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Cah. Biol. Mar. (2013) 54 : 531-540
The littoral sea cucumbers (Echinodermata: Holothuroidea)
of Guam re-assessed – a diversity curve that still
does not asymptote
François MICHONNEAU1, Giomar Helena BORRERO-PEREZ2, Magali HONEY3, Kamarul Rahim KAMARUDIN4,
Alexander M. KERR5, Sun KIM5, Marie Antonette MEÑEZ6, Allison MILLER5, Julio Adrián OCHOA3,
Ronald D. OLAVIDES6, Gustav PAULAY1, Yves SAMYN7, Ana SETYASTUTI8, Francisco SOLIS-MARIN3,
John STARMER1and Didier VANDENSPIEGEL9
(1) Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
E-mail: francois.michonneau@gmail.com, paulay@flmnh.ufl.edu
(2) Instituto de Investigaciones Marinas y Costeras (INVEMAR), Cerro Punta Betín, Santa Marta, 1016, Colombia
(3) Colección Nacional de Equinodermos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Aútónoma
de México, Apdo. Post. 70-305, México, D.F. 04510, México
(4) Institute of Oceanography and Maritime Studies (INOCEM), Kulliyyah of Science,
International Islamic University Malaysia
(5) Guam Marine Laboratory, University of Guam, Mangilao, Guam, USA
(6) Marine Science Institute, University of the Philippines, Diliman, Philippines
(7) Royal Belgian Institute of Natural Sciences, Vautierstraat 29, B-1000 Brussels
(8) Research Centre for Oceanography Indonesian Institute of Sciences - LIPI, Ambon, Indonesia
(9) Royal Museum for Central Africa Department of African Zoology, Tervuren, Belgium
Abstract: The Micronesian island of Guam has been an important site for the study of littoral tropical holothurian
taxonomy for almost 200 years. Despite substantial attention by both expeditions and resident taxonomists, new records are
still regularly added to the fauna, demonstrating the challenge of documenting even such large and well-known animals in
a small hyper-diverse area. Guam is the type locality of species described by Quoy & Gaimard (1833) and Brandt (1835).
A survey of the sea cucumber fauna by Rowe & Doty (1977) led to one of the most used guides for the identification of
tropical Pacific sea cucumbers because of the color illustrations of living animals it presented. Focus on echinoderms
including holothurians continued with numerous new records added in the following decades. Paulay (2003a) summarized
the fauna last, recording 46-47 species. At this stage the fauna was thought to be well documented. A week-long workshop
on holothurian systematics sponsored by the National Science Foundation PEET (Partnerships for Enhancing Expertise in
Taxonomy) project in 2010 included a substantial field work component, sampling both during the day and night, with
snorkeling and SCUBA, across a variety of habitats. This survey yielded 40 species, including numerous new records and
even species. Further sampling by Kerr’s lab since the workshop has added additional records. The littoral holothuroid
fauna of Guam now comprises 65 species in 17 genera and 7 families. Half of the 19 newly recorded species are the result
of unravelling cryptic species in complexes, the other half are based on new collections. Eleven species are known from
single specimens, suggesting that much still remains to be learned about the fauna.
532 THE LITTORAL SEA CUCUMBERS OF GUAM
Introduction
One of the great challenges of our age is to document the
biosphere as well as possible before it deteriorates further
under the impact of human activities. Recent large-scale
biodiversity surveys have demonstrated that our knowledge
of biodiversity is surprisingly limited. In many systems we
cannot even reliably estimate the order of magnitude of
species diversity, let alone describe and name the species
present or their biology (e.g., Bouchet et al., 2002;
Appeltans et al., 2012; Samyn & Declerck, 2012). The
marine realm is particularly challenging, because it is less
accessible to direct observation and has received
substantially less biological attention than terrestrial
systems. Nevertheless we are beginning to have a fairly
good knowledge at least of the diversity of larger marine
organisms, such as fishes, marine tetrapods, macroalgae,
and some groups of macroinvertebrates. Being large-
bodied, conspicuous, and charismatic, echinoderms rank
among the best-studied macroinvertebrates. The objective
of this paper is to review how much we know, how our
knowledge has increased, and consider how much remains
to be learned about the holothurian fauna of the
Micronesian island of Guam.
The holothurian fauna of Guam is among the best
documented of any tropical area as a result of a long history
of study, visits by major workers, and resident specialist
taxonomists. The first written record is by Quoy & Gaimard
(1834), who described Holothuria guamensis Quoy &
Gaimard, 1834 and noted (but did not name) that they
encountered five holothurian species on the island. Brandt
(1835) described Holothuria maculata Brandt, 1835 and
Stichopus chloronotus Brandt, 1835 from Guam soon after.
