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Neotropical Biodiversity
ISSN: (Print) 2376-6808 (Online) Journal homepage: http://www.tandfonline.com/loi/tneo20
An integrative identification guide to the Hydrozoa
(Cnidaria) of Bocas del Toro, Panama
Maria Pia Miglietta, Stefano Piraino, Sarah Pruski, Magdalena Alpizar
Gonzalez, Susel Castellanos-Iglesias, Sarai Jerónimo-Aguilar, Jonathan W.
Lawley, Davide Maggioni, Luis Martell, Yui Matsumoto, Andrea Moncada,
Pooja Nagale, Sornsiri Phongphattarawat, Carolina Sheridan, Joan J. Soto
Àngel, Alena Sukhoputova & Rachel Collin
To cite this article: Maria Pia Miglietta, Stefano Piraino, Sarah Pruski, Magdalena Alpizar
Gonzalez, Susel Castellanos-Iglesias, Sarai Jerónimo-Aguilar, Jonathan W. Lawley,
Davide Maggioni, Luis Martell, Yui Matsumoto, Andrea Moncada, Pooja Nagale, Sornsiri
Phongphattarawat, Carolina Sheridan, Joan J. Soto Àngel, Alena Sukhoputova & Rachel Collin
(2018) An integrative identification guide to the Hydrozoa (Cnidaria) of Bocas del Toro, Panama,
Neotropical Biodiversity, 4:1, 102-112, DOI: 10.1080/23766808.2018.1488656
To link to this article: https://doi.org/10.1080/23766808.2018.1488656
© 2018 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
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Published online: 29 Jul 2018.
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An integrative identification guide to the Hydrozoa (Cnidaria) of Bocas del
Toro, Panama
Maria Pia Miglietta
a
, Stefano Piraino
b
, Sarah Pruski
a
, Magdalena Alpizar Gonzalez
c
, Susel Castellanos-
Iglesias
d
, Sarai Jerónimo-Aguilar
e
, Jonathan W. Lawley
f
, Davide Maggioni
g,h
, Luis Martell
i
,
Yui Matsumoto
a
, Andrea Moncada
j
, Pooja Nagale
k
, Sornsiri Phongphattarawat
l
,
Carolina Sheridan
m
, Joan J. Soto Àngel
j
, Alena Sukhoputova
n
and Rachel Collin
o
a
Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas, USsa;
b
Dipartimento di Scienze e Tecnologie
Biologiche ed Ambientali, DISTEBA, Università del Salento, Lecce, Italy;
c
Zooplankton Laboratory, CIMAR, Universidad de Costa Rica,
Costa Rica;
d
Cnidaria Laboratory, Federal University of Parana (UFPR), Curitiba, Brazil;
e
Unidad Académica Sisal, Universidad Nacional
Autonóma de Mexico;
f
Departamento de Zoologia, Universidade de São Paulo, SP, Brazil;
g
Marine Research and High Education (MaRHE)
Center, Republic of Maldives;
h
Dipartimento di Scienze del Territorio e dell’Ambiente (DISAT), Università degli Studi di Milano-Bicocca,
Milano, ITALY;
i
Department of Natural History, University Museum of Bergen, University of Bergen, Bergen, Norway;
j
Institut Cavanilles
de Biodiversitat i Biologia Evolutiva, Universitat de València, València, Spain;
k
Department of Conservation, Bombay Natural History
Society, India;
l
Marine Ecology Laboratory, Department of Marine Science, Chulalongkorn University, Thailand;
m
Rodríguez, Biology
school, Universidad de Costa Rica, San José, Costa Rica;
n
Department of Biological Evolution, Lomonosov Moscow State University,
Moscow, Russia;
o
Smithsonian Tropical Research Institute, Balboa Ancon, Panama
ABSTRACT
This work is the first attempt to assess the biodiversity of the Hydrozoa in the Archipiélago de
Bocas del Toro (Panamá, Caribbean Sea) using morphology and molecular taxonomy, and to
produce field identification tools to help future identification and monitoring efforts in the
area.
We sampled, identified, vouchered, and barcoded 112 specimens of Hydrozoa from shal-
low coastal waters (0–22 m depth) in the Archipiélago de Bocas del Toro. The specimens
belong to 70 taxa, of which 53 were identified at the species level, and 17 were identified at
the genus or family level. We produced 64 sequences of the large ribosomal subunit of the
mitochondrial RNA (mt lsu-rRNA, 16S), the genetic marker generally used for barcoding
Hydrozoa. We updated the local checklist that now comprises 118 species, and produced
87 detailed taxon identification tables that display species descriptions augmented with
pictures, geographic distribution (worldwide and in Bocas del Toro), GenBank accession
numbers for the 16S mitochondrial gene, and a synopsis of the families they belong to.
ARTICLE HISTORY
Received 6 February 2018
Accepted 11 June 2018
KEYWORDS
Hydrozoa; Bocas del Toro;
identification tools;
barcoding; Caribbean; 16S;
biodiversity
Introduction
Hydrozoa are an inconspicuous and often overlooked
class of the phylum Cnidaria [1]. Most hydrozoans
have a complex life cycle characterized by a progres-
sion of three life stages: a short-living larva (the pla-
nula), generally metamorphosing into a benthic
colonial stage (the polyp), and a pelagic sexual stage
(the medusa stage) asexually budded offfrom the
polyp [2]. The life cycle can be shortened into a bi-
phasic cycle, by reduction or complete suppression of
either the polyp or the medusa stage [3]. With more
than 3,700 described species [ 4] hydrozoans are
structurally and functionally important members of
benthic and planktonic communities [5; 1]. Work on
Hydrozoa has been hampered by the scarcity of taxo-
nomic expertise, which has dramatically declined over
the past two decades [6,7]. Also, because polyps and
medusae require different expertise and each follow
their own identification rules, linking both to a single
species has proven difficult and has further hampered
cohesive taxonomic revisions. In the last 10 years
molecular tools have contributed significantly to
hydrozoan taxonomy and have shown that selected
gene sequences may be necessary, in combination
with traditional taxonomy, to correctly identify cryptic
species and disentangle taxonomic confusion [8–12].
