Field observations on the feeding of the Nudibranch Gymnodoris spp. in Japan

Abstract

Here, we report field observations of the diets of some Gymnodoris species (Nudibranchia: Opisthobranchia) inhabiting warm waters in the vicinity of Japan. Some Gymnodoris species appeared to feed exclusively on a single species: G. ceylonica fed on Nakamigawaia sp.; G. okinawae on Elysia sp.; G. striata on Elysia ornata; and an undescribed Gymnodoris sp. fed on Glossodoris cincta. In contrast, other Gymnocloris species fed on multiple species: G. citrina fed on G. okinaivae and eggs of nudibranchs; G. inornata fed on G. rubropapulosa and Dendrodoris fumata; and G. rubropapulosa fed on Chromodoris annae, C strigata, Chromodoris sp., Hypselodoris festiva, and Mexichromis multituberculata.

Full text

Field Observations on the Feeding of the Nudibranch Gymnodoris spp.
in Japan
RIE NAKANO
Department of Chemistry, Biology, and Marine Science, Faculty of Science, University of the Ryukyus, Nishihara,
Okinawa 903-0213, Japan
KOTARO TANAKA
Diving Club Concolor, Mitsune 4419-6, Hachijo-jima Is, Tokyo 100-1511, Japan
SHIN-ICHI DEWA
Diving Service Umi-annai, Masagohoncho 7-7, Kagoshima, Kagoshima 890-0067, Japan
KENJI TAKASAKI
Asada 820, Yamaguchi, Yamaguchi 753-0871, Japan
AND
ATSUSHI ONO
Dive Service Ono Nyi Nyi, Ama 532-1, Zamami, Okinawa 901-0032, Japan
Abstract. Here, we report field observations of the diets of some Gymnodoris species (Nudibranchia:
Opisthobranchia) inhabiting warm waters in the vicinity of Japan. Some Gymnodoris species appeared to feed
exclusively on a single species: G. ceylonica fed on Nakamigawaia sp.; G. okinawae on Elysia sp.; G. striata on Elysia
ornata; and an undescribed Gymnodoris sp. fed on Glossodoris cincta. In contrast, other Gymnodoris species fed on
multiple species: G. citrina fed on G. okinawae and eggs of nudibranchs; G. inornata fed on G. rubropapulosa and
Dendrodoris fumata;andG. rubropapulosa fed on Chromodoris annae,C. strigata,Chromodoris sp., Hypselodoris
festiva,andMexichromis multituberculata.
INTRODUCTION
Except for some species of Cephalaspidea, Sacoglossa,
and Anaspidea, opisthobranch mollusks are carnivo-
rous. Each carnivorous opisthobranch feeds on partic-
ular prey items, e.g., sponges, hydroids, bryozoans, or
ascidians. Some carnivorous opisthobranchs prey on
other opisthobranchs and their eggs (see Behrens,
2005). These opisthobranch-feeding opisthobranchs
include Chelidonura (Gosliner et al., 1996), Navanax
(Paine, 1963), Philinopsis (Rudman, 1972), Pleurobran-
chaea (Battle & Nybakken, 1998), Gymnodoris (Kay &
Young, 1969), Roboastra (Farmer, 1978), Melibe (Kay,
1979), and Godiva (Gosliner, 1987b). Gymnodoris
species usually feed on opisthobranchs and/or their
eggs, except for Gymnodoris nigricolor, which appar-
ently lives on some species of goby (Osumi & Yamasu,
1994), such as Amblyeleotris japonica (Williams &
Williams, 1986), by grasping the fins using their buccal
apparatus.
Few studies have reported on the diets of other
Gymnodoris species, particularly in their natural
habitats. To date, diets have been reported for nine
Gymnodoris species (Table 1). Some Gymnodoris spe-
cies appear to feed exclusively on a single species,
whereas others feed on multiple species. However, there
is considerable doubt whether animals in the laborato-
ry show their natural food habits. Therefore, data on
the feeding behavior of Gymnodoris species should be
collected in their natural habitat. To this end, we
examined diets of some Gymnodoris species inhabiting
warm waters in the vicinity of Japan.
MATERIALS
AND
METHODS
From 2000 to 2006, Gymnodoris species feeding on prey
in their natural habitats were directly observed by
SCUBA diving at Hachijo-jima Island, Tokyo (33u69
N, 139u469E), Ohomi-jima Island,Yamaguchi (34u259
The Veliger 49(2):91–96 (July 2, 2007)
THE VELIGER
#CMS, Inc., 2006

