Associations between gelatinous zooplankton and hyperiid amphipods (Crustacea: Peracarida) in the Gulf of California

Abstract

Hyperiid amphipods are pelagic crustaceans that live associated with gelatinous zooplankton including medusae, ctenophores,
siphonophores, and salps. Standard plankton sampling disrupts natural associations, so the most reliable way to determine
an association is through direct observation of the organisms in their environment. The planktonic fauna of the Gulf of California
dwelling between 10 and 3000 m was surveyed using SCUBA diving and a remotely operated submersible (ROV) during March 2003.
Here we report our observations on a total of 14 symbiotic associations found between the hyperiid amphipods and various taxa
of gelatinous zooplankton. We found parental care behavior in a group of amphipods (Oxycephalidae) in which this phenomenon
has not been previously reported. For two hyperiid species, Euthamneus rostratus and Vibilia australis, we present the first information on their symbiotic relations. Additional hosts were discovered for other well-known and
widely distributed hyperiid species (i.e. Brachyscelus crusculum, Hyperoche medusarum). Photographic evidence of some of these interactions is included in this contribution. This is the first survey of these
relationships in the Gulf of California, and many aspects of the ecology and biology of these symbioses remain to be studied.

Full text

Associations between gelatinous zooplankton and hyperiid amphipods
(Crustacea: Peracarida) in the Gulf of California
Rebeca Gasca
1,3
& Steven H.D. Haddock
2,
*
1
El Colegio de la Frontera Sur (ECOSUR). Apdo. Post. 424. Chetumal, Q. Roo 77000, Mexico
2
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA
3
Present address: Research Associate, National Museum of Natural History, Smithsonian Institution,
Washington, D.C., USA
(*Author for correspondence: E-mail: haddock@mbari.org)
Key words: symbiosis, plankton, siphonophores, medusae, ctenophores
Abstract
Hyperiid amphipods are pelagic crustaceans that live associated with gelatinous zooplankton including
medusae, ctenopho res, siphonophores, and salps. Standard plankton sampling disrupts natural associa-
tions, so the most reliable way to determine an association is through direct observation of the organisms in
their environment. The planktonic fauna of the Gulf of California dwelling between 10 and 3000 m was
surveyed using SCUBA diving and a remotely operated submersible (ROV) during March 2003. Here we
report our observations on a total of 14 symbiotic associations foun d between the hyperiid amphipods and
various taxa of gelatinous zooplankton. We found parental care behavior in a group of amphipods
(Oxycephalidae) in which this phenomenon has not been previously reported. For two hyperiid species,
Euthamneus rostratus an d Vibilia australis, we present the first information on their symbiotic relations.
Additional hosts were discovered for other well-known and widely distributed hyperiid species (i.e.
Brachyscelus crusculum, Hyperoche medusarum). Photographic evidence of some of these interactions is
included in this contribution. This is the first survey of these relationships in the Gulf of California, and
many aspects of the ecology and biology of these symbioses remain to be studied.
Introduction
Hyperiid amphipods have been advanced as a
polyphyletic group (Bowman & Gruner, 1973),
bringing together the descendants of different lin-
eages of benthic forms that have developed a
benthic-like existence on the pelagic substratum
provided by gelatinous zooplankton (Laval, 1980).
The relatively low host specificity and the mor-
phological evidence provided by the analysis of the
mouthparts suggest that parasitism in hyperiid
amphipods has evolved only recently (Ditt rich,
1988, 1992). Hyperiids are associated with differ-
ent kinds of gelatinous zooplankton at the onset of
their existence, when they are assumed to be strict
parasites (Dittrich, 1987, 1992); the duration of the
association depends on the hyperiid species and
varies according to biological and ecological fac-
tors. The relationship is nearly always detrimental
to the host, although Vader (1983) categorized the
different types of hyperiid relations as ectocom-
mensalism, endocommensalism, protection, and
micropredation, while hyperiids also obtain
buoyancy and transportation. It is assumed that
most hyperiid amphipods are not biologically
suited to a pelagic free-living existence (Laval,
1980).
Some genera and even families appear to be
restricted to associations with certain host groups,
but we are far from being able to know the
mechanisms or specificity for host selec tion. The
juveniles expelled from the pouch, in many cases
Hydrobiologia 530/531: 529–535, 2004.
D.G. Fautin, J.A. Westfall, P. Cartwright, M. Daly & C.R. Wyttenbach (eds),
Coelenterate Biology 2003: Trends in Research on Cnidaria and Ctenophora.
Ó 2004 Kluwer Academic Publishers. Printed in the Netherlands.
529

