Leptodactylus fragilis in San Andrés

ANARTIA

Publicación del Museo de Biología de la Universidad del Zulia

ISSN 1315-642X (impresa) / ISSN 2665-0347 (digital)

Anartia, 32 (junio 2021): 61-66

On a second invasive frog (Anura: Leptodactylidae) from San

Andrés, Colombian Caribbean islands

Sobre la segunda rana invasora (Anura: Leptodactylidae) de San Andrés, Caribe

insular colombiano

María Victoria Cubillos-Abrahams1, 2 & Andrés Camilo Montes-Correa2, 3

1Grupo de Investigación en Ecología Neotropical (GIEN), Universidad del Magdalena, Santa Marta, Magdalena, Colombia.

mavcubillos@gmail.com

2Fundación GECOS, Santa Marta, Magdalena, Colombia.

2Grupo de Investigación en Manejo y Conservación de Fauna, Flora y Ecosistemas Estratégicos Neotropicales (MIKU),

Universidad del Magdalena, Santa Marta, Magdalena, Colombia. andresc.montes@gmail.com

(Received: 17-07-2021 / Accepted: 28-09-2021 / Online: 15-10-2021)

with an iso-megathermal warm climate and unimodal ra-

infall regime (rainfall season from May to November, the

driest periods from March to April, Vargas-Cuervo 2004).

e natural ecosystems of San Andrés include tropical dry

and mangroove forests, but the predominant coverage are

small remnants of the original forest, surrounded by pastu-

res, crops, and shrubs (Caicedo-Portilla 2014).

e herpetofauna of San Andrés has been previously

documented with a list of 19 terrestrial species (17 reptiles

and two anurans; Dunn 1945, Dunn & Saxe 1950, Tam-

sitt & Valdivieso 1963, Valdivieso & Tamsitt 1963, Mc-

Nish 2011, Cubillos-Abrahams et al. 2021). e potential

origin of the island species was recently summarized by

Cubillos-Abrahams et al. (2021). Before this publication,

the only species of frog documented in San Andrés in li-

terature and museums was Leptodactylus insularum Bar-

bour, 1906. Nevertheless, Eleutherodactylus planirostris

(Cope, 1862) was documented for the rst time in 2018

(Cubillos-Abrahams et al. 2021). A recent expedition to

San Andrés (March and June 2021) found hundreds of a

leptodactylid frog that did not correspond to the native

species L. insularum. A detailed examination of speci-

mens and advertisement calls allowed us to identify them

as the white-lipped thin-nger frog, Leptodactylus agilis

(Brocchi, 1877), a widely distributed species, ranging from

southern to northern South America (Heyer et al. 2006,

Mendez-Narváez et al. 2009) and recently reported as

Islands are optimal model systems to understand evo-

lutionary processes such as colonization, speciation, and

extinction. eir size and distance to the continent are key

factors that shape island biodiversity (Zunino & Zullini

2003, Whittaker & Fernández-Palacios 2007). Human

have aided the displacement of species to localities that

could have otherwise not taken place through natural dis-

persal across geographical barriers (Ríos & Vargas 2003).

Invasive species, particularly in islands, can cause signi-

cant ecological changes in the trophic web structure and

habitat composition, including severe impacts on native

species and ecosystems (Gutiérrez-Bonilla 2006). Invasive

species are included among the severe threats that habi-

tats face (i.e., overexploitation of natural resources, urban

development, pollution, ecosystem modication, among

others; see Russel & Kueer 2019).

e Archipiélago de San Andrés, Providencia, and San-

ta Catalina (Colombian Caribbean islands) is part of the

Western Caribbean, an insular ecoregion recognized by its

high diversity and endemicity (Hedges et al. 2019). Among

the Colombian Caribbean islands, San Andrés is a coral

reef island, which is the largest, most diverse, and more

impacted by anthropogenic disturbance (Caicedo-Portilla

2014). is is located 483 km northwest of the Colombian

Caribbean coast and 190 km east of the Caribbean coast of

Central America (Fig. 1). e island is part of the dry tro-

pical zonobiome (Hernández-Camacho & Sánchez 1992),

DOI: https://doi.org/10.5281/zenodo.5571321

M. V. Cubillos-Abrahams & A. C. Montes-Correa

an introduced species to Cuba (Rodríguez-Cabrera et al.