Hydrozoa from the Atlantic/Caribbean coast of
Panama are abundant but scarcely studied. The
Archipiélago de Bocas del Toro, Panamá is located
on the NW Caribbean shore of Panama, close to the
Costa Rican border. It consists of more than 68
small islands and mangrove keys and is character-
ized by diverse ecosystems, from mangrove domi-
nated shallow water to coral reefs and sea grass
meadows (see Figure 1 for a map). To date, 79
nominal species have been reported in the Bocas
del Toro region [13]. However, proper descriptions
and species identification tools are lacking, inade-
quate,orscatteredinoldandhardtoaccess
CONTACT Maria Pia Miglietta miglietm@tamug.edu; Stefano Piraino stefano.piraino@unisalento.it
Supplemental data can be accessed here.
NEOTROPICAL BIODIVERSITY
2018, VOL. 4, NO. 1, 102–112
https://doi.org/10.1080/23766808.2018.1488656
© 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits
unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Published online 29 Jul 2018
articles, thus hindering the ability of nonexperts to
identify species of interest in this area.
This work is a result of the Taxonomic Training
workshop held in July 2015 in Bocas del Toro,
Panama, organized by Smithsonian Tropical
Research Institute as part of a National Science
Foundation Advancing Revisionary Taxonomy and
Systematics (ARTS) grant. During the workshop, in
which 14 students participated, we collected shal-
low water Hydrozoa around the Archipiélago de
Bocas del Toro, Panamá. Collections targeted both
pelagic medusa with plankton tows and benthic
polyps with snorkeling. In this paper, we present
an updated checklist of hydrozoan biodiversity in
the Archipiélago de Bocas del Toro,, augmented by
[I] a DNA barcoding database consisting of
sequences of a ~ 600bp gene fragment of the
mitochondrial large ribosomal RNA subunit (mt
lsu-rRNA, 16S), and [II] taxon identification tables.
The 16S gene has been successfully used for taxo-
nomic revisions and is considered the Hydrozoa
“barcoding”molecule [10,11,14–17]. Both the bar-
coding data and the taxonomic identification sheets
were produced to aid future biodiversity inventory
efforts in the region.
Material and methods
Collection
Hydrozoa were collected during the Tropical
Taxonomy Training course on systematics and
Hospital point
Bocas del Drago
Swan’s Key
Crawl Cay
Almirante piling
Figure 1. Map of the Bocas del Toro archipelago, with sampling localities.
NEOTROPICAL BIODIVERSITY 103
biology of Hydrozoa (Cnidaria) held at the
Smithsonian Tropical Research in Bocas del Toro,
Panama from 7/7/2015 to 7/21/2015. A total of 16
people (two instructors and 14 students) were in
the field during every sampling effort. A total of
11 sites were sampled. Localities sampled were:
Bocas del Toro Marine Station docks/weather sta-
tion, Punta Hospital, Crawl Cay, Bocatorito Bay vici-
nity, San Cristobal, Vicinity of Manuguar Cay, Punta
Caracol, Swans Cay, Bastimento vicinity of “Casa
Verde”, Bocas del Drago, Pandora, Almirante
(Quary’spoint)(Table 1 and Figure 1). Polyps were
collected by snorkeling (0–8mdepth)orSCUBA
diving (18–22 m depth), and medusae by plankton
towing using a net with 280µm mesh size. Plankton
tows were carried out near the Bocas del Toro
Station docks and weather station.
Polyps and medusae were sorted in the labora-
tory and identified to the lowest taxonomic level
using appropriate taxonomic literature [e.g. 16–20].
When possible, polyps from each colony where
divided in two vials and preserved in both formalin
(for morphological analyses) and 99% ethanol (for
genetic analyses). Vouchered specimens were
deposited at the Museum of Universidad the
Panamá, Panama City, Panama. When little tissue
was available, specimens were preserved in ethanol
only and used for molecular analyses. DNA samples
are currently at the University of Texas A&M at
Galveston. Pictures of live specimens featured col-
ony, polyps, medusae (or equivalent reproductive
structures), and other morphological structures use-
ful for identification.
Barcoding
Genomic DNA was extracted using standard tech-
niques followed by ethanol precipitation [8].
A ~ 600bp fragment of the large ribosomal subunit
of the mitochondrial RNA (lsu-rRNA, 16S) was
amplified using SHA and SHB primers [23],
Polymerase Chain Reaction (PCR), and conditions
as described in Miglietta [15]. The PCR product
was run on a 2% agarose gel stained with
SybrGreen I nucleic acid gel stain (Sigma-Aldrich)
to assay its quantity and quality (i.e. accessory
bands). PCR products were purified using exoSAP-
it (Affymetrix), following manufacturer’s instruction
and used as a template for double stranded
sequencing with the amplification primers. The
purified DNA was sequenced at the Texas A&M
Corpus Christi Genomics Core Laboratory.
Sequences were analyzed in Geneious R9 (http://
www.geneious.com [24]) and deposited in
Genbank (accession numbers MH361321 to
MH361381). For definition of anatomical terms
usedintheIDtables,seeonlinetaxonomic
glossary for Hydrozoa at https://stricollections.org/
portal/misc/glossarycover.php [25].
Results
We collected, vouchered, and fixed in ethanol and/or
formalin 112 specimens of Hydrozoa (Table 1). We iden-
tified a total of 53 species. An additional 17 taxa could
be identified at the genus orfamily level only due to the
lack of fertile structures, small size of the colony, or, in
the case of planktonic specimens, early age of the
medusae (Table 2 for a complete species list).
We sequenced the 16S gene for 64 out of 112
specimens belonging to 44 species. Some of the
112 specimens did not yield sufficient DNA for
Polymerase Chain Reaction and thus could not be
barcoded. For some species, however, multiple
sequences were produced. All sequences were
~ 600bp in length and were deposited in GenBank
(accession numbers MH361321-MH361332,
MH361334-MH361359, MH361361-MH361381,
MH374630).