N, 131u139E), Nagashima Island, Kagoshima (32u139
N, 130u119E), Kinko-wan Bay, Kagoshima (31u339N,
130u379E), Aka-jima Island, Okinawa (26u129N,
127u179E), Gahi-jima Island, Okinawa (26u139N,
127u179E), and Zamami-jima Island, Okinawa (26u139
N, 127u179E). Predators and prey were identified by
their external morphology and were photographed in
situ. Body lengths were measured in situ using a ruler or
determined from the photographs. We observed the
following species: Gymnodoris ceylonica (Kelaart,
1858), G. citrina (Bergh, 1875), G. inornata Bergh,
1880, G. okinawae Baba, 1936, G. rubropapulosa
(Bergh, 1905), G. striata (Eliot, 1908; .G. amakusana
[Baba, 1996]), and an undescribed Gymnodoris sp. This
undescribed species is often found around the Okinawa
Islands and is recognized by its Japanese common
name ‘‘Shirobonbon-umiushi’’ (cf. Ono, 2004).
RESULTS
AND
DISCUSSION
All feeding observations for Gymnodoris spp. are
summarized in Table 2. We observed sixteen individ-
uals of seven species of Gymnodoris. All individuals
swallowed the prey whole, even if the prey’s body
length was the same as that of the predator. In one case
of G.citrina (No. 3) and in two cases of G.amakusana
(No. 14 and No. 15), the predators were smaller in
body length than their prey and bit off pieces from the
prey.
Johnson & Boucher (1983) reported that G. ceylonica
feeds on the sea hare Stylocheilus longicauda; however,
we believe they misidentified S. striatus (Quoy &
Gaimard, 1832) as S. longicauda. Because of their
similarity in body color, S. striatus is often misidenti-
fied as S. longicauda (Rudman, 1999a), but habitat use
Table 1
Summary of the proceeding studies on the diets of Gymnodoris spp.
Predator Prey Condition Reference
Gymnodoris alba (Bergh, 1877) Aeolidiella sp. undescribed Kay & Young, 1969; Kay, 1979
Favorinus sp. undescribed Kay & Young, 1969; Kay, 1979
Sakuraeolis modesta laboratory Hughes, 1983
Flabellina alisonae laboratory Hughes, 1983
Phyllodesmium sp. laboratory Hughes, 1983
Gymnodoris aurita (Gould, 1852) Marionia sp. field Behrens, 2005
Gymnodoris bicolor (Alder &
Hancock, 1866) (,G. citrina?)
1
members of Gymnodoris undescribed Young, 1969
Gymnodoris okinawae undescribed Young, 1969; Kay & Young, 1969; Kay,
1979
the egg masses of Gymnodoris
okinawae
undescribed Young, 1969
Gymnodoris plebeia undescribed Young, 1969; Kay & Young, 1969; Kay,
1979
Gymnodoris ceylonica (Kelaart,
1858)
Stylocheilus longicauda undescribed Johnson & Boucher, 1983
Gymnodoris citrina (Bergh, 1875) Gymnodoris citrina laboratory Young, 1969
Gymnodoris citrina field Johnson & Boucher, 1983; Johnson, 1992
Gymnodoris okinawae field Johnson, 1992
Gymnodoris plebeia field Johnson, 1992
several Gymnodoris species field Johnson & Boucher, 1983
unknown Gymnodoris spp. field Johnson, 1992
eggs of other Gymnodoris species field Johnson & Boucher, 1983; Johnson, 1992
eggs of Gymnodoris ceylonica field Johnson, 1992
Gymnodoris inornata Bergh,
1880
Chromodoris orientalis laboratory Hughes, 1983
Doriopsilla miniata laboratory Hughes, 1983
Gymnodoris okinawae Baba,
1936
various species of the genus
Elysia
undescribed Kay & Young, 1969
members of Elysiidae undescribed Young, 1969
cephalaspidean undescribed Johnson & Boucher, 1983
did not eat Elysia laboratory Johnson & Boucher, 1983
Gymnodoris rubropapulosa
(Bergh, 1905)
Hypselodoris iacula field Behrens, 2005
Gymnodoris striata (Eliot, 1908) Plakobranchus ocellatus field and
laboratory
Johnson & Boucher, 1983
1
Gymnodoris bicolor (Alder & Hancock, 1866) is regarded as the junior synonym of G. ctrina (Bergh, 1875) by many authors (e.g.,
Risbec, 1953; MacNae, 1958; Baba, 1960), although Young (1969a) described their internal morphologies discriminate G. bicolor.
Page 92 The Veliger, Vol. 49, No. 2