A few echinoderms were recorded from Guam early in the
20th century, after Guam passed into US hands (Fisher,
1919, Clark, 1920). Following World War II, Cloud (1959)
reported on a number of species from Guam and
neighboring Saipan. Numerous studies followed after the
establishment of the University of Guam and the Marine
Laboratory, especially in the wake of a large outbreak of
crown-of-thorns sea stars that devastated Guam’s reefs in
1967. Echinoderms in general were studied by several
faculty and students, including Masashi Yamaguchi and
Chuck Birkeland. Holothurian specialist Frank Rowe
visited Guam in the 1970’s and worked through the fauna
with graduate student Jim Doty. Their review of the island’s
sea cucumbers (Rowe & Doty, 1977) became a popular
introduction to holothurian taxonomy in the Pacific for
years because of the numerous color plates it offered. The
echinoderms of Guam were reviewed in “A working list of
marine organisms from Guam” (UOGML, 1981), and
numerous new records added subsequently by Kerr et al.
(1992). The latest published checklist for holothurians
(Paulay, 2003a), was prepared for the Micronesica volumes
“Marine biodiversity of Guam and the Marianas”,
recording 47 species (including H. scabra Jaeger, 1833,a
Résumé : les concombres de mer (Echinodermata : Holothuroidea) littoraux de Guam réévalués - Une courbe de diversité
qui n’atteint pas d’asymptote. L’île micronésienne de Guam a été un site d’étude important pour la taxonomie des
holothuries littorales tropicales pour presque 200 ans. Malgré les efforts d’expéditions et de taxonomistes résidant sur place,
des espèces sont encore recensées pour la première fois, démontrant les difficultés associées au recensement d‘une faune
comprenant des animaux pourtant de grande taille et bien connus dans une zone aussi restreinte et diverse. Guam est la
localité type d’espèces décrites par Quoy & Gaimard (1833) et Brandt (1835). Le recensement de la faune des concombres
de mer par Rowe & Doty (1977) a généré un des guides d’identification les plus utilisés pour l’Indo-Pacifique du fait des
illustrations en couleur des animaux vivants qu’il incluait. L’attention portée aux échinodermes a continué avec de
nombreuses espèces recensées pour la première fois dans les décennies qui ont suivi. Paulay (2003a) a récapitulé la liste
faunistique incluant 46-47 espèces. A ce stade, la faune était présumée être bien connue. En 2010, un groupe de travail d’une
semaine sur la taxonomie des holothuries, organisé grâce aux subsides du projet NSF PEET a permis un travail de terrain
significatif, avec des échantillonnages de jour comme de nuit, en plongée libre et en scaphandre, et ce dans de nombreux
types d’habitats. Cet effort a conduit au recensement de 40 espèces, y compris des espèces vues pour la première fois à
Guam, et des espèces nouvelles. Des échantillonnages supplémentaires supervisés par Kerr depuis cet atelier ont encore
complété la liste d’espèces recensées. La faune des holothuries littorales de Guam comprend maintenant 65 espèces
réparties dans 17 genres et 7 familles. La moitié des 19 espèces recensées pour la première fois sont le résultat de la
découverte de complexes d’espèces, l’autre moitié est basée sur de nouvelles récoltes. Onze des espèces recensées ne sont
connues que d’un exemplaire indiquant que beaucoup reste à apprendre de cette faune.
Keywords: Holothuroids lBiodiversity lMicronesia lEchinoderms
F. MICHONNEAU, G.H. BORRERO-PEREZ, M. HONEY, K.R. KAMARUDIN, A.M. KERR, S. KIM et al. 533
doubtful record (see Paulay, 2003a), and here no longer
considered) with 10 new records. Gustav Paulay was on the
faculty of the University of Guam Marine Lab through the
1990’s, while Alex Kerr was a graduate student during part
of that time, and returned as faculty in 2005.
In June 2010, a week-long workshop on holothurian
systematics sponsored by the NSF PEET holothurian
project (Paulay & Kerr, PIs) included a substantial field
work component, sampling with snorkeling and SCUBA,
during the day and at night, across a variety of habitats, and
led to the collection of 40 species. Integrative taxonomic
studies also resolved a number of species complexes and
thus improved our knowledge of the taxonomy of several
species on Guam. Here we review how these efforts have
changed our understanding of this fauna.
Materials & Methods
We used Paulay (2003a) as the starting point of this survey,
as it critically reviewed the holothurians of Guam known to
that date. Field work since then included collections by
Kerr’s lab at the University of Guam Marine Laboratory, as
well as other local naturalists, who brought specimens to
Kerr’s lab, and collections by Paulay during a visit in 2003
and by Michonneau during a visit in 2008. In 2010 all of us
collected sea cucumbers during a two-week workshop.
Collections were by snorkel and SCUBA across all types of
reef habitats represented on the island, and included
searching in the reef matrix (mostly under rocks) and at
night. Two species were collected in 2010 by technical
diver Jim Pinson, on the deep reef slope below SCUBA-
accessible depths (> 60 m). A set of voucher specimens
were deposited in the Florida Museum of Natural History,
University of Florida (UF), with sets of duplicates in the
collections of the “Colección Nacional de Equinodermos,
Instituto de Ciencias del Mar y Limnología Universidad
Nacional Aútónoma de México” in Mexico City, Mexico,
and the Royal Belgian Institute of Natural Sciences in
Brussels, Belgium. Some specimens from previous
collections have been deposited at the US National
Museum of Natural History (USNM).