2018). In Colombia, the species is distributed on the con-

tinental Caribbean lowlands, inter-Andean valleys, and

the western portion of the Orinoquian savannahs (Acosta-

Galvis 2021). Here, we report for the rst time the presen-

ce of the white-lipped thin-nger frog L. agilis from San

Andrés, in the Colombian Caribbean islands. In addition,

we report and describe some aspects of the species natural

history in San Andres.

Leptodactylus agilis was recorded at seven localities

in the central area of the island. All the localities are part

of semi-rural to rural areas characterize by the presence

of forest remnants, shrubs, pastures, and build-up areas.

Taxonomic determination was initially based on the di-

chotomous key of Cuentas et al. (2002) for the anurans

of northern Colombia. Subsequently, the identity of the

species was conrmed by verifying the descriptions by

Heyer et al. (2006) and de Sá et al. (2014). Specimens co-

llected were euthanized following the ASIH guidelines

using a chemical anesthetic, later xed in a formalin solu-

tion (10%) and nally maintained in alcohol (70%). All

vouchers are deposited at the amphibian collection of the

Centro de Colecciones Cientícas at the Universidad del

Magdalena (CBUMAG), Santa Marta, Colombia, with

the following collection numbers: CBUMAG: ANF:

01188-89, 01199-201, 01203-04.

Figure 1. Geographic distribution of Leptodactylus agilis, based on occurrences from GBIF (2021), the extent of occurrences (EOO)

from UICN Red List (Heyer et al. 2010), and the recent record from Cuba by Rodríguez-Cabrera et al. (2018).

Leptodactylus fragilis in San Andrés

Herein, we report the new records of Leptodactylus a-

gilis: Colombia, departamento Archipiélago de San An-

drés, Providencia y Santa Catalina: San Andrés (Fig.1):

Los Corales (12°33’43.7” N, 81°42’43.4” W, 21 m asl.;

CBUMAG: ANF: 01188-89 [Fig. 2A], CBUMAG:

ANF: 01199-201), buer zone of Old Point Mangrove

Regional Park (12°33’42.4” N, 81°42’ 29.7” W, 4 m asl.),

Jack Pond (12°33’05.3” N, 81°43’07.9” W, 50 m asl.), Big

Pond (12°32’55.4” N, 81°43’12.5” W, 44 m asl.; CBU-

MAG: ANF: 01203-04), Duppy Gully (12°32’23.5” N,

81°43’15.2” W, 32 m asl.), Manuel Pond (12°32’06.8” N,

81°43’14.5” W, 32 m asl.), and Botanical Garden of San

Andrés (12°32’13.9”N, 81°42’40.5” W, 28 m asl.). At

these new localities, specimens were found sharing their

habitat with E. planirostris and L. insularum in pastures,

pond shores, tropical dry and mangrove forests edges. In

San Andres, the species is found on dierent substrates,

i.e., mud, leaf-litter, wet grasses, roots, bare soil, and cattle

footprints and droppings. Leptodactylus agilis vocalizes

throughout all the night, but apparently, the peak of vo-

calizations is in the early hours (19:00–21:00 h). e ad-

vertisement calls of L. agilis was so deafening that gene-

rally we did not hear advertisement calls of L. insularum.

In fact, the species was abundant and exceeding by far L.

insularum in all localities.

We found hundreds of individuals in the surroundings

of water sources such as Jack Pond, Manuel Pond, and Big

Pond, the latter is permanent pond. Seasonal water bodies

are heavily sedimented and have a large mass of oating

macrophytes (Pistia stratiotes), which almost completely

cover the muddy lake beds exposed during the dry season.

is seems to be an important microhabitat for L. agi-

lis, although it was also frequently found in the leaf-litter

of remnants vegetation surrounding the water bodies. In

localities without ponds, such as the Botanical Garden of

San Andrés, Los Corales, and the buer zone of Old Point

Regional Park, the specimens gathered in humid shelters,

e.g., wet surfaces due to water leaks, irrigation zones, drai-

nage gutters, greenhouses, and gardens. During rainy days,

specimens were found at the edges of tropical dry forest.

