New records of Hyachelia tortugae Barnard, 1967, and H. lowryi Serejo and Sittrop, 2009 (Amphipoda, Gammaridea, Hyalidae), from Palmyra Atoll National Wildlife Refuge : cooccurrence on Pacific green turtles (Chelonia mydas)

AMERICAN MUSEUM NOVITATES

Number 3809, 12 pp.

July 30, 2014

New Records of Hyachelia tortugae Barnard, 1967,
and H. lowryi Serejo and Sittrop, 2009 (Amphipoda:
Gammaridea: Hyalidae), from Palmyra Atoll
National Wildlife Refuge: Cooccurrence on
Pacific Green Turtles (Chelonia mydas).

MIA G. YABUT, 1 ' 2 ERIC A. LAZO-WASEM, 2
ELEANOR J. STERLING, 3 AND ANDRfiS GOMEZ 3

ABSTRACT

Amphipods of the genus Hyachelia collected during an epibiont survey conducted over
three years (2009, 2010, and 2011) at Palmyra Atoll are reported. Both known species, i.e.,
Hyachelia tortugae Barnard, 1967, and Hyachelia lowryi Serejo and Sittrop, 2009, were collected
from Pacific green turtles, Chelonia mydas (Linnaeus). Given the increased awareness of epibi-
onts and the desire of researchers to make positive identifications, figures of the diagnostic
features of both amphipod species are presented. The significance of the cooccurrence of these
two species on Pacific green turtles ( Chelonia mydas ) is discussed.

INTRODUCTION

The genus Hyachelia was established by Barnard (1967) based upon a single ectocommen-
sal amphipod species, Hyachelia tortugae. Barnard noted that this “remarkable” species was the
first record of a talitroidean amphipod living as an ectocommensal. These specimens were

1 Department of Ecology and Evolutionary Biology, Yale University, New Haven CT.

2 Division of Invertebrate Zoology, Peabody Museum of Natural History, Yale University, New Haven, CT.

3 Center for Biodiversity and Conservation, American Museum of Natural History, New York, NY.

Copyright © American Museum of Natural History 2014 ISSN 0003-0082

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FIGURE 1. A. Hyachelia tortugae. AMNH 12533-10008-451, male 7.52 mm. B. H. lowryi. AMNH 12533-
11008-002, male 4.86 mm.

collected from the buccal cavity of a green turtle, Chelonia my das (Linnaeus, 1758), examined
in the Galapagos Islands in the Pacific Ocean. H. tortugae has subsequently been reported
sporadically from Hawai’i in the central Pacific Ocean (Balazs, 1980; Aguirre et al., 1998),
occurring on the same host species. Among other characteristics that will be detailed below,
Hyachelia can be easily distinguished from other hyalid genera by its elongate urosome and
uropods one and two, and a radically reduced third uropod. (fig. 1). A second species, Hyache¬
lia lowryi Serejo and Sittrop, 2009, was described as occurring not only on green turtles but
also upon loggerhead turtles, Caretta caretta (Linnaeus, 1758) from Queensland, Australia.
Additional specimens of both these species were obtained from material collected as part of

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YABUT ET AL.: NEW RECORDS OF HYACHELIA TORTUGAE AND H. LOWRYI

3

the American Museum of Natural History’s Center for Biodiversity and Conservation (New
York) survey of the epibionts living on Pacific green turtles foraging in the vicinity of Palmyra
Atoll National Wildlife Refuge (PANWR) (2009-2011); these represent new distributional
records of both H. tortugae and H. lowryi and only the second known occurrence of the latter.
The amphipods obtained as part of the survey are reviewed and provided herein is a taxonomic
commentary and species diagnosis that will allow for their better recognition.

Methods and Materials

Palmyra Atoll National Wildlife Refuge (PANWR; fig. 2) is situated approximately halfway
between the Hawaiian Islands and American Samoa in the Central Pacific Ocean (5°53' N,
162°5' W). The atoll and 12 nautical miles of the surrounding ocean have been designated a
marine protected area by the U.S. Fish and Wildlife Service since 2001 and the area forms part
of the U.S. Pacific Remote Islands Marine National Monument established in 2009 (U.S. Fish
and Wildlife Service, 2011).

