readily available, albeit tempo-
rary, resource for consumers, but their utilization by coral reef
fishes is largely unknown. The present study describes the
feeding behavior of the rabbitfish Siganus rivulatus and sur-
geonfish Zebrasoma desjar dinii in relation to gelatinous zoo-
plankton (Ctenophora and Scyphozoa) in the northern Red
Sea.
Materials and methods
Initial observations of the rabbitfish Siganus rivulatus
attacking individuals of the Moon jellyfish Aurelia aurita
(Linnaeus, 1758) were made during a period of jellyfish abun-
dance in patch reefs off the coast of El Gouna, Egypt (approx-
imately 27°20.83′N, 33°49.63′E), in early July 2010. Such
observations were performed by snorkeling, and a combina-
tion of video and visual records were used. In July 2012, when
A. aurita was present at the same location, a pilot study was
conducted in an attempt to quantify the feeding behavior.
Observations made while SCUBA diving were too few and
we had to wait until May 2015 when a jellyfish bloom (a
combination of ctenophores and A. aurita)infringingreefs
along the coast of Hurghada, Egypt (approximately 27°4.72′
N, 33°53.03′E), allowed us to continue the quantification of
herbivorous fishes feeding on gelatinous plankton.
Two divers conducted 12 SCUBA dives (roving diving
technique) in May and June 2015 to study fishes feeding on
gelat inous z ooplankton. Prey individua ls, and as a conse-
quence their consumption by fish, were only observed at
0.5–7 m depth. Prey species, the number of fish per individual
prey, and the species composition of the feeding fish assem-
blage were recorded. Divers collected photo and video docu-
mentation supporting later analysis of the fish behavior. The
earlier observations done in July 2012 were added to the
database.
Results
In May and June 2015, several fish species including herbi-
vores were preying on unknown species of relatively large
ctenophores (length ≤100 mm; Fig. 1a) and individuals of
the Moon jellyfish Aurelia aurita in coral reefs off
Hurghada, Egypt. The latter had already been observed in
July 2012 in coral reefs off El Gouna, Egypt (Fig. 1b ).
Fishes fed on ctenophores by frequently attacking their bodies
until they disintegrated into fragments (Electronic
Supplementary Material). In the case of scyphozoans, fish
fed on the pulsating bells until the prey organisms sank to
Fig. 1 a Individuals of Siganus rivulatus and Chaetodon fasciatus
feeding on a ctenophore (arrow), b two individuals of S. rivulatus
feeding on Aurelia aurita, c Aurelia aurita showing feeding scars
(arrows) from fish attacks
Mar Biodiv
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the bottom. Feeding scars were clearly visible on the edge of
the bell (Fig. 1c).
Ctenophores were most frequently preyed upon b y
Siganus rivulatus (37 % of recorded attacks), followed by
Chaetodon fasciatus (27 %) and Zebrasoma desjardinii
(17 %; Table 1). These three species were also the most dom-
inant fishes feeding on Aur elia aurita,withS. rivulatus, C.
fasciatus and Z. desjardinii representing 51, 12 and 24 % of
the attacks, respectively (Table 1). All other fishes feeding on
gelatinous zooplankton accounted for ≤6 % of the observa-
tions (Table 1). The mean number of 2.3 and 3.3 individuals
per prey for S. rivulatus showed that this species was mostly
represented by two or more predatory fish simultaneously
(Table 1). This was found for ctenophores (Fig. 1a) and for
A. aurita (Fig. 1b). Similarly as observed for S. rivulatus, Z.
desjardinii, Diplodus noct and Chromis weberi were mostly
feeding simultaneously with two or more individuals
(Table 1). Once a prey was attacked, other fish appeared to
join the feeding. The total number of fish predators per prey,
independent of species, ranged from 1 to 8 individuals.
Schools of Abudefduf vaigiensis, Chromis weberi
(Pomacentridae), Caesio suevica (Caesionidae) and
Rastrelliger kanagurta (Cuvier, 1816; Scombridae) were reg-
ularly seen about the feeding fishes, but usually higher in the
water column without directly approaching ctenophores and
individuals of A. aurita. Few initial phase individuals of
Scarus ferrugineus Forsskål, 1775 (Scaridae) were seen ap-
proaching feeding fishes, but actual feeding of the latter spe-
cies was not recorded.