Revisionary efforts, particularly of members of the
Holothuriidae have also clarified species limits and
diversity in a number of clades since 2003. Thus
morphological revision of Labidodemas (Massin et al.,
2004) increased the recognized species of that group from
4 to 8. Studies of animals in the field (color patterns,
behavior, ecology, etc) and DNA sequence data have
allowed us to better understand species limits in a number
of complexes, including Actinopyga, Bohadschia (Kim et
al., 2013), Holothuria, and Euapta. We provide a brief sum-
mary of some of these results as they pertain to the species
diversity on Guam.
Results
Approximately 65 species of sea cucumbers are now
recorded from Guam (Table 1). New records and
nomenclatural updates are presented in systematic order
below.
Order Apodida
Family Synaptidae
Euapta tahitiensis Cherbonnier, 1955
UF 10327: Guam, Tanguisson, powerplant inflow channel,
0-5 m, 11.VI.2010, Fig. 1A.
A single Euapta species, E. godeffroyi , has been
generally recognized across the Indo-West Pacific,
although two other species have been proposed: E. magna
Heding, 1928 and E. tahitiensis. Our work indicates that E.
tahitiensis is valid; the status of E. magna remains to be
evaluated. Euapta tahitiensis is widespread in the Pacific
and is here recorded from Guam for the first time.
Examination of previous Euapta collections from Guam
revealed that the species was also collected, but not
recognized in the past.
Order Aspidochirotida
Family Stichopodidae
Stichopus herrmanni Semper, 1868
UF 1683: Guam, Apra Harbor: SW end of Glass
Breakwater, sand slope, 18 m. 10.VII.2003.
Definitively recorded from Guam based on the single
specimen above. Stichopus herrmanni is one of the largest
and most conspicuous stichopodids on reefs, thus lack of
other records suggests that the sole individual collected was
a vagrant. Stichopus herrmanni was in the past confused
with other species of the S. variegatus complex (see
below).
Stichopus sp. 1
= Stichopus ?monotuberculatus, Paulay 2003a, non Quoy
& Gaimard 1834.
Two other specimens of the Stichopus variegatus
complex have been recorded from Guam, one collected
early in the 1900’s (USNM E24500) with no indication as
to provenance other than “Guam” and not readily
identifiable to species within the complex. The second
specimen was collected and released ca. 1990, but observed
by Kerr. It was the color morph illustrated by Chao &
Chang (1989: plate I) as S. variegatus, not S. herrmanni.
These were tentatively identified by Paulay (2003a) as S.
monotuberculatus, a species since found to be restricted to
the Indian Ocean (Starmer & Paulay, unpublished; Conand
534 THE LITTORAL SEA CUCUMBERS OF GUAM
Table 1. Records of holothurians on Guam. Liste des holothuries recensées à Guam. Q&G: Quoy & Gaimard (1834); R&D: Rowe &
Doty (1977), Kerr: Kerr et al. (1992 & 1993).
Species Q&G Brandt R&D Kerr Paulay This
1834 1835 1977 1992-3 2003a study
Apodida: Synaptidae
Euapta godeffroyi (Semper, 1868) 1111
Euapta tahitiensis Cherbonnier, 1955 1
Opheodesoma grisea (Semper, 1868) 1111
Patinapta sp. 1 11
Polyplectana sp. 2 1111
Polyplectana galatheae Heding, 1928 11
Synapta maculata (Chamisso & Eysenhardt, 1821) 1111
Synaptula sp. 1 11
Apodida: Chiridotidae
Chiridota hawaiiensis Fisher, 1907 1111
Chiridota violacea Müller, 1850 11
Aspidochirotida: Stichopodidae
Stichopus chloronotus Brandt, 1835 11 111
Stichopus herrmanni Semper, 1868 1
Stichopus sp. 1 111
Stichopus horrens Selenka, 1867 1111
Stichopus noctivagus Cherbonnier, 1980 111
Thelenota ananas (Jaeger, 1833) 1111
Thelenota anax H. L. Clark, 1921 1111
Thelenota rubralineata Massin & Lane, 1991 11
Aspidochirotida: Holothuriidae
Actinopyga echinites (Jaeger, 1833) 1111
Actinopyga varians (Selenka, 1867) 111 111
Actinopyga sp. 1 1
Actinopyga palauensis Panning, 1944 111
Bohadschia argus Jaeger, 1833 1111
Bohadschia marmorata Jaeger, 1833 1111
Bohadschia koellikeri (Semper, 1868) 1
Bohadschia vitiensis (Semper, 1868) 1
Bohadschia ocellata Jaeger, 1833 1
Holothuria (Thymiosycia) arenicola Semper, 1868 1111