Little is known about the ecology, behavior, biogeography, and conservation status of sea
turtles in the central Pacific Ocean (Sterling et al., 2013). Since 2005 the Center for Biodiversity
and Conservation from the American Museum of Natural History (New York) has been imple¬
menting a sea turtle research and conservation program at PANWR, with the primary goal of
investigating the ecology, population biology, and conservation of green and hawksbill turtles
on the atoll (Sterling et al., 2013). Turtles were captured using standard methods, and the epi-
biotic fauna of each animal was collected as part of a comprehensive physical evaluation.

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AMERICAN MUSEUM NOVITATES

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Amphipods were preserved in 95% alcohol, stored in plastic vials, and subsequently brought
to the Peabody Museum of Natural History, Yale University, for sorting and identification. The
amphipod specimens were counted, categorized by sex and/or life stage, and selected individuals
were isolated for dissection. Temporary and permanent microscope slide mounts were made of
appendages from dissected individuals. Microphotographs were made from the appendages, and
from these line drawings were generated digitally in Adobe* Illustrator* CS5 following the proce¬
dures described by Coleman (2003, 2009). All specimens are deposited in the collections of the
Department of Invertebrate Zoology, American Museum of Natural History, New York.

Specimens Figured

Hyachelia tortugae:

AMNH 12533-10008-451. Male, 7.52 mm. Palmyra Atoll, 19 July 2010; host: Chelonia
mydas. AMNH 12533 - 11008 - 008 . Male, 7.91 mm. Palmyra Atoll, 12 August 2011; host:
Chelonia mydas. AMNH 12533 - 11008 - 057 . Male, 7.98 mm. Palmyra Atoll, 12 August 2011;
host: Chelonia mydas. AMNH 12533 - 08013 - 277 . Female, 5.30 mm. Palmyra Atoll, 09
August 2011; host: Chelonia mydas.

Hyachelia lowryi:

AMNH 12533-11008-002. Male, 4.86 mm. Palmyra Atoll, 21 July 2011. Host: Chelonia
mydas. AMNH 12533-11008-033. Male, 5.03 mm. Palmyra Atoll, 20 July 2010; host: Che¬
lonia mydas. AMNH 12533-11008-111. Male, 5.23 mm. Palmyra Atoll, 12 August 2011;
host: Chelonia mydas. AMNH 12533-11008-034. Male, 4.96 mm. Palmyra Atoll, 20 July
2011; host: Chelonia mydas.

RESULTS

During the three-year survey (2009-2011), a total of 170 green turtles and two hawksbill
turtles were examined for epibionts. The total of both species of Hyachelia, i.e., H. tortugae and
H. lowryi combined, was 580 specimens occurring on 50 individual host turtles (table 1). Hyache¬
lia were found exclusively on green turtles; no epibionts were found on the hawksbill turtles. Both
species of Hyachelia were found cooccurring on 11 ( 6 %) of turtle hosts. Although the number of
H. tortugae and H. lowryi was similar in the first two survey years (31 and 35 individuals respec¬
tively), in 2011 the samples were dominated by the latter: H. lowryi ( 68 %, n = 352) as compared
with H. tortugae (32%, n = 163). However, these numbers reflect only those specimens for which
a positive identification could be made; a relatively large number of immatures and juveniles
could not be identified to species. The number of specimens per turtle was not evenly distributed,
ranging from a few individuals to as many as 73 H. lowryi and 29 H. tortugae from an individual
host; most turtles had far fewer occurrences of either species. Although males and females of both
species were found, ovigerous females were very rare among specimens of H. tortugae; only three
were observed. By comparison, ovigerous females of H. lowryi were very common {n = 105).

Spatial distribution of H. tortugae revealed a strong positional bias; nearly 85% of the 2011
samples of H. tortugae were collected from the anterior region of the host (positional data were
not recorded in 2009-2010). For H. lowryi, there was no obvious trend with about an even
distribution on the anterior and posterior of the host.