We recorded the reproductive activity of Leptodactylus

agilis from the beginning to the end of the eldwork

period. We heard the advertisement call and found foam

nests with tadpoles in the driest time of the year (March to

April). Foam nests were deposited in humid cavities at the

oor level (Fig. 2B), under fallen logs, boards, boulders,

and coral rocks, which were not in direct contact with wa-

ter. We observed parental care in four foam nests that in-

volves the males sitting next to the nest within the burrow.

Specimens were identied as Leptodactylus agilis

by the following combination of characters (Heyer et al.

2006, de Sá et al. 2014): relatively small size (maximum

size in snout-vent length [SVL]: 44 mm in females, 43 mm

in males), head longer than wide, spatulated snout, bulging

in lateral view and rounded canthus rostralis. Two to four

longitudinal folds, two weak dorsolateral and two discon-

tinuous lateral. Lateral fringes of toes absent. All speci-

mens had a white stripe on the upper lip and a dark su-

pratympanic fold. Two lateral vocal sacs, from pigmented

grayish to heavily dark. Leptodactylus agilis is easily dis-

tinguished from L. insularum (morphological characters

of L. insularum in parenthesis) by its considerable smaller

size (maximum size 120 mm SVL), snout shape spatula-

ted, rounded in lateral view (not spatulated), absence of

lateral fringes in toes (lateral fringes present), and the pai-

red lateral vocal sacs (single subgular vocal sac). Likewi-

se, L. agilis can be distinguished from Eleutherodactylus

planirostris (morphological characters of E. planirostris in

parenthesis) by a considerably larger size (maximum size:

23.2 mm SVL) and the absence of digital ornamentation

(lateral fringes present, digital discs slightly expanded and

truncated, with pads and circumferential groove).

Figure 2. Adult specimen (A, CBUMAG: ANF: 1189) and

foam nest (B) of Leptodactylus agilis from Los Corales, San

Andrés, Colombia.

M. V. Cubillos-Abrahams & A. C. Montes-Correa

e record of L. agilis in San Andrés represents the

third known anuran, the second invasive frog species,

and the ninth non-native herp documented from the

Colombian Caribbean islands (Cubillos-Abrahams et

al. 2021). Leptodactylus agilis is a very adaptable spe-

cies with a high invasive potential in San Andrés (and

other Caribbean islands, see Rodríguez-Cabrera et al.

2018), since as suggested by its high relative abundance

(0.81 individuals/hours/observers, Cubillos-Abrahams

& Montes-Correa, unpublished data). Given that this

species can reproduce even in the driest season (i.e. using

articial water sources, the small remnants of seasonal

water bodies, or the only one permanent pond), we assu-

me that the species could have a continuous reproductive

cycle throughout the year. e latter is rare in amphi-

bians found in tropical dry forests in northern Colom-

bia, which exhibit explosive breeding events mediated by

the availability of water resources (Vargas-Salinas et al.

2019). e reproductive cycle of L. agilis appears to be

somewhere between a prolonged and explosive breeding

pattern (sensu Wells 2007, Vargas-Salinas et al. 2019),

because reproductive activity was extended throughout

the study (from the driest season to the beginning of ra-

infalls), frogs densely gathered in reproductive habitats

of variable stability (both temporary to permanent water

bodies or humid shelters), and males vocalized perma-

nently every night at all sampling sites.

e response of amphibians to water scarcity in tropical

dry forest depends on a constant interaction of physiologi-

cal, ecological, and behavioral strategies (Urbina-Cardona

et al. 2014). Five ecological and behavioral strategies of

tropical dry forest frogs from northern Colombia were

described to tolerate desiccation in dry periods (Cuentas

et al. 2002), two active strategies (horizontal and vertical

movements towards microhabitats with optimal humidi-

ty) and three passive ones (staying in water bodies or hu-

mid shelters, and estivation). According to Cuentas et al.