Holothuria (Halodeima) atra Jaeger, 1833 1111
Holothuria (Semperothuria) cinerascens (Brandt, 1835) 1111
Holothuria (Mertensiothuria) coronopertusa Cherbonnier, 1980 1
Holothuria (Platyperona) difficilis Semper, 1868 1111
Holothuria (Stauropora) discrepans Semper, 1868 1
Holothuria (Halodeima) edulis Lesson, 1830 1111
Holothuria (Halodeima) aff. edulis Lesson, 1830 1
Holothuria (Platyperona) excellens (Ludwig, 1875) 111
Holothuria (Semperothuria) flavomaculata Semper, 1868 111
Holothuria (Stauropora) fuscocinerea Jaeger, 1833 111
Holothuria (Microthele) fuscopunctata Jaeger, 1833 1111
Holothuria (Lessonothuria) hawaiiensis Fisher, 1907 11
Holothuria (Thymiosycia) hilla Lesson, 1830 1111
Holothuria (Thymiosycia) impatiens ESU1 (Forsskål, 1775) 1111
Holothuria (Thymiosycia) impatiens ESU2 (Forsskål, 1775) 1
Holothuria (Thymiosycia) impatiens ESU4 (Forsskål, 1775) 1
Holothuria (Cystipus) inhabilis Selenka, 1867 1111
Holothuria (Mertensiothuria) leucospilota Brandt, 1867 1111
Holothuria (Lessonothuria) lineata Ludwig, 1875 1111
Holothuria (Microthele) fuscogilva Cherbonnier, 1980 1111
Holothuria (Stauropora) olivacea Ludwig, 1888 1
Holothuria (Lessonothuria) pardalis Selenka, 1867 1
Holothuria (Stauropora) pervicax Selenka, 1867 1111
Holothuria (Cystipus) rigida (Selenka, 1867) 1
et al., 2010). Thus at least two species of the S. variegatus
complex have now been recorded from Guam.
Order Aspidochirotida
Family Holothuriidae
Actinopyga sp. 1
UF 237: Guam, Anae Islet, NS side, in sand patch, 5-7 m.
14.X.1994.
Study of specimens of black Actinopyga taken on Guam
revealed that a second species is present in addition to A.
palauensis (= A. obesa, in Kerr et al., 1992). Ossicles of this
species somewhat resemble those of A. spinea, but it differs
from that as well as other species studied to date in its COI
sequence. This species also occurs in the Philippines.
Actinopyga varians (Selenka, 1867)
= Actinopyga mauritiana, Rowe & Doty, 1977; Paulay,
2003a; non Quoy & Gaimard, 1834.
Netchy & Paulay (in prep) separate the Pacific form of the
widespread Actinopyga mauritiana species complex as A.
varians.
Bohadschia marmorata Jaeger, 1833, species complex
Bohadschia marmorata Jaeger, 1833
UF 4748: Guam, Piti Bombholes, in and near inshore
seagrass bed 1 m. 28.VI.2003.
Bohadschia vitiensis (Semper, 1868)
UF 4701: Guam, Piti Bombholes lagoon on sand, out in day
5-7 m. 20.VII.2003.
Bohadschia koellikeri (Semper, 1868)
UF 4705: Guam, Piti Bombholes moat, 0-2 m. 19.VII.2003.
Bohadschia ocellata Jaeger, 1833
UF 7143: Guam, Tumon sand flat, 1-1.5 m. IV.2008.
Bohadschia is one of the most challenging genera
among holothurians for species delineation, as the group
has very simple ossicles, with substantial intraspecific
variation and limited interspecific differentiation both in
ossicles as well as in color pattern (Kim et al., 2013). Rowe
& Doty (1977) showed the great variability of their color
patterns and considered all forms on Guam, other than the
distinctive B. argus, to represent a single species, B.
marmorata. Paulay (2003a) noted at least two distinguish-
able species in this complex but did not separate them;
these two forms were then distinguished with mtDNA
sequences by Clouse et al. (2005). Subsequent work
focusing on color patterns and mtDNA sequences
demonstrate that four species are involved, and all four
occur on Guam (Kim et al., 2013).
Holothuria (Cystipus) inhabilis Selenka, 1867
= Holothuria (Cystipus) rigida Rowe & Doty, 1977;
Paulay, 2003a, non Selenka, 1867.
Holothuria rigida is confused in much of the literature
with H. inhabilis. Previous records of H. rigida from Guam
all appear to pertain to H. inhabilis.
Holothuria (Cystipus) rigida (Selenka, 1867)
UF 12507: Guam: Ylig Bay (“Turtle Cove”), inner reef flat,
1 m, under coralline rubble. 24.IV.2012, Fig. 1J.
While H. inhabilis is fairly common on Guam, H. rigida
proper has not been recorded until recently and is known
from the single specimen cited above.
Holothuria (Halodeima) aff. edulis Lesson, 1830
UF 11292: Guam, Tumon Bay, deep reef slope, 100 m. 2011.
