Short Communication |
Corresponding author: Raffael Ernst ( raffael.ernst@senckenberg.de ) Academic editor: Robert Colautti
© 2019 Franziska Leonhardt, Juan David Jimenez-Bolaño, Raffael Ernst.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Leonhardt F, Jimenez-Bolaño JD, Ernst R (2019) Whistling invaders: Status and distribution of Johnstone’s Whistling frog (Eleutherodactylus johnstonei Barbour, 1914), 25 years after its introduction to Colombia. NeoBiota 45: 39-54. https://doi.org/10.3897/neobiota.45.33515
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Despite increased attention to the problem of alien amphibian invasions, systematic assessments of the actual invasion status and potential, required to estimate possible environmental and economic impacts of introduced species, are often missing. A prime example is Johnstone’s Whistling Frog (Eleutherodactylus johnstonei), a Caribbean native that now occurs widely throughout the South American mainland, including Colombia. We conducted the first systematic and comprehensive countrywide assessment of the introduction status of the species in Colombia, combining both intensive field surveys, as well as a first population genetic analysis. The species was strictly confined to urban habitats with specific environmental conditions (plant nurseries and private gardens) and did not show any signs of dispersal into the extra-urban matrix. Genetic data support previously hypothesised independent introduction events in the Andes and along the Caribbean Coast and shed light on potential dispersal pathways. The results of this study challenge both the active spread, as well as the broad environmental tolerance hypothesis previously suggested, to explain the observed range extension. A critical reassessment of the categorisation of the species as highly invasive under IUCN-ISSG standards is required.
Anura, alien amphibians, Colombia, distribution, disturbed areas, invasion status, new records, population genetics
Johnstone’s Whistling Frog, Eleutherodactylus johnstonei Barbour, 1914, a native of the Lesser Antilles, presumably St. Lucia or the northern Lesser Antilles (
Given this broad distribution (Fig.
Global (country-level) distribution of Eleutherodactylus johnstonei. Black, Presumed native range (A or B); grey, introduced range (1–13). A St Maarten/St Martin, Saba, St Eustatius, St Kitts and Nevis, Antigua (
Amongst all countries, to which E. johnstonei has been introduced successfully, Colombia deserves special attention because of the comparatively long introduction history and the large number of populations reported to have established in different parts of the country. In the present study, we provide the first systematic and comprehensive countrywide assessment of the introduction status of E. johnstonei in Colombia. Known populations are reassessed and additional localities are investigated for the occurrence of the target species. For the first time, we assessed the species’ population genetic structure in Colombia. We subsequently discuss the geographic distribution pattern in the light of the controversy surrounding the actual invasion potential of the species in Colombia and finally provide an outlook for future research directions.
To assess the countrywide distribution of E. johnstonei, we conducted opportunistic surveys, covering natural urban peripheral and urban areas, in all major biogeographic regions (Caribbean, Andean, Pacific, Orinoco and Amazonas region; Fig.
Presence-absence and haplotype distribution (A) and network (B) for Eleutherodactylus johnstonei in Colombia. A Small symbols: circles = urban areas; triangles = natural areas; filled symbols = presence, blank symbols = absence. White labels encode major geographic regions based on affiliation of administrative regions (www.colombia.com/colombia-info/informacion-general/geografia/regiones/): CA, Caribbean region; AD, Andean region; PC, Pacific region; OQ, Orinoco region; AM, Amazonas region. Black labels encode cities with presence of E. johnstonei: SM, Santa Marta; BQ, Barranquilla; CG, Cartagena; BG, Bucaramanga; MD, Medellín; MQ, Mariquita; IB, Ibague; CH, Fusagasuga-Chinauta; CL, Cali. Large coloured circles present haplotype frequencies at sampled localities. Orange: Ht1, red: Ht2, yellow: Ht3; circle sizes refer to numbers of samples at each locality as illustrated in inlet B Haplotype network based on the Integer-Neighbour-Joining Network implemented in POPART (
Occurrence data (presence-absence) in both urban and pristine areas were acquired through opportunistic visual and acoustic encounter surveys (VES and AES, following
Systematic surveys in the nine urban focus areas were undertaken between June and August 2017 and in March 2018, thus covering both wet and dry season periods. We pre-selected at least two urban districts per focus area, in which two of us (FL and JDJB) conducted standardised VES and AES (following
A total of 69 tissue samples from all sampled localities were used to generate mitochondrial (mt) haplotypes from partial sequences of 12S rRNA and D-loop regions, two established mt-markers previously used for population genetic and phylogeographic analyses in congeneric species (
The first published record of E. johnstonei for Colombia dates back to 1992. The species was reported for Barranquilla (
The presence of E. johnstonei was confirmed for three out of the five major geographic areas in Columbia. These include the costal lowlands of the Caribbean region and the Eastern, Central and Western Andes within the Andean and the Pacific Region. Unlike previous reports, these records are based on multiple evidence (visual, acoustic and voucher records). We could not find any evidence for the presence of the target species along the Pacific coast and in the Amazon and Orinoco region. Moreover, opportunistic VES and AES did not yield records outside of urban areas in any of the investigated regions throughout Colombia (see Fig.