without swimming appendages (Dittrich, 1992),
would have a very little likelihood of encountering
a host by themselves. The adult female does not
produce a large number of eggs to compensate for
this low probability of host encounter; therefore,
she is responsible for the dissemination of her
limited progeny, seeking the correct hosts and
demarsupiating on them.
Prior works have described some of these pe-
culiar symbiotic interactions (Madin & Harbison,
1977; Thurston, 1977; Laval, 1980). In this con-
tribution, we report our observations on the
interaction of hyperiids with different gelatinous
zooplankton obtained during surveys of the water
column between the surface and 3000 m in four
different areas of the Gulf of California.
Methods
The planktonic fauna of the Gulf of California
was surveyed during an oceanographic cruise
carried out aboard the R/V Western Flyer of the
Monterey Bay Aquarium Research Institute
(MBARI). The cruise took place between March
12 and 31, 2 003, and included sampling stations in
Guaymas, Pescadero, and Farallon Basins and
Alarco
´
n seamount of the southern Gulf of Cali-
fornia (Fig. 1). We used blue-water SCUBA diving
to survey the upper 20 m, and a remotely operated
submersible (ROV) to sample the zooplankton
fauna between 200 and 3000 m depths. Specimens
were captured together with their associated hy-
periids in glass jars on SCUBA dives, or using
‘detritus samplers’ described by Youngbluth
(1984) for the ROV sampl es. In short, the samplers
are acrylic cylinders with hydraulically actuated
lids on the top and bottom. These slide closed to
seal the vessel when the animal has been maneu-
vered into the chamber. Once brought on board
the ship, the host species and its associated cope-
pods and amphiods were examined and identified.
After this initial manipulation in vivo, the speci-
mens were fixed in 4% formaldehyde and pre-
served in a solution of propylene glycol (4.5%),
propylene phenoxetol (0.5%), and sea water (95%)
for further taxonomic examination. The identifi-
cation of the hyperiid amphipods was made using
the ke ys, illustrations, and descriptions of Zeidler
(1992, 1998), Shih & Chen (1995), and Vinogradov
et al. (1996). The hydromedusa described herein as
Aequorea coerulescens was called A. macrodactyla
Figure 1. The Gulf of California region showing the stations where ROV and blue-water SCUBA dives were conducted.
530

by Stretch & King (1980) during their study of the
region.
Results and discussion
We identified the following gelatinous organisms
carrying hyperiid amphipods: two species of
hydromedusae, and one each of scyphomedusa,
siphonophore, salp, heteropod mollusc, and
ctenophore (Fig. 2). Up to six species of hyperiids
were recorded in association with these animals
(Table 1). Previous faunistic work in the Gulf
(Siegel-Causey, 1982; Brinton et al., 1986) has re-
ported on the composition and distribution of the
hyperiid fauna, but not in relation with their hosts.
Figure 2. Amphipods and their gelatinous hosts. (A) Vibilia australis on Cyclosalpa bakeri. (B) Hyperoche medusarum on Chro-
matonema erythrogonon. (C, D) Parascelus typhoides on Athorybia rosacea. (E) Oxycephalus clausi female and juveniles on Ocyropsis
crystallina crystallina. (F) Brachyscelus crusculum and (G) Sapphirina nigromaculata on Aequorea coerulescens. (H) Euthamneus
rostratus on Pelagia noctiluca. (I) Euthamneus rostratus juveniles on Aequorea coerulescens.
531