This gray colored, reef-dwelling variant of H. edulis is
suspected to be a distinct species, and is known
sporadically across the Pacific (O’Loughlin et al., 2007). A
single specimen was collected in deep water by technical
diver Jim Pinson on Guam recently. Jim saw several
F. MICHONNEAU, G.H. BORRERO-PEREZ, M. HONEY, K.R. KAMARUDIN, A.M. KERR, S. KIM et al. 535
Holothuria (Metriatyla) scabra Jaeger, 1833 10
Holothuria (Halodeima) signata Ludwig, 1875 11
Holothuria (Lessonothuria) verrucosa Selenka, 1867 11
Holothuria (Theelothuria) turriscelsa Cherbonnier, 1980 111
Holothuria (Microthele) whitmaei Bell, 1887 1111
Holothuria (“Thymiosycia”) n. sp. 1
Labidodemas semperianum Selenka, 1867 1111
Labidodemas pseudosemperianum Massin, Samyn & Thandar, 2004 1
Labidodemas pertinax (Ludwig, 1875) 1
Labidodemas rugosum (Ludwig, 1875) 1
Pearsonothuria graeffei (Semper, 1868) 1111
Dendrochirotida: Cucumariidae
Thyone okeni Bell, 1884 1111
Dendrochirotida: Phyllophoridae
Phyrella n. sp. 1
Dendrochirotida: Sclerodactylidae
Afrocucumis africana (Semper, 1868) 1111
536 THE LITTORAL SEA CUCUMBERS OF GUAM
animals at this location, but has otherwise not seen the
species elsewhere in deep water on Guam.
Holothuria (Lessonothuria) verrucosa Selenka, 1867
= Holothuria (Lessonothuria) sp. 1 in Paulay, 2003a.
This species, first recorded by Paulay (2003a), has now
been identified as H. verrucosa.
Holothuria (Mertensiothuria) coronopertusa
Cherbonnier, 1980
UF 11543: Guam, on coralline sand, 100 m. 22.XI.2010,
Fig. 1I.
This striking holothurian described from New Caledonia
has turned up in recent years across much of the Indo-West
Pacific in deep water. A single specimen was collected on
Guam, 100 m deep, by technical diver Jim Pinson.
Holothuria (Microthele) fuscogilva Cherbonnier, 1980
= H. (Microthele) nobilis Paulay, 2003a; non Selenka,
1867.
See Paulay (2003a) for discussion of the history of
identification in this complex on Guam. Uthicke et al.
(2004) have reassessed the group based on broad sampling
and sequence data and showed that the appropriate name
for the dark and light mottled Pacific form is H. fuscogilva.
Holothuria (Stauropora) discrepans Semper, 1868
UF 10319: Guam, Double Reef, deep under rock, 1-2 m.
11.VI.2010, Fig. 1D.
This rather inconspicuous and relatively small Stauropora
is easy to overlook and uncommon, but appears to be rather
widespread in the western and central Pacific. A single
specimen was collected on Guam in 2010.
Holothuria (Stauropora) olivacea Ludwig, 1888
UF 10760: Guam, Apra Harbor, Kilo Wharf wharf wall and
lagoon slope, 0-15 m. 23.VI.2010, Fig. 1B.
Another inconspicuous and small Stauropora, known
from many locations, but not previously recorded from
Guam.
Holothuria (Thymiosycia) impatiens (Forsskål, 1775),
species complex
Holothuria (Thymiosycia) impatiens ESU1
UF 10341: Guam, Apra Harbor, Glass Breakwater, near
sunken barges, 1-15 m. 15.VI.2010, Fig. 1F.
Holothuria (Thymiosycia) impatiens ESU2
UF 6729: Guam, Hagatna, S of Adalupe Island. 0-1 m.
6.II.2008, Fig. 1E.
Holothuria (Thymiosycia) impatiens ESU4
UF 4709: Guam, Pago Bay reef flat to crest channel, under
rocks 0-2 m. 2003.
Michonneau’s dissertation research is demonstrating that
H. impatiens is a large species complex that includes at
least 12 ESUs (Evolutionarily Significant Units, or phylo-
genetic species, see Malay & Paulay, 2010 for definition),
species which can be differentiated based on subtle
morphological and clear genetic characters. Three of these
have now been recorded from Guam.
Holothuria (“Thymiosycia”) sp. nov.
UF 10317: Guam, Tanguisson outer reef slope under rock
on sand 22-25 m. 11.VI.2010, Fig. 1G.
A single specimen of a distinctive, fairly large
Holothuria, with Thymiosycia-type ossicles was collected
in 2010, and appears to represent an undescribed species.
Phylogenetic analysis of DNA sequences indicates the
species is not related to other Thymiosycia, and represents
a deeply divergent lineage.
Labidodemas pseudosemperianum Massin, Samyn &
Thandar, 2004
Labidodemas was not studied in detail on Guam in the past.
Massin et al. (2004) revised the genus, doubling the number
of species known, and recorded L. pseudosemperianum
from Guam based on a specimen (USNM E 53083)
collected in Tumon Bay by Kerr.