(2002), L. agilis remains in the surroundings of water bo-

dies, and they did not obtain records of the species during

prolonged dry periods (which could suggest that there is

a process of estivation). However, we found specimens of

L. agilis at the time of maximum drought densely grou-

ped around permanent water bodies, in the wet mud of

seasonal water bodies, and in humid areas not necessarily

related to the presence of water bodies. erefore, it seems

that L. agilis displays a wide range of ecological and beha-

vioral responses to desiccation, which could be inuenced

by the variation of climatic conditions both in natural and

non-native distribution area. Laying eggs in a foam nest

is a Leptodactylus frog trait that improves tadpole survi-

val against desiccation, a common threat in tropical dry

forests, and even in South temperate areas (among other

functions, see Gould 2021). Terrestrial and underground

foam nests were previously considered as a synapomorphic

character for the Leptodactylus fuscus species group, but

recognition of the derived or primitive condition for the

genus Leptodactylus depends on the discovering what kind

of nesting prevails in the members of the genus Hydrolae-

tare (Heyer 1969, see de Sá et al. 2014). is reproduc-

tive mode can provide adaptive advantages compared to

species (like L. insularum) that lay their eggs on the water

surface (Gould 2021).

e invasive populations of L. agilis in San Andrés

show high abundance, ecological tolerance to multiple ha-

bitats, and reproduce successfully in all sites where it was

recorded. For all the above, we consider that the invasive

population of this species in San Andrés is in the “spread

stage” (category D2) according to the framework for bio-

logical invasions proposed by Blackburn et al. (2011). is

stage is assigned to self-sustaining non-native populations

which survive and reproduce at a signicant distance from

the original point of introduction. In the non-native popu-

lation of L. agilis stablished in Cuba (Rodríguez-Cabrera

et al. 2018), the invasion is at an intermediate stage (bet-

ween establishment and dispersal stages sensu Blackburn et

al. 2011). Although the species may be locally abundant,

it has not dispersed enough to increase its extent of occu-

rrence signicantly. On the other hand, the extent of oc-

currence of L. agilis in San Andrés (2.68 km2) occupies

22.3% of the total area of the island, and it is likely that

this is greater than documented here. erefore, it is evi-

dent that the invasive potential of L. agilis is greater in

small islands.

Future research is critically need it to understand the

ecological aspects of L. agilis and how it shares its eco-

logical niche with the native L. insularum, to determine if

the apparent reproductive advantages and greater relative

abundance of L. agilis may threaten the survival of L. in-

sularum in San Andrés. Similarly, it is important to assess

if the invasion of L. agilis has any eect on the acoustic

niche of L. insularum, as estimated in Cuba with the en-

demic toad Peltophryne empusa Cope, 1862 (del Castillo-

Domínguez et al. 2021). In the same way, genetic studies

are required to determine the origin of this invasive L.

agilis population. Cuban population of L. agilis is the

product of a recent invasion from northern South Ame-

rica facilitated by trade between the countries of Cuba

and Venezuela (Rodríguez-Cabrera et al. 2018). Since San

Andrés is a free port and receives merchandise from mul-

tiple Central American countries, as well as continental

Colombia, the populations of L. agilis could come from

almost anywhere in their natural distribution range.

Leptodactylus fragilis in San Andrés

ACKNOWLEDGMENTS

is study is a preliminary result of the project “¿Cómo

es la vida en un paraíso tropical? Ecología de la herpetofau-

na terrestre de San Andrés, islas del Caribe colombiano”,

which was subscribed as the degree project of MVCA

at Universidad del Magdalena. Collection activities are

supported by framework permit for specimen collection

of the Universidad del Magdalena, granted in resolution

1293 (2014) of the Autoridad Nacional de Licencias Am-

bientales (ANLA). anks to the Abrahams family, Gus-

tavo Baker, and Benigno Yépez for allowing us to conduct

eldwork at their homes. We are grateful to Jairo Medina

and Rafael Mora for their logistic support at the Botani-

cal Garden of San Andrés. Special mentions go to Carlos

Hawkins, Daniela Chaparro, Michelle Navarro, Mauricio

Cabrera, Natalia Uribe, and Benigno Yépes for their led

assistance. anks to Jhulyana López-Caro and Liliana Sa-

boyá-Acosta for her comments on an early version of our

manuscript and perform the Figure 1, respectively. We are

very grateful to Roberto Guerrero Flórez by receiving and

safeguarding the specimens collected during the execution

of this project at the Centro de Colecciones Cientícas

de la Universidad del Magdalena. We nally thank three

anonymous reviewers for helping us to improve a prelimi-

nary version of this note with their valuable suggestions

and corrections.

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