Morphological, ecological, and barcoding data where
assembled in Taxon Identification Tables. We produced
87 tables featuring 28 families (13 in the order
Anthoathecata; 12 in the order Leptothecata, 2 in the
order Trachymedusae and 1 in the Order
Limnomedusae) and 55 species (Appendix 1). These 55
species represent the most common Hydrozoa found in
Bocas del Toro during the workshop. For the most spe-
ciose taxa we supply identification keys (to genera and/or
to species). One of the most abundant families found in
theareawastheCampanulariidae,with3generaand9
species. Because the polyps of the three genera sampled
(Clytia, Gastroblasta,andObelia) can be easily confused
we also supply identification tables for each genus.
Discussion
Check list of Bocas del Toro Hydrozoa
A comprehensive inventory of the Hydrozoa from the
Caribbean coast of Panama was previously produced by
Calder and Kirkendale [13], who gathered three different
collections acquired in 1969, 2002, and 2004, mostly from
the Bocas del Toro region. They recorded 79 nominal
species (of which were 17 identified at the genus or
family level only) belonging to 22 families. We found 53
species, of which only 31 were in common with Calder
and Kirkendale [13]. We merged our own inventory with
that of Calder and Kirkendale [13],to produce an updated
checklist of the Hydrozoa of Bocas del Toro that now
comprises 118 taxa, of which 86 identified at the species
level and 32 identified at the genus or higher level
(Table 3).Givensuchasmallgeographicalarea
(250 km
2
), this is an impressive number. For comparison,
118 species constitutes about ¼ of the total known
104 M. P. MIGLIETTA ET AL.
Table 1. Samples collected during the 2015 Hydrozoa workshop held in Bocas del Toro, Panama. Date of collections, sample ID, species identified, type of fixative used for preservation (ethanol or
formalin), GenBank accession number, and location within the Bocas del Toro archipelago are reported. In the table N = No, Y = Yes.
Date Sample ID Species Fertile Ethanol Formalin Sequenced/ GenBank accession # Location
1 7/7/2015 BTH.15.1 Kirchenpaueria halecioides Y Y N N STRI BDT docks/weather station
2 7/7/2015 BTH.15.2 Halecium cf. bermudense Y Y N N STRI BDT docks/weather station
3 7/7/2015 BTH.15.3 Nemalecium lighti N Y Y N STRI BDT docks/weather station
4 7/7/2015 BTH.15.4 Nemalecium lighti N Y Y MH361321 STRI BDT docks/weather station
5 7/7/2015 BTH.15.5 Kirchenpaueria halecioides N Y Y N STRI BDT docks/weather station
6 7/7/2015 BTH.15.6 Clytia linearis Y Y N MH374630 STRI BDT docks/weather station
7 7/7/2015 BTH.15.7 Dynamena crisioides Y Y N MH361322 STRI BDT docks/weather station
8 7/7/2015 BTH.15.8 ?Cytaeis N Y Y N STRI BDT docks/weather station
9 7/7/2015 BTH.15.9 Dynamena crisioides Y Y N MH361323 STRI BDT docks/weather station
10 7/7/2015 BTH.15.10 Halecium bermudense Y Y N N STRI BDT docks/weather station
11 7/8/2015 BTH.15.11 Myrionema amboinense N Y Y N Punta hospital
12 7/8/2015 BTH.15.12 Plumularia sp. N Y Y N Punta hospital
13 7/8/2015 BTH.15.13 Antennella secundaria Y Y N MH361324 Punta hospital
14 7/8/2015 BTH.15.14 Halopteris alternata N Y N MH361325 Punta hospital
15 7/8/2015 BTH.15.15 Eudendrium carneum N Y Y MH361326 Punta hospital
16 7/8/2015 BTH.15.16 Salacia desmoides Y Y Y MH361327 Punta hospital
17 7/8/2015 BTH.15.17 Eudendrium bermudense Y Y Y N Punta hospital
18 7/8/2015 BTH.15.18 Antennella secundaria Y Y Y MH361328 Punta hospital
19 7/8/2015 BTH.15.19 Obelia dichotoma Y Y Y N Punta hospital
20 7/8/2015 BTH.15.20 Aglaophenia latecarinata N Y Y N BDT docks/weather station
21 7/8/2015 BTH.15.21 Kirchenpaueria halecioides Y N Y N Punta hospital
22 7/8/2015 BTH.15.22 Plumularia sp. N Y Y N Punta hospital
23 7/9/2015 BTH.15.23 Pennaria disticha Y Y Y MH361329 Crawl Cay
24 7/9/2015 BTH.15.24 Ralpharia gorganiae Y Y N MH361330 Crawl Cay
25 7/9/2015 BTH.15.25 Stylaster roseus N Y Y MH361331 Crawl Cay
26 7/9/2015 BTH.15.26 Thyroscyphus marginatus Y Y Y MH361332 Crawl Cay
27 7/9/2015 BTH.15.27 Gastroblasta raffaelei N Y Y N Crawl Cay
28 7/9/2015 BTH.15.28 Pennaria disticha Y Y N N Crawl Cay
29 7/9/2015 BTH.15.29 Thyroscyphus marginatus N Y N MH361334 Crawl Cay
30 7/9/2015 BTH.15.30 ?Obelia dichotoma N Y Y N Crawl Cay
31 7/9/2015 BTH.15.31 Millepora alcicornis N Y N MH361335 Crawl Cay
32 7/9/2015 BTH.15.32 Dynamena disticha N Y Y MH361336 Crawl Cay
33 7/9/2015 BTH.15.33 Dynamena crisioides N Y N N Crawl Cay
34 7/9/2015 BTH.15.34 Obelia dichotoma Y N Y N Crawl Cay
35 7/9/2015 BTH.15.35 Eudendrium capillare Y Y Y MH361337 Crawl Cay
36 7/9/2015 BTH.15.36 Clytia hemisphaerica Y Y N N Crawl Cay
37 7/9/2015 BTH.15.37 Clytia hemisphaerica N N Y N Crawl Cay
38 7/9/2015 BTH.15.38 Halecium sp.2 Y Y Y MH361338 Crawl Cay
39 7/9/2015 BTH.15.39 Hincksella formosa N Y Y MH361339 Crawl Cay
40 7/10/2015 BTH.15.40 Sphaerocoryne cf. agassizii N Y Y MH361340 Near Bocatorito Bay
41 7/10/2015 BTH.15.41 Clytia hemisphaerica N Y Y N Near Bocatorito Bay
42 7/10/2015 BTH.15.42 Monotheca margaretta Y Y Y N Near Bocatorito Bay
43 7/10/2015 BTH.15.43 Sertularia distans N Y Y MH361341 Near Bocatorito Bay
44 7/10/2015 BTH.15.44 Gastroblasta raffaelei N Y Y MH361342 Near Bocatorito Bay
45 7/10/2015 BTH.15.45 Halecium cf. nanum N Y Y MH361343 Near Bocatorito Bay
46 7/10/2015 BTH.15.46 Gastroblasta raffaelei N Y Y N Near Bocatorito Bay
47 7/10/2015 BTH.15.47 Kirchenpaueria halecioides N Y N MH361344 Near Bocatorito Bay
(Continued)
NEOTROPICAL BIODIVERSITY 105
Table 1. (Continued).