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TABLE 1. Hyachelia collected from green turtles at Palmyra Atoll, 2009-2011.

Year

Turtles with Hyachelia spp.

H . tortugae

H . lowryi

Total

2009

5

11

14

25

2010

10

20

21

41

2011

38

163

351

514

Total

53

194

386

580

There was a detectable association between the occurrence of H. lowryi and the presence
of the platylepadid barnacle Platylepas sp.: nearly half of all H. lowryi were collected in the
presence of this barnacle. A similar trend was not observed for H. tortugae ; less than 5% were
found cooccurring with Platylepas sp.

Taxonomic Commentary and Species Diagnosis

While superficially H. tortugae and H. lowryi appear very similar, they display important
differences in key appendages. These appendages include the maxilliped, gnathopod 1, gnatho-
pod 2, pereopod 6, and pereopod 7; pereopod 5 can also be diagnostic, but variably so. Further
description of these appendages will provide guidance for species identification. These key
differences make the question of cooccurrence on the same host individual more significant.

Hyachelia tortugae Barnard, 1967
Figures 3, 4, and 5A

Hyachelia tortugae is easily recognized based upon features of gnathopod 1 (males only)
and pereopods 6 and 7. In males, article six of gnathopod 1 is very broad. The palm is sinuous
and lined with stout robust setae. Additionally, four thick robust setae cover the posterodistal
end of the sixth article. The dactyl is strikingly short, extending to only half the length of the
palm. Gnathopod 2 (males), the palm is lined with robust setae and the proximoposterior
corner protuberant. All the above characteristics can be seen through a microscope without
dissection. However, the easiest way to recognize both males and females of this species is to
examine the morphology of the sixth article of pereopods 6 and 7 (as well as pereopod 5,
though this article is variable). If the distal margins of the sixth article of these pereopods are
transverse, the specimen can be identified as H. tortugae ; these margins are lobed and lined
with grasping robust setae. Another distinct characteristic of H. tortugae is the shape of the
uropods. The outer ramus of uropod 1 is broad and spatulate and its inner ramus is completely
bare. The inner ramus of uropod 2 lacks setae, and is distinctly lanceolate.

Hyachelia lowryi Serejo and Sittrop, 2009
Figures 5B, 6, and 7

The presence of a whiplike seta on the distal segment of the maxilliped palp (males only)
immediately distinguishes the specimen as H. lowryi (figs. 5B and 6). This whiplike seta on the
maxilliped can be seen in lateral view of the head without dissection (figs. IB and 5B). In many
of the male specimens examined the large second gnathopods were seen “reversed,” or upside

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NO. 3809

FIGURE 3. Hyachelia tortugae. AMNH 12533-11008-008, male 7.91 mm. A. Gnathopod 1 (outside lateral
view). B. Gnathopod 2 (inside lateral view).

down, reflecting an essentially prehensile condition. Males and females of H. lowryi can be identi¬
fied by their strongly oblique anterodistal margin of pereopods 6 and 7. These anterior distal
margins are covered by seven falcate, robust setae. The morphology of the uropods in H. lowryi
is consistent among males and females: both rami are lanceolate and their posterior margins are
armed with robust setae (figs. 6D and 6E). Another notable feature limited to males is the broadly
convex palm of the gnathopod 1; the anterodistal corner is weakly produced and covered with
fine scales. The dactyl length equals that of the palm. In male gnathopod 2 the palm exceeds the
length of the dactyl and the proximoposterior corner lacks robust setate.

When encountered together, adults of H. tortugae are generally much larger than H. lowryi.
For example, males of H. tortugae are typically 7-8 mm and females are approximately 6-7
mm. Males of H. lowryi are smaller at about 4.5-5.0 mm in length, while females are typically
around 4 mm. Although many of the aforementioned characteristics are useful in recognizing
both species, the strong sexual dimorphism displayed in H. tortugae and H. lowryi limit several

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FIGURE 4. Hyachelia tortugae. AMNH 12533-11008-057, male 7.98 mm. A. Pereopod 6. B. Pereopod 7. C.
Maxilliped. AMNH 12533-08013-277, female 5.30 mm. D. Uropod 1. E. Uropod 2.

of these characteristics to the males. Females of H. lowryi do not possess the whiplike seta of
the maxilliped and neither female Hyachelia species exhibit distinctive gnathopods. However,
the diagnostic characters of the pereopods are observable in all adult specimens. Furthermore,
the robust setae in the anterodistal corner of the pereopods are not fully developed in very
small juveniles of H. tortugae, and their distal margin may appear oblique.