Labidodemas pertinax (Ludwig, 1875)
UF 10329: Guam, Tepungan Channel tunnel, under road, 0-
2 m. 12.VI.2010, Fig. 1H.
In 2010, we encountered two species of Labidodemas on
F. MICHONNEAU, G.H. BORRERO-PEREZ, M. HONEY, K.R. KAMARUDIN, A.M. KERR, S. KIM et al. 537
Figure 1. Live photographs of newly recorded species. Photographies d’espèces recensées pour la première fois. A. Euapta tahitien-
sis (UF 10327). B. H. olivacea (UF 10760). C. Phyrella sp. nov. (UF 10336). D. H. discrepans (UF 10319). E. H. impatiens ESU2
(UF 6729). F. H. impatiens ESU1 (UF 10341). G. Holothuria sp. nov. (UF 10317). H. Labidodemas pertinax (UF 10329). I. Holothuria
coronopertusa (UF 11543). J. H. rigida (UF 12507).
Guam, both fairly common, L. semperianum and L.
pertinax. The latter represents a new record.
Labidodemas rugosum (Ludwig, 1875)
UF 6721: Guam, Hagatna, S. of Adalupe Island, 0-1 m.
9.II.2008.
This species known from a single individual is otherwise
widespread in the Indo-West Pacific. It can be
differentiated from other Labidodemas by its uniform gray-
pinkish body wall, the cream colored tentacles, and a
yellow circle around the suckers of the ventral tube feet. It
represents a new record and fourth Labidodemas species in
Guam’s fauna.
Order Dendrochirotida
Family Phyllophoridae
Phyrella sp. nov.
UF 10336: Guam, Gun Beach, N end of Tumon Bay reef
flat and reef front, 0-2 m. 12.VI.2010, Fig. 1C.
Since 2003, three specimens of an undescribed Phyrella
have been collected on Guam (Michonneau & Paulay, in
press). The species is densely covered with podia and has
relatively few ossicles. Only two dendrochirotids have been
recorded from Guam previously, the common sclero-
dactylid Afrocucumis africana, and Thyone okeni,
(considered a synonym of Thyone venusta Selenka, 1868
by Thandar (1990)) recorded by Rowe & Doty (1977)
based on a small specimen (described as 5 mm long in the
text, and 2 cm long in the plate legend). The latter species
was not described, the illustration presented of the live
animal is of too limited resolution to evaluate. The
specimen has now been located at the Australian Museum
(AM J.9328), but not yet reexamined. It is possible that this
specimen represents a juvenile of the Phyrella species here
recorded. Thyone okeni is noted to lack ossicles (Bell,
1884), but the presence/absence of ossicles is not discussed
for the Guam specimen. Ossicles are often uncommon in
juvenile species of Phyrella. Thyone okeni is presumed to
have 10 tentacles like other members of the genus, while
Phyrella n. sp. has 17-18, but likely several are added
during ontogeny.
Discussion
The 65 species of sea cucumbers recorded from Guam
represent a greater diversity than known from almost any
other comparable-sized area (541 km2). It is comparable to
the recorded fauna of the Spermonde archipelago in
Indonesia (56 species: Massin, 1999) near the global center
of marine diversity (Hoeksema, 2007; Renema et al., 2008).
The high richness reflects both the proximity of Guam to
the diversity center and the intense scrutiny the fauna has
received over the years by both resident and visiting
holothurian specialists.
The large increase in recorded diversity (from 46 to 65
species) in the past decade is remarkable, given the long
history of research on holothurians in Guam, and the fact
that sea cucumbers are among the largest and most
conspicuous mobile invertebrates on reefs. The diversity vs.
time curve on Guam shows no sign of reaching an
asymptote (Fig. 2). This trend underscores how little we
know about marine diversity (e.g., Bouchet et al., 2002;
Paulay, 2003b). Three species appear to be undescribed,
while another four remain unidentified.
Half of the new records (8 of 19) are genuinely new,
meaning they were not encountered and recorded
previously. Remarkably, 7 of these, together with 4-5 others
(previously recorded or part of species complexes) are
known from single specimens on Guam (Synaptula sp. 1,
Stichopus herrmanni, Thelenota rubralineata, Holothuria
coronopertusa, H. discrepans, H. aff. edulis, H. olivacea,
H. rigida, Holothuria n. sp., Labidodemas pseudo -
semperianum, L. rugosum, and possibly “Thyone okeni”).
Three of these species represented by singletons are known
only from deep water on Guam (T. rubralineata, H.
538 THE LITTORAL SEA CUCUMBERS OF GUAM
Figure 2. Increase of known diversity of holothurians on
Guam over time. Augmentation au cours du temps de la diversité
connue des holothuries de Guam.
coronopertusa, H. aff. edulis), and their rarity likely reflects
the difficulty of accessing this habitat. Six are parts of
species complexes or are fairly non-descript, and may have
been missed by less focused past surveys (Euapta
tahitiensis, H. discrepans, H. olivacea, H. pardalis, H.
rigida, Labidodemas pseudosemperianum). Two are minute
and cryptic (Synaptula sp. 1, “Thyone okeni”). Increased
sampling efforts, in particular below SCUBA-accessible
depths, will likely lead to additional records.
