Research Article |
Corresponding author: Frédéric Grandjean ( frederic.grandjean@univ-poitiers.fr ) Academic editor: Aaron Bauer
© 2020 Michel Breuil, David Schikorski, Barbara Vuillaume, Ulrike Krauss, Matthew N. Morton, Elizabeth Corry, Nicolas Bech, Mišel Jelić, Frédéric Grandjean.
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:
Breuil M, Schikorski D, Vuillaume B, Krauss U, Morton MN, Corry E, Bech N, Jelić M, Grandjean F (2020) Painted black: Iguana melanoderma (Reptilia, Squamata, Iguanidae) a new melanistic endemic species from Saba and Montserrat islands (Lesser Antilles). ZooKeys 926: 95-131. https://doi.org/10.3897/zookeys.926.48679
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The Lesser Antilles, in the Eastern Caribbean, is inhabited by three Iguana species: the Lesser Antillean iguana Iguana delicatissima, which is endemic to the northernmost islands of the Lesser Antilles, the introduced common iguana from South America, Iguana iguana iguana, represented also by the two newly described endemic subspecies Iguana iguana sanctaluciae from Saint Lucia and Iguana iguana insularis from Saint Vincent and the Grenadines, and Grenada, and the introduced Iguana rhinolopha from Central America. Drawing on both morphological and genetic data, this paper describes the Iguana populations from Saba and Montserrat as a new species, Iguana melanoderma. This species is recognized on the basis of the following combination of characteristics: private microsatellite alleles, unique mitochondrial ND4 haplotypes, a distinctive black spot between the eye and tympanum, a dorsal carpet pattern on juveniles and young adults, a darkening of body coloration with aging (except for the anterior part of the snout), a black dewlap, pink on the jowl, the high number of large tubercular nape scales, fewer than ten medium sized–triangular dewlap spikes, high dorsal spikes, and lack of horns on the snout. This new melanistic taxon is threatened by unsustainable harvesting (including for the pet trade) and both competition and hybridization from escaped or released invasive alien iguanas (I. iguana iguana and I. rhinolopha) from South and Central America, respectively. The authors call for action to conserve Iguana melanoderma in Saba and Montserrat and for further research to investigate its relationship to other melanistic iguanas from the Virgin Islands and coastal islands of Venezuela.
Conservation Biology, Iguana, Lesser Antilles, microsatellites, mtDNA, new endemic species, phylogeny
In the 1960s,
Geographical distribution of the three iguana groups identified by
Morphological studies of the St. Lucia Iguana, belonging to the third group of
In Saba, the local iguana, the Saban Black Iguana is considered as a flagship species. In Montserrat, the local melanistic iguana does not receive special attention due to its putative exotic origin. The two flagship herp species for conservation on the island are the mountain chicken (Leptodactylus fallax) and the Galliwasp (Diploglossus montiserrati).
Melanistic iguanas phenotypically close to those of Saba-Montserrat also occur in the northern islands (St. Croix, St. Thomas: USA Virgin Islands, USVI) and also on the island of Margarita and other coastal islands such as Los Roques and La Banquilla (Venezuela) (
The extension of the range of the Common Green Iguana from Central America, considered by
The paper aims to describe the common melanistic iguanas from the islands of Saba and Montserrat as a new taxon and to establish its relationships with other Common Green Iguanas. An outcome of this study will be the enabling of conservationists to accurately differentiate this endemic lineage from invasive iguanas and investigate its ecology and biology population on these two very small islands that are subject to a range of environmental disturbances including hurricanes, earthquakes and volcanic eruptions.
Morphological, molecular (i.e., mitochondrial and microsatellites markers) and biological data were used to compare the iguanas of Saba and Montserrat with Iguana iguana (South America), Iguana rhinolopha (Central America), and the two new subspecies I. iguana insularis and I. iguana sanctaluciae from southern Lesser Antilles (
The morphological traits used to identify iguanas are described in
We also reviewed photographs of Iguana found on the Internet using the Google Images search engine for the islands of St. Croix, St. Thomas (US Virgin Islands), for the coastal islets of Venezuela and for the vicinity of Cumana (Venezuela), regions known to be inhabited by melanistic iguanas, in relation to published data.