Date Sample ID Species Fertile Ethanol Formalin Sequenced/ GenBank accession # Location
48 7/10/2015 BTH.15.48 Gastroblasta raffaelei N Y N N Near Bocatorito Bay
49 7/10/2015 BTH.15.49 Gastroblasta raffaelei N Y N N Near Bocatorito Bay
50 7/10/2015 BTH.15.50 Halopteris alternata N Y Y MH361345 Near Bocatorito Bay
51 7/10/2015 BTH.15.51 Monotheca margaretta Y Y Y MH361346 Near Bocatorito Bay
52 7/10/2015 BTH.15.52 Halecium sp. [sensu 17] N Y N MH361347 Near Bocatorito Bay
53 7/10/2015 BTH.15.53 Halopteris alternata N Y N MH361348 Near Bocatorito Bay
54 7/10/2015 BTH.15.54 Kirchenpaueria halecioides Y Y Y MH361349 Near Bocatorito Bay
55 7/11/2015 BTH.15.55 Gastroblasta raffaelei N Y Y N San Cristobal
56 7/11/2015 BTH.15.56 Oceaniidae indet N Y Y N San Cristobal
57 7/11/2015 BTH.15.57 Halecium sp.1 N Y N MH361350 San Cristobal
58 7/11/2015 BTH.15.58 Nemalecium lighti N Y N MH361351 San Cristobal
59 7/11/2015 BTH.15.59 Oceaniidae indet N Y N N San Cristobal
60 7/11/2015 BTH.15.60 Obelia bidentata N Y N MH361352 San Cristobal
61 7/11/2015 BTH.15.61 Amphinema dinema Medusa N N N San Cristobal
62 7/11/2015 BTH.15.62 Clytia gracilis Y Y Y N San Cristobal
63 7/11/2015 BTH.15.63 Liriope tetraphylla Medusa Y Y MH361353 San Cristobal
64 7/11/2015 BTH.15.64 Thecocodium sp. N Y N MH361354 San Cristobal
65 7/12/2015 BTH.15.65 Plumularia floridana Y Y Y MH361355 Vicinity of Manuguar Cay
66 7/12/2015 BTH.15.66 Cirrholovenia tetranema N N Y N Vicinity of Manuguar Cay
67 7/12/2015 BTH.15.67 Clytia hummelincki Y Y Y N Vicinity of Manuguar Cay
68 7/12/2015 BTH.15.68 Clytia linearis N Y N MH361356 Vicinity of Manuguar Cay
69 7/12/2015 BTH.15.69 Sphaerocoryne cf. agassizii N Y N N Vicinity of Manuguar Cay
70 7/12/2015 BTH.15.70 Halecium tenellum Y Y Y N Vicinity of Manuguar Cay
71 7/12/2015 BTH.15.71 Egmundella sp. (on Clytia linearis) N N Y N Vicinity of Manuguar Cay
72 7/12/2015 BTH.15.72 Clytia hummelincki Y Y N MH361357 Vicinity of Manuguar Cay
73 7/12/2015 BTH.15.73 Dynamena crisioides Y Y Y MH361358 Vicinity of Manuguar Cay
74 7/12/2015 BTH.15.74 Dynamena crisioides N Y N MH361359 Vicinity of Manuguar Cay
75 7/12/2015 BTH.15.75 Obelia bidentata N Y Y N Vicinity of Manuguar Cay
76 7/12/2015 BTH.15.76 Clytia linearis N Y Y MH361361 Vicinity of Manuguar Cay
77 7/12/2015 BTH.15.77 Nemalecium lighti Y Y N MH361362 Vicinity of Manuguar Cay
78 7/13/2015 BTH.15.78 Pteroclava krempfiN Y Y MH361363 Punta Caracol
79 7/13/2015 BTH.15.79 Sphaerocoryne cf. agassizi NY N MH361364 Punta Caracol
80 7/13/2015 BTH.15.80 Eudendrium capillare N Y N N Punta Caracol
81 7/13/2015 BTH.15.81 Pteroclava krempfiN Y Y N Punta Caracol
82 7/13/2015 BTH.15.82 Eudendrium capillare Y Y Y N Punta Caracol
83 7/13/2015 BTH.15.83 Halopteris alternata N Y Y N Punta Caracol
84 7/13/2015 BTH.15.84 Clytia noliformis Y Y N N Punta Caracol
85 7/13/2015 BTH.15.85 Bougainvilliidae/?Bimeria N Y Y MH361365 Punta Caracol
86 7/13/2015 BTH.15.86 Codonorchis sp. N Y N N Punta Caracol
87 7/14/2015 BTH.15.87 Solanderia gracilis Y Y Y MH361366 Swans Cay
88 7/14/2015 BTH.15.88 Eudendrium bermudense Y Y Y MH361367 Swans Cay
89 7/14/2015 BTH.15.89 Thyroscyphus ramosus N Y Y MH361368 Swans Cay
90 7/14/2015 BTH.15.90 Pennaria disticha Y Y Y MH361369 Swans Cay
91 7/14/2015 BTH.15.91 Eudendrium carneum Y (Female) Y Y MH361370 Swans Cay
92 7/14/2015 BTH.15.92 Stylaster roseus N Y Y MH361371 Swans Cay
93 7/14/2015 BTH.15.93 Stauridiosarsia nipponica N Y Y MH361372 Swans Cay
94 7/14/2015 BTH.15.94 Sertularia marginata N Y Y MH361373 Swans Cay
95 7/14/2015 BTH.15.95 Eudendrium bermudense Y (male) Y Y N Swans Cay
(Continued)