Table 1. Amphipods (A) and copepods (Co) associated with different gelatinous taxa (M = medusae; S = siphonophores; Ct = ctenophores; H = heteropod) collected in
the Gulf of California at different depths (in m) during the survey period
Associated crustacean Host Locality Depth (m) Dive
Hyperoche medusarum (Kro
¨
yer, 1838) (A) w/eggs Chromatonema erythrogonon (Bigelow, 1909) (M) Carmen Basin 1100 ROV 546
Vibilia australis Stebbing, 1888 (A) Cyclosalpa bakeri Ritter, 1905 (Salp) Alarco
´
n Seamount 244 ROV 547
Brachyscelus crusculum (A) w/larvae in marsupium Pterotrachea hippocampus Philippi, 1836 (H) Pescadero Basin 15 BW9
Brachyscelus crusculum Bate, 1861 (A) Aequorea coerulescens (Brandt, 1838) (M) Isla Cerralvo 10 BW1
Brachyscelus crusculum (A) with eggs Aequorea coerulescens (M) Farallon Basin 15 BW3
Brachyscelus crusculum (A) & Sapphirina
nigromaculata Claus, 1863 (Co)
Aequorea coerulescens (M) Guaymas Basin 10 BW4
Brachyscelus crusculum juv. male (A) &
Sapphirina nigromaculata (Co)
Aequorea coerulescens (M) Alarco
´
n Seamount 10 BW10
Brachyscelid (A) unidentifiable juv. Aequorea coerulescens (M) Pescadero Basin 10 BW8
Euthamneus rostratus (A) adult and juv. Pelagia noctiluca (Forska
˚
l, 1775)(M) Pescadero Basin 10 BW8
Euthamneus rostratus (Bovallius, 1887) (A) juv. Aequorea coerulescens (M) Farallon Basin 10 BW3
Oxycephalus clausi Bovallius, 1887 (A) and juv. Ocyropsis crystallina crystallina (Rang, 1826) (Ct) Pescadero Basin 10 BW2
Oxycephalus clausi Bovallius, 1887 (A) and juvs. Ocyropsis crystallina crystallina (Ct) Farallon Basin 10 BW5
Parascelus typhoides Claus, 1879 (A) Athorybia rosacea (Forska
˚
l, 1775) (S) Isla Cerralvo 10 BW1
Parascelus typhoides (A) Athorybia rosacea (S) Pescadero Basin 10 BW8
532

Parental care
Many benthic amphipods have shown different
degrees of parental care (Thiel, 1997; Thiel et al.,
1997), whereas this phenomenon seems to be quite
unusual (or unknown) in the planktonic forms.
Members of the hyperiid family Phronimidae are
the only hyperiid crustaceans for which maternal
care has been reported (Thiel, 1976, 2000). In this
family, the mother feeds and keep the larvae
within barrel-shaped salp tests after demarsupia-
tion. In our study, a female of Oxycephalus clausi,
a member of the family Oxycephalidae, was ob-
served taking care of the juveniles demarsupiated
into the ctenophore Ocyropsis crystallina; the fe-
male was keeping the young individuals (ca. 30
juveniles) on the surface of the ctenophore, where
they were randomly distributed across the host.
The female, using her pereopods, kept the juvenile-
carrying ctenophore in constant motion and swam
about in different directions without losing con tact
with the ctenophore (Fig. 2E). Thi s behavior per-
sisted for several hours after the time of collection.
This is the first report of maternal care in this
hyperiid family; further studies could elucidate if,
as reported for the Phronimidae, the oxycephaliids
also feed their larvae or if they feed directly on the
ctenophore tissues. Demarsupiation is yet another
interesting process by which the females expell s the
larvae from her pouch to the host surface where
they can feed upon the host tissues (Laval, 1980).
This phenomenon was not observed in the speci-
mens examined herein.
Remarks on the species
Shih & Chen (1995) stated that most of the asso-
ciations reported in the literature involve amphi-
pods of the families of the Infraorder
Physocephalata (except for some Scina); all the
species recorded herein belong to this taxon.
Euthamneus rostratus is a relatively rare species,
but it is widely dist ributed; it has been known to
occur in tropical as well as temperate areas. It was
found at a depth of 10 m associated with the
scyphomedusa Pelagia noctiluca (Fig. 2H) and the
hydromedusa Aequorea coerulescens (Fig. 2I),
both of which are known to host a wide variety of
hyperiids (Laval, 1980). However, there are no
previous records of symbiosis of this hyperiid.
Vibilia australis is a species widely distributed
in the surface waters of the tropical latitudes of the
oceans. This genus is said to be restricted to salps
(see Madin & Harbison, 1977), and in our case it
was recovered from Cyclosalpa bakeri collected
with the ROV. However, as noted for E. rostratus,
this is the first information about the symbiotic
relation of this hyperiid species.
Parascelus typhoides dwells in the upper 200 m
layer. It is a relatively rare species distributed in
tropical and temperate regions. The females of this
species were recently synonymized under P. ed-
wardsi Claus, 1879, by Zeidler (1998) . This species
has been found in the siphonophore Forskalia
?edwardsi Ko
¨
lliker, 1853 (Laval, 1980), and in our
surveys two females of this species were recorded
at a depth of 10 m in association with another
siphonophore, Athorybia rosacea (Fig. 2C and D).
Brachyscelus crusculum is a common epipelagic
form, widely distributed in the oceans. This species
has been found in symbiosis with several groups of
pelagic organisms, mainly with salps (Salpa fusi-
formis Cuvier, 1804, Salpa maxima Forska
˚
l, 1775,
Thalia democratica (Forska
˚
l, 1775)) but also with
medusae (Aequorea spp.) and heteropod molluscs
(Pterotrachea spp.) (see Laval, 1980). On several
occasions, we found this species associated with
the hydromedusa Aequorea coerulescens (Fig. 2F)
and with the heteropod Pterotrachea hippocampus.
The only male specimen in any of our samples was
a juvenile of this species associated with A. coe-
rulescens.
Hyperoche medusarum is considered to be a
bipolar form; it was recorded at 1100 m depth in
the Gulf of California. This amphipod has been
found in symbiosis with a wide variety of pelagic
coelenterates, including six species of medusae,
and six ctenophores (see Laval, 1980). The finding
of this species with the medusa Chromatonema
erythrogonon has not been reported before and
adds this species to the host list of H. medusarum
(Fig. 2B). (The specimens referred to herein as
H. medusarum show some morphological differ-
ences from previous descriptions. Hence, if the
taxonomic status of these sp ecimens changes, this
record could reflect to a new association.)
Oxycephalus clausi (Fig. 2E) has been found
more frequently in ctenopho res such as Eurham-
phaea vexilligera Gegenbaur, 1856, Mnemiopsis
mccradyi Mayer, 1900, Bolinopsis vitrea (L. Agassiz,
533