Simplified Taxonomic Key to the Species of Hyachelia

la. Pereopods 6 and 7, anterodistal margin transverse; distal article (males) of maxilliped palp

with truncate robust setae. lowryi

lb. Pereopods 6 and 7, anterodistal margin oblique; distal article (males) of maxilliped palp

with whiplike seta. tortugae

AMERICAN MUSEUM NOVITATES

NO. 3809

DISCUSSION

Our report of both Hyachelia tortugae and H. lowryi from Palmyra Atoll represents a sig¬
nificant range extension from previously known occurrences. In particular, H. lowyri was previ¬
ously known only from the type locality of Queensland, Australia; the new records represent
a significant westerly extension of nearly 6000 kilometers. Although both species have been
reported as epibionts from primarily Pacific green turtles, it is significant that they have been
found living together on the same host individual. Given that these species have never been
found independently from a turtle host, we can presume both H. lowryi and H. tortugae are
obligate ectocommensals. Baldinger (2000) reported that the only other amphipod known
exclusively from a marine turtle host is Podocerus chelonophilus (Chevreux and de Guerne,
1888). Although Podocerus umigame Yamato, 1992, has also been reported as an obligate epi-
biont amphipod, Baldinger (2000) has suggested that P. umigame is most likely a junior syn¬
onym of P. chelonophilus ; this has been affirmed by Lazo-Wasem et al. (2011).

While the data are limited, the number of Hyachelia tortugae versus H. lowryi found in the
samples from Palmyra Atoll provides insight into the population characteristics of both these
epibionts. The number of H. lowryi specimens greatly outnumbered H. tortugae individuals
almost two to one. Additionally, only three ovigerous H. tortugae specimens were found as com¬
pared to 105 ovigerous H. lowryi. The overwhelming presence of ovigerous H. lowryi specimens
versus ovigerous H. tortugae specimens indicates that these two species apparently do not have
a contemporaneous mating/brooding period. Furthermore, positional occurrence of H. tortugae
as compared with H. lowryi points to a trend that the former reside predominantly (85% occur¬
rence) at the anterior of the turtle, implying that many came from either the crop lavages or tissue
folds surrounding the neck region. This would correlate with the original report of this species
in the buccal cavity of a green turtle (Barnard, 1967) and subsequent reports (Balazs, 1980) of
Hyachelia (as H. tortugae) from the same host species. It should be noted that another epibiont,
the platylepadid turtle barnacle Stomatolepas praegustator Pilsbry, 1910, has also been found to
inhabit the buccal cavity of marine turtles in a nonparasitic relationship.

Although spatial occurrence of Hyachelia lowryi on their host did not point to any particu¬
lar trend, more than half of the specimens collected were found in association with a platyle¬
padid barnacle, Platylepas sp. Many of these barnacles were covered in tufts of algae, and some
of these tufts had H. lowryi adhering with their prehensile pereopods even after death and
preservation. The importance of barnacles as substrate for algae-nestling invertebrates such as
amphipods has been previously discussed (Lazo-Wasem et al., 2011).

Biogeographically, the currently known distribution of Hyachelia tortugae and H. lowryi in
the Pacific Ocean is interesting. The former is previously known from the Galapagos Islands
and the Hawaii Islands; reports on the latter species from Australia and now from Palmyra
Atoll indicate a broad distribution of this genus in the Pacific. However, neither has been
reported from turtles inhabiting the Pacific waters adjacent to the western coast of Mexico or
elsewhere along the continental margin. Instead, the only obligate commensal amphipod of
marine turtles reported from these coastal waters is Podocerus chelonophilus from Mexico
(Hernandez-Vasquez and Valadez-Gonzalez, 1998; Gamez Vivaldo et al., 2006; Angulo-Lozano
et al., 2007 [incorrectly as Caprella ]; Lazo-Wasem et al., 2011).