12S rRNA mitochondrial marker sequences (360 bp, partial sequence) did not show any variation amongst the 69 samples collected across the entire Colombian distributional range. However, a clear differentiation existed in respective D-loop sequences (249 bp, partial sequence). Nucleotide diversity amongst the 48 individuals, for which sequences could be generated, amounted to 0.46% with a maximum of three variable sites, revealing three distinct haplotypes (Ht, see Table
Haplotype distribution at sampled localities. N, number of individuals sampled per locality, haplotype (Ht) diversity and haplotype frequencies at each locality.
Locality | N | Haplotype diversity | Haplotype frequency | ||
---|---|---|---|---|---|
GGT (Ht1) | GGC (Ht2) | AAT (Ht3) | |||
Barranquilla | 10 | 0.18 | 0.1 | 0.9 | |
Cartagena | 10 | 0 | 1.0 | ||
Santa Marta | 3 | 0.67 | 0.33 | 0.67 | |
Bucaramanga | 5 | 0 | 1.0 | ||
Medellin | 5 | 0 | 1.0 | ||
Ibagué | 5 | 0 | 1.0 | ||
Cali | 5 | 0 | 1.0 | ||
Fusgasugá | 5 | 0 | 1.0 | ||
Total | 48 | 0.61 | 0.52 | 0.25 | 0.23 |
Roughly 25 years after its introduction to Colombia, E. johnstonei has managed to establish populations in nine different urban areas, ranging from the Caribbean Coast at almost sea level to the Andes at altitudes of more than 1,700 m a.s.l. Climatic conditions in these newly colonised localities vary significantly and comprise arid to semi-arid as well as tropical wet environments. Mean annual temperatures range from as low as 19.4 °C (Fusagasugá, 1,717 m a.s.l.) to as high as 28.3 °C (Santa Marta, 12 m a.s.l.).
This broad environmental gradient implies a significant environmental tolerance and, in combination with the comparatively wide geographic distribution across the country, it appears to corroborate results from macroecological models predicting significant future range extensions (
However, this macro-perspective is misleading. A rather different interpretation suggests itself, when considering small-scale spatial patterns and local environmental features obtained from field surveys. A look at the spatial pattern of distribution reveals markedly disjunct distributions at larger geographic scales (countrywide distribution) that are recursively replicated at smaller geographic scales (within cities). This pattern confirms earlier findings suggesting human facilitated jump dispersal (
A prevalence for site tenacity and very small home ranges d (≤ 2 m in diameter) has previously been shown in a study on long-term and nightly movement patterns in E. johnstonei in Barbados (
We therefore conclude that the active invasion potential seems to be very limited and distributional extensions are rather determined by the availability and frequency of passive transportation mediated by human transport.
When considering site-specific attributes, a second non-random pattern emerges that challenges both the active spread as well as the broad environmental tolerance hypothesis. Again this pattern is somewhat recursive as it can be observed at two spatial scales. At the country level, E. johnstonei is restricted to urban or disturbed urban peripheral areas as previously reported from countries outside the native range (e.g.
Overall, our results are in line with studies that report E. johnstonei exclusively from non-natural, urban areas in Colombia (e.g.
Despite obvious limitations with respect to genetic sample sizes (N = 69/48), as well as limited choice of molecular markers (two different markers covering a total of 609 bp) that prove to be applicable in the current analytical framework, we were able to retrieve first informative patterns describing the population genetic setup of the Colombian populations under investigation. The macro-scale pattern (coastal vs. hinterland populations) is likely to prove robust and should be confirmed in future studies. With only 0.46% nucleotide divergence and only three variable sites recovered, the overall genetic diversity amongst the Colombian populations is much lower than expected, based on the limited data available from studies on congeneric frog species from the Caribbean that used similar markers (
The observed geographic distribution of D-loop haplotypes (see Figure
The results of our study underscore the need to critically reassess the actual distribution status and dispersal potential of Johnstone’s Whistling Frog in its non-native range and re-evaluate the current classification as an extensively spreading invasive amphibian species. Both the observed historic dispersal patterns revealed through a first population genetic assessment of the Colombian populations, as well as the actual present distributional patterns retrieved through intense field surveys, challenge available model predictions that are based on macro-ecological descriptors and coarse-scale climatic variables. Based on the two lines of evidence (molecular and field-data) provided in this study, we consider the current risk of further range extensions into natural or even ex-urban areas as very low but recommend intensified surveys in non-urban areas. In keeping with
Permission for fieldwork was given by the government of Colombia, Ministry of Environment and Sustainable Development, through resolution no. 0255 (permiso marco otorgado a la UNC de recolección de especímenes de especies silvestres de la diversidad biológica con fines de investigación científica no comercial para la asignatura ‘Conservación genética’). Export of genetic samples was authorised by the Colombian “Autoridad Nacional de Licancias Ambientales” under reference number 2018060578-2-000. We are particularly indebted to M. Vargas-Ramírez for his help in obtaining permission, as well as for providing logistic support during fieldwork. We especially like to thank all local partners who granted access to their private properties. Without this support, fieldwork would not have been possible. C. Kehlmaier, A. Müller and H. Stuckas significantly supported the lab work and helped with primer design. We thank D. Escoriza and W. Dawson for their valuable comments on our manuscript.
Table S1
Data type: occurence
Explanation note: Presence-absence data for Eleutherodactylus johnstonei in Colombia.