106 M. P. MIGLIETTA ET AL.
Hydrozoa species from the Mediterranean Sea [26], and
more than a half of the species known from the Arctic [27]
or the Antarctic [28]. Seven families and 12 genera are
also reported for the first time in Bocas del Toro. Genera
added to the checklist are: Amphynema, Cytaeis,
Codonorchis, Rhizogeton, Thecocodium, Turritopsoides (?),
Gastroblasta, Egmundella, Pteroclava, Cubaia, Lyriope,and
Persa. Families new to the Bocas del Toro region are:
Pandeidae, Cytaeididae, Cladocorynidae, Ptilocodidae,
Olindiidae, Geryoniidae, Rhopalonematidae. Of the new
species added to the list, of particular interest is
Thecocodium sp. The genus Thecocodium was never
reported in the Caribbean and was only recently
recorded for the firsttimeintheAtlanticOcean[29].
Thecocodium sp. (specimen BTH 15.64) presents unique
morphological features and may represent a new species.
Another species of interest is a species of the genus
Coryne (specimen 15.93) found in Swans Key. The colony
could not be identified at the species level; however in
GenBank its 16S sequence showed 100% identity with
Coryne japonica (AY512540) from New Zealand. C. japo-
nica has been reported from the Pacific Ocean but never
from the Atlantic Ocean. Our record from Bocas del Toro
is the first in the Atlantic Ocean and may represent an
introduced species.
Taxon identification sheets
Taxon Identification Sheets collate the taxonomic descrip-
tion of 56 species found during the Hydrozoa Taxonomy
course and confidently identified at the species level.
They also include a brief synopsis of the 28 families they
belong to (see Tables 1–88 in Supplementary Materials.
For each family we included authorship, corresponding
Order, number of species (worldwide and in Bocas del
Toro), morphologically similar taxa that could be mista-
kenly identified as member of the family of interest, and
their key diagnostic characters. The species identification
sheets include author, diagnostic characters of the colony
and their reproductive structures (medusae, eumedu-
soids, or fixed gonophores), species ecology, species dis-
tribution in Bocas del Toro, number of specimens
collected, pictures and, when available, GenBank acces-
sion numbers for their 16S sequence(s). These species
identification sheets assemble in simple format informa-
tion that can be used for a correct identification. The
morphological description, pictures, and link to their 16S
barcoding sequence represent a comprehensive display
of information that integrates traditional and modern
taxonomy into a practical tool to aid identification of the
most commons species of Hydrozoa in the shallow waters
of the Archipiélago de Bocas del Toro, Panamá.
Conclusive remarks
Knowledge on the local biodiversity is an essential pre-
requisite for the monitoring and management of
Table 1. (Continued).
Date Sample ID Species Fertile Ethanol Formalin Sequenced/ GenBank accession # Location
96 7/14/2015 BTH.15.96 Pennaria disticha N Y N MH361374 Swans Cay
97 7/14/2015 BTH.15.97 Macrorhynchia grandis N Y Y N Swans Cay
98 7/14/2015 BTH.15.98 Bougainvilliidae 2/?Bimeria N Y Y MH361375 Swans Cay
99 7/14/2015 BTH.15.99 Clytia sp. Y Y N MH361376 Swans Cay
100 7/16/2015 BTH.15.100 Antennella secundaria Y Y Y N Bastimento vicinity of “Casa Verde”
101 7/15/2015 BTH.15.101 Dentitheca dendritica N Y N MH361377 The Wall (25mt)/Pandora (20m)
102 7/17/2015 BTH.15.102 Filifera (on hermit crab)/?Turritopsoides N Y N MH361378 Almirante (Quary’s point)
103 7/17/2015 BTH.15.103 Persa incolorata Medusa Y N N Plankton tow near BDT docks
104 7/17/2015 BTH.15.104 Bougainvillia ?pyramidata Medusa Y N MH361379 Plankton tow near BDT docks
105 7/17/2015 BTH.15.105 Cubaia aphrodite Medusa N Y N Plankton tow near BDT docks
106 7/18/2015 BTH.15.106 Sertularia rugosissima N Y Y N Bocas del Drago
107 7/18/2015 BTH.15.107 Sertularia rugosissima N Y N N Bocas del Drago
108 7/18/2015 BTH.15.108 Rhizogeton sterreri N Y Y MH361380 Bocas del Drago
109 7/15/2015 BTH.15.109 Sertularella diaphana N Y Y MH361381 The wall (25mt)/Pandora (20m)
110 7/10/2015 No Voucher Turritopsis sp.1 Y N N MH029856, MH029857 Close to Bocatorito Bay
111 7/7/2015 No Voucher Zanclea alba N N N N STRI BDT docks/weather station
112 7/7/2015 No Voucher Millepora complanata N N N N STRI BDT docks/weather station
113 7/7/2015 No Voucher Turritopsis dohrnii Y N N MH029858, MH029859 Multiple locations
NEOTROPICAL BIODIVERSITY 107
Table 2. List of species found in Bocas del Toro during the Hydrozoa Taxonomy course in 2015. For each species we report
voucher name(s), number of barcoding sequences (mt lsu-rRNA, 16S) produced per species, and whether their taxonomic
description is in the Taxon Identification Tables. A total of 53 taxa were identified at the species level. At the bottom, 17 taxa
identified at the genus or higher taxonomic level.