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FIGURE 5. A. Hyachelia tortugae. AMNH 12533-10008-451, male 7.52 mm. B. H. lowryi. AMNH 12533-
11008-002, male 4.86 mm. Scale bars = 0.5 mm.

The available data suggests a distribution of Hyachelia spp. across the Pacific Ocean (Galapa¬
gos, Hawaii, Palmyra, and Australia) exclusive of western continental localities. Almost all Pacific
Ocean records of Hyachelia have been from green turtles. In fact only a single record is reported
from a different host, a loggerhead turtle ( Caretta caretta) from Australia, which harbored several
individuals of H. lowryi (Serejo and Sittrop, 2009). That the aforementioned epibiont studies have
encountered primarily olive ridley turtles (green turtle sampling being very limited) may indicate
that Hyachelia simply do not occur on olive ridleys and are essentially host-specific on green
turtles. This may be further supported by the fact that olive ridleys are not devoid of all obligate
commensal amphipods, given the routine occurrence of Podocerus chelonophilus.

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FIGURE 6. Hyachelia lowryi. AMNH 12533-11008-033, male 5.03 mm. A. Pereopod 6. B. Pereopod 7. AMNH
12533-11008-111, male 5.23 mm. C. Maxilliped. D. Uropod 1. E. Uropod 2.

Increased collecting of epibionts throughout the Pacific will undoubtedly fill in gaps of
the distribution of Hyachelia spp. relative to geography and host occurrence. Furthermore,
increased sampling may help to determine demographic and reproductive periodicity as well
as potential host specificity. For example, if Podocerus and Hyachelia are ever found to cooc¬
cur, the lack of the latter on olive ridleys may be solely a function of host, rather than a result
of geography or the presence of the former.

ACKNOWLEDGMENTS

We thank Daniel Drew (Yale Peabody Museum) for logistical help in the lab and Lourdes
Rojas (Yale Peabody Museum) for help in the field during M. Yabut’s initial fieldwork train-

2014

YABUT ET AL.: NEW RECORDS OF HYACHELIA TORTUGAE AND H. LOWRYI

11

ing; field assistance was also received
from Elizabeth Brill (Corning, NY)
and Craig Tepper (Cornell College).

The Peabody Museum Summer Intern¬
ship Program and Benjamin Silliman
Fellowship sponsored training and
fieldwork to M. Yabut. M. Yabut also
thanks Marta Wells, Yale College EEB
Faculty, for support and advising.

Fieldwork at Palmyra Atoll was con¬
ducted by the Center for Biodiversity
and Conservation (American Museum
of Natural History) and we thank the
Palmyra Sea Turtle field team for their
assistance. This research was approved
by the American Museum of Natural
History’s Institutional Animal Care
and Use Committee (IACUC), under
permits authorized by the National
Oceanic and Atmospheric Administra¬
tion (NOAA/NMFS Permit #10027) as
well as the USFWS (Special Use Permit
#12533-08013, #12533-09018, #12533-
10008, #12533-11008). The research
was supported by funds from the
National Oceanic and Atmospheric
Administration and the Regina Bauer
Frankenberg Foundation for Animal
Welfare. This is Palmyra Atoll Research
Consortium publication number
PARC-0106. Dennis Richardson
(Quinnipiac University) gave advice
on staining protocol and slide-making techniques. Oliver Coleman (Museum fur Naturkunde)
provided digital illustration techniques; subsequent help was received from Sally Pallatto and
Rosemary Volpe (Yale Peabody Museum). Adam Baldinger (Museum of Comparative Zool¬
ogy, Harvard University) helped obtain important literature.

FIGURE 7. Hyachelia lowry. AMNH 12533-11008-033, male
5.03 mm. A. Gnathopod 1 (inside lateral view). AMNH
12533-11008-034, male 4.96 mm. B. Gnathopod 2 (inside
lateral view).

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