Collection and preparation of genetic material
Genomic DNA was isolated from 44 individuals from tissue, shed skin and/or blood samples using the QIAamp DNA Mini Kit (QIAGEN, Deutschland) and following the manufacturer’s recommendations (Table
Sampling and haplotype information. The effectives in the locality column correspond to the number of individuals studied for the microsatellites and the mitochondrial ND4 gene. The number in the ND4 column is the length of the sequence used in the analysis. SabaNP, Saba National Park. SBHNR, Saint Barthélemy Natural Reserve. DWCT, Durrell Wildlife Conservation Trust.
Locality/Status | Microsatellites | ND4 | Collectors | GenBank |
---|---|---|---|---|
Saba (N = 7/N = 6) | SABA01 | SABA01 (888) | SabaNP/SBHRN | MN590163 |
SABA02 | SABA02 (890) | SabaNP/SBHRN | MN590164 | |
SABA03 | SABA03 (739) | SabaNP/SBHRN | ||
SABA04 | SABA04 (892) | SabaNP/SBHRN | MN590165 | |
SABA05 | SABA05 (892) | SabaNP/SBHRN | MN590166 | |
SABA06 | SABA06 (892) | SabaNP/SBHRN | MN590167 | |
SABA07 | SABA07 (891) | SabaNP/SBHRN | MN590168 | |
Montserrat (N = 12/N = 4) | IGU86 | E. Corry DWCT | ||
IGU87 | E. Corry DWCT | |||
IGU88 | IGU88 (713) | E. Corry DWCT | MN590169 | |
IGU89 | IGU89(711) | E. Corry DWCT | MN590170 | |
IGU90 | E. Corry DWCT | |||
IGU91 | E. Corry DWCT | |||
IGU92 | IGU92(713) | E. Corry DWCT | MN590171 | |
IGU93 | IGU93(713) | E. Corry DWCT | MN590172 | |
IGU94 | E. Corry DWCT | |||
IGU95 | E. Corry DWCT | |||
IGU96 | E. Corry DWCT | |||
IGU99 | E. Corry DWCT | |||
St. Lucia /End (N 13/N = 2) | IGU58 | IGU63(779) | St. Lucia authors | MK687397 |
IGU59 | St. Lucia authors | |||
IGU60 | St. Lucia authors | |||
IGU61 | St. Lucia authors | |||
IGU62 | St. Lucia authors | |||
IGU63 | IGU63(737) | St. Lucia authors | MK687398 | |
IGU64 | St. Lucia authors | |||
IGU67 | St. Lucia authors | |||
IGU68 | St. Lucia authors | |||
IGU69 | St. Lucia authors | |||
IGU70 | St. Lucia authors | |||
IGU71 | St. Lucia authors | |||
IGU72 | St. Lucia authors | |||
Grenadines/End (N = 4/N = 4) | IGU73 | J. Daltry/G. Gaymes | MK787400 | |
IGU75 | J. Daltry/G. Gaymes | MK787401 | ||
IGU76 | J. Daltry/G. Gaymes | MK787403 | ||
IGU77 | J. Daltry/G. Gaymes | MK787404 | ||
Guiana/auto (N = 7/N = 4) | IGU78 | IGU78 (702) | F. Catzefis (CNRS) | MK687405 |
IGU79 | IGU79 (593) | F. Catzefis (CNRS) | MK687406 | |
IGU80 | F. Catzefis (CNRS) | |||
IGU81 | B. de Thoisy (Pasteur) | |||
IGU82 | IGU82 (712) | B. de Thoisy (Pasteur) | MK687407 | |
IGU83 | B. de Thoisy (Pasteur) | |||
IGU84 | IGU84 (697) | B. de Thoisy (Pasteur) | MK687408 | |
IGU85 | B. de Thoisy (Pasteur) |
Fragments of the ND4 mitochondrial locus, encompassing the 3' end of the NADH dehydrogenase subunit 4 gene (ND4) and the tRNA genes histidine, serine and leucine (partial 5' end), were PCR-amplified using the primer pair and protocols of
The best nucleotide substitution model was chosen using JModelTest 2 (