The other half of new records emerged from
differentiation of species complexes. Molecular and
morphological examination of fresh material and
collaborative integrative revisions of the reef-associated
holothurians pursued partly through the NSF PEET
holothurian project has revealed high levels of cryptic
diversity in several species complexes. About one third
(~ 15 of 46) of the species recorded from Guam in the past
are now known to be species complexes. Many of these
complexes include or are comprised of a geographic mosaic
of allopatric species, of which only a single species is
known to occur on Guam. For these, revisions have
changed or may change the name of the Guam form.
However five of the species include multiple sympatric
cryptic species not previously differentiated on Guam,
adding substantially to the diversity of the fauna: Euapta
godeffroyi, Bohadschia marmorata, Holothuria edulis, H.
impatiens, and Labidodemas semperianum. Integrative
taxonomic studies have revealed species lost in synonymies
(e.g., 4 species in the Bohadschia marmorata complex), not
recognized since their description (e.g., distinction of
Euapta tahitiensis and E. godeffroyi), and species that were
missed because characters traditionally used in species
delimitation do not vary among related forms (e.g., the
three species in the H. impatiens complex).
The fauna is dominated by the Holothuriidae (44
species: 70%), followed by the Synaptidae and the
Stichopodidae (both 8 species: 13%); two species of
Chiridotidae, and one each of Cucumariidae,
Sclerodactylidae, and Phyllophoridae, round out the fauna
(Fig. 3). The dominance of aspidochirotids (81%) and poor
representation of dendrochirotids (5%) is typical of oligo -
trophic environments such as oceanic islands in the tropics.
Similarly dendrochirotids comprise 5% (2 of 37 species) of
the holothurians of the oceanic island La Réunion (Conand
et al., 2010) and 2.1% of the fauna off the oligotrophic
coast of Kenya (Samyn, 2003; Samyn & Tallon, 2005),
while they represent 34% (42 of 122 species) of the fauna
on Madagascar (Cherbonnier, 1988), a neighboring
microcontinent. Oligotrophic waters and isolation likely
both contribute to the underrepresentation of this
suspension feeding group with lecithotrophic development.
Acknowledgements
We thank the staff of the University of Guam Marine
Laboratory for hosting and helping with the workshop that
produced this study. Funding by NSF PEET (DEB
0529724) is gratefully acknowledged. The authors would
like to thank Chantal Conand and Claude Massin for
constructive remarks that improved this manuscript.
References
Appeltans W. et al. 2012. The magnitude of global marine
species diversity. Current Biology, 22: 2189-2202.
Bell F.J. 1884. Report on the Zoological Collections made in the
Indo-Pacific Ocean during the Voyage of H.M.S. Albert, 1881-
2. pp. 117-177 & 509-512.
Bouchet P., Lozouet P., Maestrati P. & Heros V. 2002.
Assessing the magnitude of species richness in tropical marine
environments: exceptionally high numbers of molluscs at a
New Caledonia site. Biological Journal of the Linnean Society,
75: 421-436.
Brandt J.F. 1835. Echinodermata ordo Holothurina. In:
Prodromus Descriptionis Animalium Ab H. Mertensio in Orbis
Terrarum Circumnavigatione Observatorum. Fasc. I, pp. 42-
62. Petropoli.
Chao S.M. & Chang K.H. 1989. The shallow-water holothurians
(Echinodermata: Holothurioidea) of southern Taiwan. Bulletin
of the Institute of Zoology Academia Sinica (Taipei), 28: 107-
137.
Cherbonnier G. 1988. Echinodermes: Holothurides. Faune de
Madagascar, 70: 1-292.
F. MICHONNEAU, G.H. BORRERO-PEREZ, M. HONEY, K.R. KAMARUDIN, A.M. KERR, S. KIM et al. 539
Figure 3.Species richness for each sea cucumber family
represented in Guam.
Clark H.L. 1920. Tropical Pacific Holothurioidea. In: Reports on
the scientific results of the expedition to the eastern tropical
Pacific, in charge of Alexander Agassiz, by the US. Fish.
Commission Steamer ALBATROSS, October 1904-March
1905, Lieut. Commander LM. Garret, USN, commanding.
XXXIII. Memoirs Museum of Comparative Zoology, Harvard,
39: 121-154
Cloud P.E. Jr. 1959. Geology of Saipan Mariana Islands Part 4.
Submarine topography and shoal-water ecology. Geological
Survey Professional Paper, 280-K.
Clouse R., Janies D. & Kerr A.M. 2005. Resurrection of
Bohadschia bivittata from B. marmorata (Holothuroidea:
Holothuriidae) based on behavioral, morphological, and
mitochondrial DNA evidence. Zoology, 108: 27-39.
Conand C., Michonneau F., Paulay G. & Bruggemann H.
