New contributions to the heterobranch sea slug biodiversity of Bocas del Toro, Panama

Abstract

A survey of heterobranch sea slug diversity in the Bocas del Toro Archipelago documented a total of 20 species of Anaspi-dea, Cephalaspidea, Nudibranchia, and Pleurobranchomorpha during an 81-hour search effort. This includes four new records for Bocas del Toro in addition to a potentially undescribed species and an unidentified species. Both direct and indirect collecting methods were used. Species were identified and photographed in the lab, and most are illustrated herein. The present paper constitutes the most updated study of sea slug diversity in the Bocas del Toro Archipelago.

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THE NAUTILUS 138(3–4):75–81, 2024 Page 75
New contributions to the heterobranch sea slug biodiversity
of Bocas del Toro, Panama
Jaime L. Neill, Maggie M. Dillon, Cassie Bilecki, Samantha Bollinger, Sandra C. Dansereau,
Abigail Flores, Kathrina B. Go Garcia, Rianna A. Hernandez-Thorn, Matthew Kim, Priscilla V. Martinez,
Casey B. Pua, Daniel F. Ramirez, Daniel Sebastian, Jordyn A. Scott, Betty Wong, Abby A. Yuen,
Jeremy T. Claisse, Ángel Valdés1
Department of Biological Sciences,
California State Polytechnic University Pomona
Pomona, California 91867, USA
ABSTRACT
A survey of heterobranch sea slug diversity in the Bocas del
Toro Archipelago documented a total of 20 species of Anaspi-
dea, Cephalaspidea, Nudibranchia, and Pleurobranchomorpha
during an 81-hour search effort. This includes four new records
for Bocas del Toro in addition to a potentially undescribed spe-
cies and an unidentied species. Both direct and indirect
collecting methods were used. Species were identied and
photographed in the lab, and most are illustrated herein. The
present paper constitutes the most updated study of sea slug
diversity in the Bocas del Toro Archipelago.
INTRODUCTION
The Bocas del Toro Archipelago is located off the Carib-
bean coast of Panama and comprises several islands near
the border with Costa Rica. The archipelago includes
various marine ecosystems such as mangroves, seagrass,
and coral reefs (Collin etal., 2005). A comprehensive sur-
vey in 2015 resulted in the publication of an identication
guide (Goodheart etal., 2016), which expanded the num-
ber of recorded species from 19 to 82, representing the
most complete study of this area to date. However, almost
ten years have passed since the publication of that study,
with no further research on the sea slugs within Bocas del
Toro, and the progress in taxonomic research on sea slugs
elsewhere has rendered it out of date.
During April 2024, 16 California State Polytechnic
University, Pomona students and two faculty participated
in a eld ecology trip to Bocas del Toro at the Institute for
Tropical Ecology and Conservation (ITEC) located on
Isla Colón. The expedition’s main objective was to pro-
vide students with eld experiences conducting research
in shallow tropical marine systems by carrying out several
pilot studies. These included a reassessment of the sea
slug biodiversity in the ecoregion. In this paper, we pres-
ent the results of this study, with the most updated record
of sea slug diversity in the Bocas del Toro Archipelago.
The goal of the present study is to follow up on the previ-
ous survey by Goodheart etal. (2016), adding new records
and comparing the results of the collecting efforts.
MATERIALS AND METHODS
Sea slug surveys were conducted from March 31st to
April 2nd and April 6th to April 8th, 2024, in the Bocas
del Toro Archipelago, Panama, as part of the Tropical
Marine Ecology Panama course at California State Poly-
technic University (CPP), Pomona (BIO 4550/L). Sur-
veys were conducted along the west side of Bocas del
Toro in ve localities numbered as follows: Soropta Pen-
insula (1), Bocas del Drago (2), Pete’s Reef (3), Punta
Caracol (4), and Casa Blanca (5) (Figure 1). Direct sur-
vey methods were based on snorkeling, exclusively during
the daytime, while indirect methods consisted of sub-
strate collections (primarily the algae Caulerpa spp. and
Halimeda spp.) that were thoroughly sifted through later
in the day at ITEC facilities. Substrate materials were
separated into trays with seawater and left to rest over-
night to allow for further specimen collection. A Nikon
D850 camera was used to photograph live specimens on
black fabric. Individual sea slugs were released at their
respective collection locality the following day.
Collection and documentation were carried out by a
total of 18 observers with various levels of sea slug survey
experience (minimum and maximum number of observ-
ers at any given time was 1 and 17 respectively). Search
effort was measured by search time and number of
observers in each location with the total time calculated
as the sum of search time by all observers in each survey.
The substrate amount was not measured, and species
abundance represents an estimation of individuals found
using both direct and indirect methods.
Specimens were identied to the lowest possible taxon
primarily using the eld guide by Valdés etal. (2006) and
1 Corresponding author: aavaldes@cpp.edu