Table 2
Gymnodoris spp. and their preys: field observation.
Predator No.
Body
length
Prey
(body length)
Water
temperature Site
1
Depth
2
Habitat Date
Gymnodoris ceylonica (Kelaart,
1858)
01 20 mm Nakamigawaia sp. (8 mm) NR Aka Is. 6 m sand Summer, 2002
Gymnodoris citrina (Bergh, 1875) 02 20 mm Gymnodoris okinawae
(10 mm)
19uC Hachijo Is. 5 m rock, occasional coral 6, February, 2002
03 10 mm Gymnodoris okinawae
(18 mm)
20uC Hachijo Is. 5 m rock April, 2003
04 12 mm eggs of nudibranch NR Gahi Is. 4 m dead coral May, 2001
Gymnodoris inornata Bergh,
1880
05 50 mm Gymnodoris rubropapulosa
(50 mm)
NR Kinkoh Bay 15 m rock, occasional sand Autumn, 2002
06 50 mm Dendrodoris fumata (40 mm) 16.8uC Kinkoh Bay 11 m mud 8, January, 2006
Gymnodoris okinawae Baba,
1936
07 18 mm Elysia sp. (18 mm) 20uC Hachijo Is. 5 m rock April, 2003
Gymnodoris rubropapulosa
(Bergh, 1905)
08 30 mm Chromodoris annae (25 mm) 25uC Hachijo Is. NR rock November, 2004
09 50 mm Chromodoris strigata
(30 mm)
27uC Hachijo Is. 10 m rock 18, June, 2000
10 30 mm Chromodoris sp. (20 mm) 25uC Hachijo Is. NR rock November, 2004
11 30 mm Chromodoris sp. (15 mm) 21uC Hachijo Is. 5 m rock 30, May, 2006
12 30 mm Hypselodoris festiva
(15 mm)
25uC Hachijo Is. NR rock November, 2004
13 50 mm Mexichromis
multituberculata (20 mm)
24uC Gahi Is. 20 m dead coral May, 2000
Gymnodoris amakusana
3
(Baba,
1996)
14 20 mm Elysia ornata (50 mm) 15uC Ohmi Is. 6 m muddy sand 21, December, 2003
15 10 mm Elysia ornata (40 mm) 12.5uC Nagashima
Is.
10 m muddy sand,
occasional rock
7, January, 2001
Gymnodoris sp. 16 60 mm Glossodoris cincta
(unknown)
22uC Zamami Is. 15 m sand May, 2001
1
See ‘‘materials and method’’ for details.
2
NR, No record.
3
Rudman (1999c) referred G. amakusana as a junior synonym of G. striata.
R. Nakano et al., 2006 Page 93

clearly differs between the species. Stylocheilus longi-
cauda is usually found on drifting brown algae in the
open ocean, where G. ceylonica never occurs (Rudman,
1999b), whereas S. striatus is benthic, and is often
found with G. ceylonica. We observed that G. ceylonica
feeds on Nakamigawaia sp. (Aglajidae, Cephalaspidea).
This undescribed species is often found in Japan and is
recognized by its Japanese common name ‘‘Kuro-
bouzu’’ (cf. Ono, 1999). Nakamigawaia sp. is usually
found on the sandy bottom. This observation indi-
cates the possibility that G. ceylonica feeds not only on
S. striatus, but also on other species in the same
habitat.
Two individuals of Gymnodoris citrina fed on the
congener G. okinawae, and one individual fed on the
eggs of a nudibranch. Gymnodoris citrina was reported
to feed on several Gymnodoris species, including G.
okinawae and G. plebeia, in the field (Johnson &
Boucher, 1983; Johnson, 1992), and on the eggs of
congeners, such h as G. ceylonica, in the field and in
aquaria (Young, 1967; Johnson & Boucher, 1983;
Johnson, 1992). Moreover, G. citrina is cannibalistic.
Young (1967) observed a 10-mm specimen consume a 6-
mm specimen in an aquarium and reported that this
occurrence was probably induced by unnaturally
crowded conditions in the aquarium. However, John-
son (1992) observed this behavior in the field, in
aquaria, and even in collecting jars, and concluded that
cannibalism is normal behavior for G. citrina. Thus, it
appears that G. citrina preys on several congeners and
their eggs, as well as on conspecifics.
We observed that Gymnodoris inornata fed on G.
rubropapulosa and Dendrodoris fumata in the field. In
previous studies, G. inornata was reported to feed on
Figure 1. Gymnodoris species feeding on opisthobranchs in their natural habitats. (A) G. okinawae (right) feeding on a sacoglossan
Thuridilla sp. (left). (B) G. rubropapulosa (left) feeding on Mexichromis multituberculata (right). (C) G. amakusana (left) feeding on
Elysia ornata (right). (D) Gymnodoris sp. (right) feeding on Glossodoris cincta (left). Scale bars 510 mm.
Page 94 The Veliger, Vol. 49, No. 2