Discussion
In the present study, S. rivulatus actively selected ctenophores
and scyphozoans as prey items. While this species consumes a
wide variety of algae, it feeds less selectively during cold
seasons and is reported to accidentally ingest small inverte-
brates while feeding on algae (Lundberg et al. 2004;Bariche
2006; Shakman et al. 2009). Predation on ctenophores by this
fish has not been previously recorded, and data on consump-
tion of A. aurita have not been presented before. Cruz-Rivera
and El-Regal (2015) observed attacks on the jellyfish Cephea
cephea and concluded that rabbitfishes were the feeding spe-
cies. The direct observations of feeding activity resulting in
scars on the bell of A. aurita (Fig. 1c) c onfirmed that
S. rivulatus feeds on scyphozoans. Moreover, deliberately
feeding on animal tissue by siganids has not been reported
before. Kuo et al. (2015) found the congeneric S. fuscescens
leaving grazing scars on soft coral tissue, but this damage
resulted from feeding on algae growing at the surface of the
soft coral.
Pelagic fishes are known to feed on ctenophores and are
well adapted to utilize this food resource (Mianzan et al. 1996;
Cardona et al. 2012; Milisenda et al. 2014). Similarly, preda-
tion on planktonic cnidarians has been widely documented for
pelagic fishes (Purcell and Arai 2001;Arai2005). In the case
of coral reef fishes, species that have been reported to feed on
gelatinous zooplankton have been predominantly generalist
carnivores (Purcell and Arai 2001; Arai 2005), which was
supported by our findings. Of the 12 fish species recorded to
attack ctenophores and jellyfish in our study in the northern
Red Sea, all but 3 are considered carnivorous, and only 1
(Abudefduf vaigiensis) belongs to a taxon of more specialized
planktivo res (Table 1). Herbivorous fishes find their main
food source in coral reefs or other coastal waters, and are
usually limited to feeding on algae. In the northern Red Sea,
algal growth may vary seasonally, with a decline in algal cover
starting in late spring and early summer (Benayahu and Loya
1977; Mergner and Svoboda 1977). The ability to utilize sea-
sonal blooms of gelatinous zooplankton as an alternative food
Table 1 Fish species (with
taxonomic authority and family
taxon) in order of predation
dominance (%) on Ctenophora
(n = 66) and Aurelia aurita
(n = 20) and mean number of
feeding fish per prey individual
Species Taxonomic authority Family Ctenophora Aurelia aurita
%Mean% Mean
Siganus rivulatus Forsskål and Niebuhr, 1775 Siganidae 37 2.3 51 3.3
Chaetodon fasciatus Forsskål, 1775 Chaetodontidae 27 1.7 12 1.4
Zebrasoma desjardinii (Bennet, 1936) Acanthuridae 17 2.4 24 2.0
Chaetodon auriga Forsskål, 1775 Chaetodontidae 6 1.2 2 1.0
Chromis weberi Fowler and Bean, 1928 Pomacentridae 4 2.3 ––
Thalassoma rueppellii (Klunzinger, 1871) Labridae 3 1.0 ––
Heniochus intermedius Steindachner, 1893 Pomacanthidae 3 1.3 ––
Caesio suevica Klunzinger, 1884 Caesionidae 2 1.0 ––
Naso hexacanthus (Bleeker, 1855) Acanthuridae 1 1.0 ––
Diplodus noct (Valenciennes, 1830) Sparidae –– 62.0
Cantherhinus pardalis (Rüppell, 1837) Monacanthidae –– 32.0
Abudefduf vaigiensis (Quoy and Gaimard, 1825) Pomacentridae –– 21.0
Mar Biodiv
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source by S. rivulatus and other herbivores would be clearly
advantageous.
Three previous studies suggest that the opportunistic use of
gelatinous zooplankton by herbivorous marine fish may be
underappreciated. First, Senta et al. (1993) reported that sipho-
nophores and thaliaceans (but no algae) were common in the
gut contents of two species of Kyphosus.Ofthese,K.
cinerascens (Forsskål, 1775) has been found to be a predom-
inantly herbivorous species by other researchers using similar
methods (Clements and Choat 1997). Second, gut content
analyses by Choat et al. (2002) found that four species of
unicornfish (Naso spp.) consumed moderate to predominant
amounts of gelatinous zooplankton. Finally, qualitative obser-
vations of predation on the scyphozoan Cephea cephea by S.
stellatus, S. rivulatus and Zebrasoma desjardinii in the Red
Sea have recently been reported (Cruz-Rivera and El-Regal
2015). The acanthurid Z. desjardinii was one of the three
species that readily consumed ctenophores and scyphozoans
in the present study. Taken together, these observations sug-
gest that the trophic role of some coral reef fish, particularly
some siganids, requires a reevaluation.
Acknowledgment We greatly acknowledge the support of Khamis
Elsayed (Dive Pro Academy) for providing an excellent diving
infrastructure.
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