Page 76 THE NAUTILUS Vol. 138, No. 3–4
the papers by Collin etal. (2005) and Goodheart etal.
(2016) as well as taxonomically specialized literature for
nomenclatural and taxonomic updates (e.g., Bazzicalupo
et al., 2020; Camacho-García and Gosliner, 2008; Car-
mona etal. 2014; Ghanimi etal., 2020; Goodheart etal.,
2015; Krug etal., 2016; Padula etal., 2016; Turani etal.,
2024; Zamora-Silva and Malaquias, 2018). The species
documented were organized into ve different clades
(orders): Anaspidea, Cephalaspidea, Nudibranchia, Pleu-
robranchomorpha, and Sacoglossa.
RESULTS
After approximately 81 person-hours of eld searching,
20 species belonging to ve clades of heterobranch sea
slugs were documented (Tables 1, 3). Sacoglossa was rep-
resented by the highest number of specimens (n = 61,
~60% of total) and was present in three of the ve locali-
ties, followed by Nudibranchia (n = 21, ~21% of total),
which was present in all but one locality. In contrast, the
orders Anaspidea (n = 4, 4% of total) and Cephalaspidea
(n = 6, ~6% of total) were only found in two localities
(Table 2).
The highest number of specimens (n = 48) was found
at locality 4, which included all 5 clades of heterobranch
sea slugs (Table 3). All ve clades were also found at
locality 5 (n = 23), while locality 2 (n = 25) only included
Nudibranchia and Sacoglossa. The lowest overall speci-
men numbers were recorded in localities 1 (n = 1) and 3
(n = 4), potentially due to the fewest search hours
invested (4.3 and 5 h, respectively) (Table 3). The aver-
age search time was 16.2 hours, yielding an average of 20
specimens per locality.
Individual species and localities found during the sur-
vey are listed in Table 1 and photos of most species are
provided in Figures 2–19. One juvenile specimen of a
species of Felimare Marcus and Marcus, 1967 and a spec-
imen of a species of Tenellia Costa, 1866 could not be
identied to the species level, and the latter could poten-
tially constitute an undescribed species.
DISCUSSION
This study contributes additional information to the lim-
ited knowledge on Caribbean heterobranch sea slug
diversity by providing new records and data on collecting
effort by hour in the Bocas del Toro Archipelago. During
a total of 81 search-effort hours, we found 20 sea slug
species of Anaspidea, Cephalaspidea, Nudibranchia,
Pleurobranchomorpha, and Sacoglossa, which represents
Figure 1. Map of localities surveyed for this study.