1860), and Ocyropsis maculata (Rang, 1826),
among others (Harbison et al., 1978); the list in-
cludes also Ocyropsis crystallina crystallina on
which it was found during this survey. It has also
been found associated with the heteropod mollusc
Pterotrachea hippocampus and with the tunicates
Pegea socia and Salpa cylindrica (Madin & Harbi-
son, 1977).
General remarks
There is still much to be studied with respect to
these biological interactions. Some authors suggest
that hyperiids associate with hosts only intermit-
tently for food, transportation, or protection
(Vader, 1983; Dittrich, 1992). Others argue that
these crustaceans are mostly free-living forms
(Evans & Sheader, 1972; Westernhagen, 1976),
while a third view is that they are obligate sym-
bionts of their hosts and that they are not able to
survive independently (Laval, 1980). The range of
behavior within these associations is very wide:
some species show a parasitoid behavior, leaving
their offspring in the host, while other species have
a marked and relatively prolonged parental care.
Another interesting issue yet to be studied is
whether males are more independent from hosts
than females. Males are not usually found on the
hosts and some hyperiid males even remain un-
known (Laval, 1980). We found only one juvenile
male (B. crusculum) associated with the gelatinous
zooplankton examined herein. New investigative
efforts could be directed to find out if these sym-
biotic relations are species-specific or are estab-
lished between well-defined taxa. This could lead
to an improved understanding of the degree of co-
evolution of hyperiids with their hosts (see Dit-
trich, 1992). Many unanswered questions remain
concerning reproduction and development, fertil-
ity, and the impact of parental care on the species
success-survival. Further in situ observations and
direct collections will improve our understanding
of these complex and fascinating interactions
between phyla.
Acknowledgments
We thank Bruce Robison for inviting Rebeca
Gasca to participate on the cruise where this work
was initiated. Eduardo Sua
´
rez-Morales, Iva
´
n
Castellanos, and Edgar Tovar (ECOSUR-Chetu-
mal) helped in the identification of some of the
organisms. This work was developed during a
sabbatical year of R.G. spent at the National
Museum of Natural History, Smithsonian Insti-
tution, Washington, DC. Important support was
received from CONACYT (Mexico) through a
sabbatical award for foreign institutions (ref.
010379/2002) and from the David and Lucile
Packard Foundation.
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