2010. Diversity of the holothurian fauna (Echinodermata) in
La Réunion (Western Indian Ocean). The Western Indian
Ocean Journal of Marine Science, 9: 145-151.
Fisher W.K. 1919. Starfishes of the Philippine Sea and adjacent
waters. Bulletin of the U. S. National Museum, 100: 1-711.
Hoeksema B. 2007. Delineation of the Indo-Malayan Centre of
maximum marine biodiversity: the Coral Triangle. In:
Biogeography, Time, and Place: Distributions, Barriers, and
Islands (W. Renema ed), pp. 117-178. Springer: Netherlands.
Kerr A.M., Norris D.R., Schupp P.J., Meyer K.D., Pitlik T.J.,
Hopper D.R., Chamberlain J.D. & Meyer L.S. 1992. Range
extensions of echinoderms (Asteroidea, Echinoidea and
Holothuroidea) to Guam, Mariana Islands. Micronesica, 25:
201-216.
Kerr A.M., Stoffel E.M. & Yoon R.L. 1993. Abundance
distribution of holothuroids (Echinodermata: Holothuroidea)
on a windward and leeward fringing coral reef, Guam, Mariana
Islands. Bulletin of Marine Science, 52: 780-791.
Kim S.W., Kerr A.M. & Paulay G. 2013. Coloyr, confusion, and
crossing: resolution of species problems in Bohadschia
(Echinodermata: Holothuroidea). Zoological Journal of the
Linnean Society, 168: 81-97.
Malay M.C. & Paulay G. 2010. Peripatric speciation drives
diversification and distributional pattern of reef hermit crabs
(Decapoda: Diogenidae: Calcinus). Evolution, 64: 634-662.
Massin C. 1999. Reef-dwelling Holothuroidea (Echinodermata)
of the Spermonde Archipelago (south-west Sulawesi,
Indonesia). Zoologische Verhandelingen (Leiden), 329: 1-144.
Massin C., Samyn Y. & Thandar A.S. 2004. The genus
Labidodemas (Holothuroidea: Aspidochirotida) revisited, with
description of three new species and with re-positioning of
Holothuria (Irenothuria) maccullochi Deichmann, 1958.
Journal of Natural History, 38: 1811-1847.
Michonneau F. & Paulay G. Revision of the genus Phyrella
(Holothuroidea: Dendrochirotida) with the description of a
new species from Guam. Zootaxa. in press.
O’Loughlin P.M., Paulay G., VandenSpiegel D. & Samyn Y.
2007. New Holothuria species from Australia (Echinodermata:
Holothuroidea: Holothuriidae), with comments on the origin of
deep and cool holothuriids. Memoirs of Museum Victoria, 64:
35-52.
Paulay G. 2003a. The Asteroidea, Echinoidea, and Holothuroidea
(Echinodermata) of the Mariana Islands. Micronesica,35-36:
563-583.
Paulay G. 2003b. Marine biodiversity of Guam and the Marianas:
overview. Micronesica,35-36: 3-25.
Quoy J.R.C. & Gaimard J.P. 1833 [1834]. Holothuries. In:
Voyage de la Corvette L’astrolabe. Exécuté par Ordre du Roi
Pendant les Années 1826-1829 sous le Commandement de M.
J. Dumont D’Urville - Zoologie: Zoophytes, pp. 108-133. J.
Tastu: Paris.
Renema W., Bellwood D.R., Braga J.C., Bromfield K., Hall R.
et al. 2008. Hopping hotspots: global shifts in marine bio -
diversity. Science, 321: 654-657.
Rowe F.W.E. & Doty J.E. 1977. The shallow water holothurians
of Guam. Micronesica, 13: 217-250.
Samyn Y. 2003. Shallow-water Holothuroidea (Echinodermata)
from Kenya and Pemba Island, Tanzania. Studies in
Afrotropical Zoology, 292: 1-158.
Samyn Y. & Talon I. 2005. Zoogeography of the shallow-water
holothuroids of the western Indian Ocean. Journal of
Biogeography, 32:1523-1558.
Samyn Y. & De Clerck O. 2012. No name, no game. European
Journal of Taxonomy, 10: 1-3.
Selenka E. 1867. Beitrage zur Anatomie und Systematik der
Holothurien. Der Philosophischen Facultat zu Gottingen in
December 1866, als Dissertation vorgelegt.: pp. 291-374.
Thandar A.S. 1990. The phyllophorid holothurians of southern
Africa with the erection of a new genus. South African Journal
of Zoology, 25: 207-223.
UOGML (University of Guam Marine Laboratory) 1981. A
working list of marine organisms from Guam. Preliminary
checklist of echinoderms from Guam. University of Guam
Marine Laboratory, Technical Report, 70: 54-58.
Uthicke S., O’Hara T.D. & Byrne M. 2004. Species composition
and molecular phylogeny of the Indo-Pacific teatfish
(Echinodermata : Holothuroidea) bêche-de-mer fishery.
Marine and Freshwater Research, 55: 837-848.
540 THE LITTORAL SEA CUCUMBERS OF GUAM