Jaime L. Neill et al., 2024 Page 77
Table 1. Total number of specimens per species found in each locality. *unidentied
juvenile; **potentially undescribed species; #new records for Bocas del Toro.
Clade Species
Localities
(total specimens)
Anaspidea Aplysia dactlylomela 5(3)
Stylocheilus striatus 4(1)
Cephalaspidea Chelidonura hirundinina #5(1)
Haminoea antillarum 4(5)
Nudibranchia Anteaeolidiella lurana 4(2)
Cadlina rumia 3(1) 4(1)
Dendrodoris krebsii 5(1)
Diaulula phoca 5(3)
Felimare sp. (juvenile) * 4(1)
Felimida clenchi 3(1) 5(2)
Jorunna spazzola 3(1) 5(1)
Phidiana lynceus 2(3)
Taringa telopia #5(3)
Tenellia sp. ** #3(1)
Pleurobranchomorpha Berthella vialactea #5(1)
Berthellina quadridens 4(6)
Pleurobranchus areolatus 1(1) 4(1)
Sacoglossa Elysia crispata 2(20) 5(1)
Elysia velutinus 2(30) 4(2) 5(7)
Cynlindrobulla beauii #4(1)
Table 2. Number and percentages of specimens found per clade during the
present study.
Order Number of specimens % of total Localities
Anaspidea 4 4.0 4, 5
Cephalaspidea 6 5.9 4, 5
Nudibranchia 21 20.8 2, 3, 4, 5
Pleurobranchomorpha 9 8.9 1, 4, 5
Sacoglossa 61 60.4 2, 4, 5
Table 3. Number of specimens found per clade and search time in each locality.
Locality Search time (h) Anaspidea Cephalaspidea Nudibranchia
Pleurobrancho-
morpha Sacoglossa Total
1 4.3 - - - 1 - 1
2 16 - - 3 - 22 25
3 5 - - 4 - - 4
4 24.9 1 5 4 7 31 48
5 30.9 3 1 10 1 8 23

Page 78 THE NAUTILUS Vol. 138, No. 3–4
about 6.5% of the total biodiversity in the Caribbean
(n = 308) (see Valdés etal., 2006). A study conducted
prior to our research in Bocas del Toro documented 86
species, 27.9% of total Caribbean biodiversity during
307.5 hours of search time (Goodheart etal., 2016). Prior
to the 2016 study, only 19 species of Caribbean hetero-
branch sea slugs had been formally documented in the
Bocas del Toro region. In our study, we found four spe-
cies that were not mentioned in previous publications by
Collin et al. (2005) and Goodheart et al. (2016):
Chelidonura hirundinina (Quoy and Gaimard, 1833)
(Cephalaspidea), Berthella vialactea Ghanimi etal., 2020
(Pleurobranchomorpha), Taringa telopia Er. Marcus,
1955 (Nudibranchia), and Cynlindrobulla beauii Fischer,
1857 (Sacoglossa). In addition, a juvenile Felimare spe-
cies and a potentially undescribed species of Tenellia
were not identied past the genus level.
Among the total sea slug numbers, counts of individu-
als of species of the genus Elysia Risso, 1818 were mark-
edly above the specimen numbers reported for all other
taxa, which yielded a single-digit number per species
(n ≤ 6). Elysia velutinus Pruvot-Fol, 1947 was the most
common species in the current study (n = 39), followed
by Elysia crispata Mörch, 1863 (n = 21). In contrast,
Figures 2–9. Photographs of living animals of Cephalaspidea, Pleurobranchomorpha, Anaspidea, and Sacoglossa. 2. Haminoea
antillarum (d’Orbigny, 1841). 3. Chelidonura hirundinina (Quoy and Gaimard 1832). 4. Berthella vialactea Ghanimi etal., 2020.
5. Pleurobranchus areolatus Mörch, 1863. 6. Stylocheilus striatus (Quoy and Gaimard, 1832). 7. Elysia crispata Mörch, 1863.
8. Elysia velutinus Pruvot-Fol, 1947. 9. Cylindrobulla beauii P. Fisher, 1857.