Chromodoris orientalis and Dendrodoris miniata
(Hughes, 1983), but this was only observed in aquaria.
Further field surveys are required to determine whether
G. inornata feeds on these non-Gymnodoris species in
nature.
In our field observations, Gymnodoris okinawae fed
on Thuridilla sp. (Sacoglossa; Fig. 1A). This unde-
scribed Thuridilla species is commonly found in
southern parts of Japan, and is known by its Japanese
common name ‘‘Fujiiro-midorigai’’ (cf. Ono, 2004).
Kay & Young (1969) reported that G. okinawae fed on
various species of Elysia (Sacoglossa). These observa-
tions suggest that G. okinawae preys on the sacoglossan
family Elysiidae. In contrast, Johnson & Boucher
(1983) reported that their specimens did not feed on
several Elysia species in aquaria, but fed on small
cephalaspideans in undescribed conditions. We do not
know whether their specimens showed normal feeding
behavior, because the habitat in which they were
observed feeding, i.e., field or laboratory, was not
described. Further field studies should be conducted to
clarify whether G. okinawae feeds on cephalaspideans
in nature.
We observed that Gymnodoris rubropapulosa fed on
Chromodoris strigata,Chromodoris sp., Hypselodoris
festiva,andMexichromis multituberculata (Fig. 1B).
Behrens (2005) reported that G. rubropapulosa fed on
H. iacula. This species also fed on Glossodoris
rufomarginata,H. dollfusi,H. krakatoa,andM. marieri
(Behrens, personal communication). Chromodoris sp. is
an undescribed species that is commonly found only in
the vicinity of Hachijo-jima Island and the Bonin
Islands, and is recognized by its Japanese common
name ‘‘Kongasuri-umiushi’’ (cf. Nakano, 2004). These
observations suggest that G. rubropapulosa feeds on
various species of the family Chromodorididae. We
observed that G. amakusana fed on Elysia ornata
(Fig. 1C). In contrast, Rudman (1999c) referred to G.
amakusana as a junior synonym of G. striata, which
feeds on Plakobranchus ocellatus (Johnson & Boucher,
1983). If G. striata and G. amakusana are synonymous,
they may show the same food habits. Gymnodoris sp. or
Shirobonbon-umiushi differs from all other gymnodor-
ids in shape and color (Rudman, 1999d). It has a white
body with many large, puff-like pustules. We observed
this species feeding on Glossodoris cincta. This is the
first observation of its diet (Fig. 1D).
As described above, the diet of each Gymnodoris
species encompasses a particular range of species. Some
Gymnodoris species feed on various nudibranchs,
whereas others have more selective diets. However,
little is known about why and how Gymnodoris species
identify and select their prey. For instance, Paine (1963)
observed that the opisthobranch Navanax inermis
locates its prey by contact (not distance) chemorecep-
tion via the mucus trail of the prey. It is unknown
whether Gymnodoris species locate their prey using this
same method. To gain a better understanding of the
distinct food habits of these opisthobranch opistho-
branch-feeders, we should determine how they detect
and identify their prey, despite their low mobility.
Acknowledgments. We are grateful to Euichi Hirose (Univer-
sity of the Ryukyus) for providing constructive advice for the
completion of this paper. We also thank David W. Behrens
(Sea Challengers) and Constantinos Petrinos (photographer)
for kindly providing valuable information.
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