Species Voucher Name Family
Barcoding (n. of
sequences)
Taxon
Identification Table
1Turritopsis dohrnii Yes Oceaniidae Yes (2) Yes
2Turritopsis sp. 1 BTH.15.110 Oceaniidae Yes (2) Yes
3Turritopsis sp. 4 No Oceaniidae No Yes
4Rhizogeton sterreri BTH.15.108 Oceaniidae Yes (1) Yes
5Bougainvillia cf. pyramidata
medusae
BTH.15.104 Bougainvilliidae Yes (1) No
6Amphinema dinema BTH.15.61 Pandeidae No Yes
7Stylaster roseus BTH.15.25; BTH.15.92 Stylasteridae Yes (2) Yes
8Eudendrium bermudense BTH.15.17; BTH.15.95; BTH.15.88 Eudendriidae Yes (1) Yes
9Eudendrium capillare BTH.15.80; BTH.15.82 Eudendriidae No Yes
10 Eudendrium carneum BTH.15.91; BTH.15.15; BTH.15.35 Eudendriidae Yes (3) Yes
11 Myrionema amboinense BTH.15.11 Eudendriidae No Yes
12 Ralpharia gorgoniae BTH.15.24 Tubulariidae Yes (1) Yes
13 Millepora alcicornis BTH.15.31 Milleporidae Yes (1) Yes
14 Millepora complanata Yes Not sampled. Milleporidae No No
15 Solanderia gracilis BTH.15.87 Solanderiidae Yes (1) Yes
16 Pennaria disticha BTH.15.23; BTH.15.90; BTH.15.96 Pennariidae Yes (3) Yes
17 Sphaerocoryne cf. agassizii BTH.15.40; BTH.15.79; BTH.15.69 Sphaerocorynidae Yes (2) Yes
18 Pteroclava krempfiBTH.15.78; BTH.15.81 Cladocorynidae Yes (1) Yes
19 Zanclea alba Yes Not Vouchered Zancleidae No Yes
20 Aglaophenia latecarinata BTH.15.20 Aglaopheniidae No Yes
21 Macrorhynchia grandis BTH.15.97 Aglaopheniidae No Yes
22 Antennella secundaria BTH.15.13; BTH.15.100; BTH.15.18 Halopterididae Yes (2) Yes
23 Halopteris alternata BTH.15.50; BTH.15.53; BTH.15.83; BTH.15.14 Halopterididae Yes (3) Yes
24 Kirchenpaueria halecioides BTH.15.1; BTH.15.5; BTH.15.47; BTH.15.21;
BTH.15.54
Kirchenpaueriidae Yes (2) Yes
25 Dentitheca dendritica BTH.15.101 Plumulariidae Yes (1) Yes
26 Plumularia margaretta BTH.15.42; BTH.15.51 Plumulariidae Yes (1) Yes
27 Plumularia floridana BTH.15.65 Plumulariidae Yes (1) Yes
28 Thyroscyphus marginatus BTH.15.26; BTH.15.29 Thyroscyphidae Yes (2) Yes
29 Thyroscyphus ramosus BTH.15.89 Thyroscyphidae Yes (1) Yes
30 Hincksella formosa BTH.15.39 Syntheciidae Yes (1) Yes
31 Dynamena crisioides BTH.15.7; BTH.15.9; BTH.15.33; BTH.15.73;
BTH.15.74
Sertulariidae Yes (4) Yes
32 Dynamena disticha BTH.15.32 Sertulariidae Yes (1) Yes
33 Sertularella diaphana BTH.15.109 Sertulariidae Yes (1) Yes
34 Sertularia rugosissima BTH.15.106; BTH.15.107 Sertulariidae No Yes
35 Sertularia marginata BTH.15.94 Sertulariidae Yes (1) Yes
36 Sertularia distans BTH.15.43 Sertulariidae Yes (1) Yes
37 Salacia desmoides BTH.15.16 Sertulariidae Yes (1) Yes
38 Gastroblasta raffaelei BTH.15.27; BTH.15.44; BTH.15.46; BTH.15.48;
BTH.15.49; BTH.15.55
Campanulariidae Yes (1) Yes
39 Clytia gracilis BTH.15.62 Campanulariidae No Yes
40 Clytia hemisphaerica BTH.15.36; BTH.15.37; BTH.15.41 Campanulariidae No Yes
41 Clytia linearis BTH.15.6; BTH.15.76; BTH15.68 Campanulariidae Yes (3) Yes
42 Clytia noliformis BTH.15.84 Campanulariidae No Yes
43 Clytia hummelincki BTH.15.62; BTH.15.67; BTH.15.72 Campanulariidae Yes (1) Yes
44 Obelia bidentata BTH.15.60; BTH.15.75 Campanulariidae Yes (1) Yes
45 Obelia dichotoma BTH.15.30?, BTH.15.19; BTH.15.34 Campanulariidae No Yes
46 Cirrholovenia tetranema BTH.15.66 Lovenellidae No Yes
47 Halecium cf. nanum BTH.15.45 Haleciidae Yes (1) Yes
48 Halecium tenellum BTH.15.70 Haleciidae No Yes
49 Halecium bermudense BTH.15.2, BTH.15.10 Haleciidae No Yes
50 Nemalecium lighti BTH.15.77; BTH.15.3; BTH.15.4; BTH.15.58 Haleciidae Yes (3) Yes
51 Cubaia aphrodite medusa BTH.15.105 Olindiidae No Yes
52 Liriope tetraphylla medusa BTH.15.63 Geryoniidae Yes (1) Yes
53 Persa incolorata medusa BTH.15.103 Rhopalonematidae No Yes
1 Filifera (on hermit Crab: ?
Turritopsoides)
BTH.15.102 ? Yes (1) No
2?Cytaeis sp. BTH.15.8 Cytaeididae No No
3Codonorchis sp. BTH.15.86 Pandeidae No Yes
4 Oceaniidae indet BTH.15.56 Oceaniidae No No
5 Oceaniidae indet BTH.15.59 Oceaniidae No No
6 Bougainvilliidae 2/Bimeria? BTH.15.98 Bougainvilliidae Yes (1) No
7 Bougainvilliidae/Bimeria? BTH.15.85 Bougainvilliidae Yes (1) No
8Stauridiosarsia nipponica BTH.15.93 Corynidae Yes (1) Yes
9Thecocodium sp. BTH.15.64 Ptilocodiidae Yes (1) No
10 Halecium cf. bermudense BTH.15.2 Haleciidae No No
11 Halecium sp. 1 BTH.15.57 Haleciidae Yes (1) No
12 Halecium sp. 2 BTH.15.38 Haleciidae Yes (1) No
(Continued)
108 M. P. MIGLIETTA ET AL.
Table 2. (Continued).