Jaime L. Neill et al., 2024 Page 79
other studies previously stated that E. crispata was the
most abundant taxon (Collin et al., 2005; Goodheart
etal., 2016) and indicated that this species is one of the
most common within waters surrounding Bocas del Toro
and the Caribbean region (Collin et al., 2005; Valdés
etal., 2006). The bulk of our sampling efforts, measured
in terms of person-hours and number of participants,
involved direct observation methods. Direct observation
as the primary surveying method likely exerted a signi-
cant inuence on higher documented diversity of large
Figures 10–19. Photographs of living animals of Nudibranchia. 10. Cadlina rumia Er. Marcus, 1955. 11. Dendrodoris krebsii
(Mörch, 1863). 12. Diaulula phoca (Ev. Marcus and Er. Marcus, 1967). 13. Felimida clenchi (Russell, 1935). 14. Felimare sp.
( juvenile). 15. Taringa telopia Er. Marcus, 1955. 16. Jorunna spazzola (Er. Marcus, 1955). 17. Phidiana lynceus Bergh, 1867.
18. Anteaeolidiella lurana (Ev. Marcus and Er. Marcus, 1967). 19. Tenellia sp.

Page 80 THE NAUTILUS Vol. 138, No. 3–4
species, including E. crispata. Factors such as the larger
adult size of this species, combined with its abundance,
and occasional tendency to venture onto non-dietary sub-
strates (Krug etal., 2016), make it more easily detectable.
On the contrary, the high counts of E. velutinus, a rela-
tively small, camouaged species (Krug etal., 2016) can
be attributed to indirect collecting of substrate. Indirect
sampling accounted for only two species, E. velutinus
and C. beauii, and therefore it did not impact biodiversity
estimates substantially.
Difculties in locating these organisms can be
attributed to how they appear to collectors, and the char-
acteristics of their surrounding environment. In addition
to distribution and abundance, sea slug appearances are
also determined by their life history traits such as cryptic
coloration, size, and behavior. Likewise, environmental
characteristics inuence both behavioral responses of sea
slugs and observer encounters; these include variation in
habitat-type assemblages, resource availability of food or
shelter, and abiotic factors such as water turbidity. Other
limiting factors in the present study include a substan-
tially broad range in search skills and physical abilities in
the water by the collectors. Some observers have con-
ducted surveys in the eld, whereas a majority lacked
prior experience in searching for sea slugs. Even seasoned
observers may encounter challenges due to the inherent
complexities of locating specimens. The diversity of
methodologies and levels of researcher experience ulti-
mately exerts inuence on the nal observation counts.
The resulting dataset is inherently affected by these mul-
tifaceted factors, and some may explain the relatively
lower numbers obtained in our study compared to those
with more experienced observers, such as the study con-
ducted by Goodheart etal. (2016).
In addition to previous research by Collin etal. (2005)
and Goodheart etal. (2016), the current study contrib-
utes to the inventory of heterobranch sea slug species
within the Bocas del Toro Archipelago. All these publica-
tions are important taking into account the shifting base-
line theory, where changes to existing environmental
conditions are often unnoticed by future generations of
society experiencing the new environment (Jackson,
1997). We contributed hours to searching for sea slugs to
assess the biodiversity of this group and document elu-
sive and rare species. Even though the collecting effort of
our study was considerably less in comparison to earlier
studies, we found several previously undocumented spe-
cies within the Bocas del Toro Archipelago. This suggests
that the diversity of sea slug species in the Caribbean
region is still poorly known and further studies on sea
slug biodiversity are needed.
ACKNOWLEDGMENTS
We thank Dr. Peter Castro for supporting student and
faculty travel costs to Panama. Funding for student
travel and supplies was also provided through the
CPP Instructionally Related Activities (to the IRA
Group: Biological Sciences Field Educational Opportu-
nities for Students) and the California State University
Council on Ocean Affairs, Science & Technology (CSU
COAST) through their Field Experiences Support Pro-
gram. TheCPP College of Science and the Department
of Biological Sciences also provided funding for some
aspects of faculty travel, student international travel
insurance, and staff support for completing travel paper-
work requirements. We also thank Dr. Pete Lahanas and
Dr. Leo Caballos and (ITEC) the Institute for Tropical
Ecology and Conservation for hosting us at their eld
station inBocas del Toro and providing extensive logisti-
cal support.
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