Species Voucher Name Family
Barcoding (n. of
sequences)
Taxon
Identification Table
13 Halecium sp. [sensu 17] BTH.15.52 Haleciidae Yes (1) No
14 Plumularia sp.1 BTH.15.22 Plumulariidae No No
15 Plumularia sp.2 BTH.15.12 Plumulariidae No No
16 Clytia sp. BTH.15.99 Campanulariidae Yes (1) No
17 Egmundella sp. (on Clytia
linearis)
BTH.15.71 Campanulinidae No Yes
Table 3. Updated checklist of the Hydrozoa of Bocas del Toro. The list includes species reported in Calder and Kirkendale [13],
and this paper. For the species in this paper, the voucher number is reported. At the bottom, taxa identified at the genus or
higher taxonomic level.
Family Species
Calder & Kirkerdale
[13] This paper
1 Pandeidae Amphinema dinema No BTH.15.61
2 Cordylophoridae Corydendrium parasiticum Yes No
3 Oceaniidae Turritopsis dohrnii No Yes
4 Oceaniidae Turritopsis sp. 1 No BTH.15.110
5 Oceaniidae Turritopsis sp. 4 No No
6 Oceaniidae Turritopsis nutricula Yes No
7 Oceaniidae Rhizogeton sterreri No BTH.15.108
8 Bougainvilliidae Bimeria vestita Yes No
9 Bougainvilliidae Bougainvillia ?pyramidata No BTH.15.104
10 Bougainvilliidae Parawrightia robusta Yes No
11 Bougainvilliidae Silhouetta uvacarpa Yes No
12 Stylasteridae Stylaster roseus Yes BTH.15.25; BTH.15.92
13 Eudendriidae Eudendrium bermudense Yes BTH.15.17; BTH.15.95; BTH.15.88
14 Eudendriidae Eudendrium capillare Yes BTH.15.80; BTH.15.82
15 Eudendriidae Eudendrium carneum Yes BTH.15.91; BTH.15.15; BTH.15.35
16 Eudendriidae Eudendrium sp., aff.album Yes No
17 Eudendriidae Myrionema amboinense Yes BTH.15.11
18 Tubulariidae Ectopleura mayeri Yes No
19 Tubulariidae Ralpharia gorgoniae Yes BTH.15.24
20 Tubulariidae Zyzzyzus calderi Yes No
21 Sphaerocorynidae Sphaerocoryne cf. agassizii No BTH.15.40; BTH.15.79; BTH.15.69
22 Sphaerocorynidae Sphaerocoryne bedoti Yes No
23 Cladocorynidae Pteroclava krempfiBTH.15.78; BTH.15.81
24 Corynidae Stauridiosarsia nipponica No BTH.15.93
25 Zancleidae Zanclea alba Yes Yes, Not vouchered.
26 Solanderiidae Solanderia gracilis Yes BTH.15.87
27 Pennariidae Pennaria disticha Yes BTH.15.23; BTH.15.28; BTH.15.90; BTH.15.96
28 Milleporidae Millepora alcicornis Yes BTH.15.31
29 Milleporidae Millepora complanata Yes No
30 Milleporidae Millepora squarrosa Yes No
31 Laphoeinidae Cirrholovenia tetranema Yes BTH.15.66
32 Haleciidae Halecium lightbourni Yes No
33 Haleciidae Halecium nanum Yes No
34 Haleciidae Halecium cf. nanum No BTH.15.45
35 Haleciidae Halecium tenellum Yes BTH.15.70
36 Haleciidae Halecium bermudense No BTH.15.2, BTH.15.10
37 Haleciidae Nemalecium lighti Yes BTH.15.77; BTH.15.3; BTH.15.4; BTH.15.58
38 Haleciidae Sagamihydra dyssymetra Yes No
39 Kirchenpaueriidae Kirchenpaueria halecioides Yes BTH.15.1; BTH.15.5; BTH.15.47; BTH.15.21; BTH.15.54
40 Plumulariidae Dentitheca dendritica Yes BTH.15.101
41 Plumulariidae Monotheca margaretta Yes BTH.15.42; BTH.15.51
42 Plumulariidae Plumularia floridana Yes BTH.15.65
43 Plumulariidae Plumularia setacea Yes No
44 Plumulariidae Plumularia strictocarpa Yes No
45 Halopterididae Antennella curvitheca Yes No
46 Halopterididae Antennella secundaria Yes BTH.15.13; BTH.15.100; BTH.15.18
47 Halopterididae Halopteris alternata Yes BTH.15.50; BTH.15.53; BTH.15.83; BTH.15.14
48 Halopterididae Halopteris carinata Yes No
49 Aglaopheniidae Aglaophenia dubia Yes No
50 Aglaopheniidae Aglaophenia latecarinata Yes BTH.15.20
51 Aglaopheniidae Macrorhynchia philippina Yes No
52 Aglaopheniidae Macrorhynchia grandis BTH.15.97
53 Thyroscyphidae Thyroscyphus marginatus Yes BTH.15.26; BTH.15.29
54 Thyroscyphidae Symmetroscyphus intermedius Yes No
55 Thyroscyphidae Thyroscyphus ramosus Yes BTH.15.89
56 Syntheciidae Hincksella formosa Yes BTH.15.39
57 Syntheciidae Synthecium tubithecum Yes No
58 Sertulariidae Diphasia tropica Yes No
(Continued)
NEOTROPICAL BIODIVERSITY 109
environmental assets and ecosystem health worldwide.
The present inventory of the marine hydrozoan fauna in
the Bocas del Toro shallow water is far to be exhaustive
due to the inherent limitation of our sampling efforts,
based mostly on snorkeling and more rarely on SCUBA
diving collections. However, the high number of
recorded taxa suggests that the Caribbean Sea should
be considered a region of high hydrozoan diversity.
Paradoxically, taxonomy is a science at brink of extinc-
tion. The ARTS courses have been devoted not only to
increase knowledge on local biodiversity, but towards
the conservation and promotion of biodiversity
Table 3. (Continued).
Family Species
Calder & Kirkerdale
[13] This paper
59 Sertulariidae Dynamena crisioides Yes BTH.15.7; BTH.15.9; BTH.15.33; BTH.15.73; BTH.15.74
60 Sertulariidae Dynamena disticha Yes BTH.15.32
61 Sertulariidae Dynamena quadridentata Yes No
62 Sertulariidae Sertularella cylindritheca Yes No
63 Sertulariidae Sertularella diaphana No BTH.15.109
64 Sertulariidae Sertularella hartlaubi Yes No
65 Sertulariidae Sertularia rugosissima No BTH.15.106; BTH.15.107
66 Sertulariidae Sertularia loculosa Yes No
67 Sertulariidae Sertularia marginata Yes BTH.15.94
68 Sertulariidae Tridentata subtilis Yes No
69 Sertulariidae Sertularia turbinata Yes No
70 Sertulariidae Sertularia distans No BTH.15.43
71 Sertulariidae Sertularia vervoorti Yes No
72 Sertulariidae Salacia desmoides No BTH.15.16
73 Campanulariidae Gastroblasta raffaelei No BTH.15.27; BTH.15.44; BTH.15.46; BTH.15.48; BTH.15.49;
BTH.15.55
74 Campanulariidae Clytia gracilis Yes BTH.15.62
75 Campanulariidae Clytia hemisphaerica Yes BTH.15.36; BTH.15.37; BTH.15.41
76 Campanulariidae Clytia linearis Yes BTH.15.6 ; BTH.15.76; BTH15.68
77 Campanulariidae Clytia paulensis Yes No
78 Campanulariidae Clytia stolonifera Yes No
79 Campanulariidae Clytia gracilis No BTH.15.62
80 Campanulariidae Clytia noliformis No BTH.15.84
81 Campanulariidae Clytia hummelincki No BTH.15.62; BTH.15.67; BTH.15.72
82 Campanulariidae Obelia bidentata Yes BTH.15.60; BTH.15.75
83 Campanulariidae Obelia dichotoma Yes BTH.15.30?, BTH.15.19; BTH.15.34
84 Olindiidae Cubaia aphrodite medusa No BTH.15.105
85 Geryoniidae Liriope tetraphylla medusa No BTH.15.63
86 Rhopalonematidae Persa incolorata medusa No BTH.15.103
Family Species Calder This paper
1 ? Filifera (on Hermit Crab) (?
Turritopsoides)
No BTH.15.102
2 Cytaeididae ?Cytaeis sp. No BTH.15.8
3 Pandeidae Codonorchis sp. No BTH.15.86
4 Cordylophoridae Rhizodendrium sp. Yes No
5 Oceaniidae Oceaniidae indet. No BTH.15.56
6 Oceaniidae Oceaniidae indet. No BTH.15.59
7 Bougainvilliidae Bougainvilliidae 2/?Bimeria No BTH.15.98
8 Bougainvilliidae Bougainvilliidae/?Bimeria No BTH.15.85
9 Bougainvilliidae Bougainvilliidae indet. Yes No
10 Eudendriidae Eudendrium sp. Yes No
11 Corynidae Coryne sp. Yes No
12 Corynidae Corynidae indet. Yes No
13 Zancleidae Zanclea sp. Yes No
14 Hydrocorynidae Hydrocoryne sp. Yes No
15 Ptilocodiidae Thecocodium sp. No BTH.15.64
16 Haleciidae Halecium cf. bermudense No BTH.15.2
17 Haleciidae Halecium sp. Yes No
18 Haleciidae Halecium sp. 1 No BTH.15.57
19 Haleciidae Halecium sp. 2 No BTH.15.38
20 Haleciidae Halecium sp. [sensu 17] No BTH.15.52
21 Haleciidae Hydranthea sp. Yes No
22 Plumulariidae Plumularia sp. No BTH.15.22
23 Plumulariidae Plumularia sp. No BTH.15.12
24 Campanulariidae Clytia sp., aff.kincaidi Yes No
25 Campanulariidae Clytia sp. No BTH.15.99
26 Campanulariidae Clytia sp. A Yes No
27 Campanulariidae Clytia sp. B Yes No
28 Campanulariidae Clytia sp. C Yes No
29 Campanulariidae Orthopyxis sp. Yes No
30 Halammohydridae Halammohydra sp. Yes No
31 Otohydridae Otohydra sp. Yes No
32 Campanulinidae Egmundella sp. (on Clytia linearis) No BTH.15.71
110 M. P. MIGLIETTA ET AL.
expertise. More generally, training a new generation of
taxonomists is a current challenge and a mandatory
urge to understanding ecosystem functioning in face
of local and global changes, and to address the needs of
sustainability of humankind activities.
Author contributions
MPM and S. Piraino designed the experiments; S. Pruski
produced the barcoding sequences, all authors collected
samples and contributed the Taxon Identification Tables:
MPM wrote the paper.
Acknowledgments
The authors would like to thank the National Science
Foundation for funding. We would also like to thank the
staffat the Smithsonian Tropical Research Institute’s Bocas
del Toro Research Station for their support and help during
the 2015 taxonomy course, the Panamanian Ministry of the
Environment (MiAmbiente) for permission to conduct this
research, and two anonymous reviewers for their useful
comments.
Associate Editor: Federico Brown
Disclosure statement
No potential conflict of interest was reported by the
authors.
Funding
This study was funded by the National Science Foundation
ARTS grant number DEB-1456501 to MPM and DEB-1456674
to RC, the Texas Sea Grantnumber 02-S170210 and the
Texas A&M Pesca Grant to MPM.
ORCID
Maria Pia Miglietta http://orcid.org/0000-0002-9458-593X
Stefano Piraino http://orcid.org/0000-0002-8752-9390
Magdalena Alpizar Gonzalez http://orcid.org/0000-0003-
1277-5527
Sarai Jerónimo-Aguilar http://orcid.org/0000-0001-8556-
8663
Jonathan W. Lawley http://orcid.org/0000-0003-1267-
5294
Davide Maggioni http://orcid.org/0000-0003-0508-3987
Luis Martell http://orcid.org/0000-0002-7062-8915
Yui Matsumoto http://orcid.org/0000-0001-9942-9330
Pooja Nagale http://orcid.org/0000-0002-2319-4675
Sornsiri Phongphattarawat http://orcid.org/0000-0002-
6776-8570
Carolina Sheridan http://orcid.org/0000-0001-5881-8057
Joan J. Soto Àngel http://orcid.org/0000-0002-9132-4822
Rachel Collin http://orcid.org/0000-0001-5103-4460
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