Analyses based on microsatellite molecular markers included 43 individuals of both insular and continental origins (Table
We tested the departures from Hardy-Weinberg expectations and linkage disequilibria using exact tests (1200 permutations) as implemented in the fstat software ver. 2.9.3.2 (
We calculated paired Fst values between populations (
Hierarchical genetic structure of Iguana inferred by Structure and Structure harvester. Bar plots show admixture coefficient of each analyzed individuals (represented by each vertical bar) for the inferred genetic clusters K (represented by a different color). The graphs show Delta K values (
Based on microsatellite variation, genetic diversity (He) ranged from 0 to 0.82 (Table
Genetic diversity parameters for each locus. Key: Ar, allelic richness, He, expected heterozygosity, and Fis were computed for each population and loci using FSTAT ver. 2.9.3.2 software (
Loci | Montserrat | Saba | Saint Lucia | Grenadines | Guiana | All | |
---|---|---|---|---|---|---|---|
L2 | Ar | 1.72 | 1.00 | 1.00 | 1.00 | 1.84 | 2.98 |
He | 0.23 | 0.00 | 0.00 | 0.00 | 0.26 | 0.10 | |
Fis | -0.10 | NA | NA | NA | -0.09 | -0.10 | |
L3 | Ar | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 |
He | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | |
Fis | NA | NA | NA | NA | NA | NA | |
L5 | Ar | 1.94 | 1.91 | 1.00 | 1.00 | 2.00 | 1.91 |
He | 0.39 | 0.33 | 0.00 | 0.00 | 0.52 | 0.25 | |
Fis | -0.29 | 1.00 | NA | NA | -0.09 | 0.21 | |
L6 | Ar | 2.66 | 1.80 | 1.00 | 1.00 | 2.00 | 3.36 |
He | 0.53 | 0.20 | 0.00 | 0.00 | 0.52 | 0.25 | |
Fis | 0.37 | 0.00 | NA | NA | 0.73 | 0.37 | |
L8 | Ar | 1.00 | 1.00 | 1.00 | 1.00 | 1.84 | 1.18 |
He | 0.00 | 0.00 | 0.00 | 0.00 | 0.26 | 0.05 | |
Fis | NA | NA | NA | NA | -0.09 | -0.09 | |
L9 | Ar | 3.42 | 2.96 | 1.00 | 3.00 | 2.89 | 3.80 |
He | 0.66 | 0.72 | 0.00 | 0.75 | 0.61 | 0.55 | |
Fis | 0.18 | 0.54 | NA | 0.33 | -0.41 | 0.16 | |
L13 | Ar | 1.00 | 1.00 | 1.00 | 2.00 | 1.00 | 1.99 |
He | 0.00 | 0.00 | 0.00 | 0.50 | 0.00 | 0.10 | |
Fis | NA | NA | NA | 1.00 | NA | 1.00 | |
L14 | Ar | 1.98 | 2.91 | 1.36 | 1.00 | 1.57 | 2.65 |
He | 0.45 | 0.68 | 0.09 | 0.00 | 0.14 | 0.27 | |
Fis | -0.43 | 0.02 | 0.00 | NA | 0.00 | -0.10 | |
L15 | Ar | 1.33 | 1.00 | 1.00 | 1.00 | 2.93 | 2.33 |
He | 0.08 | 0.00 | 0.00 | 0.00 | 0.68 | 0.15 | |
Fis | 0.00 | NA | NA | NA | 0.16 | 0.08 | |
L16 | Ar | 1.00 | 1.00 | 1.00 | 2.00 | 1.57 | 1.19 |
He | 0.00 | 0.00 | 0.00 | 0.25 | 0.14 | 0.08 | |
Fis | NA | NA | NA | 0.00 | 0.00 | 0.00 | |
L17 | Ar | 1.00 | 1.00 | 1.00 | 1.00 | 2.52 | 2.36 |
He | 0.00 | 0.00 | 0.00 | 0.00 | 0.49 | 0.10 | |
Fis | NA | NA | NA | NA | 0.42 | 0.42 | |
L18 | Ar | 2.41 | 1.00 | 1.00 | 1.00 | 2.00 | 1.81 |
He | 0.40 | 0.00 | 0.00 | 0.00 | 0.53 | 0.19 | |
Fis | 0.45 | NA | NA | NA | -0.25 | 0.10 | |
L19 | Ar | 2.91 | 2.00 | 1.00 | 1.00 | 2.00 | 3.13 |
He | 0.67 | 0.53 | 0.00 | 0.00 | 0.52 | 0.34 | |
Fis | -0.13 | 0.06 | NA | NA | -0.36 | -0.14 | |
L20 | Ar | 1.98 | 1.00 | 1.00 | 1.00 | 3.14 | 3.44 |
He | 0.46 | 0.00 | 0.00 | 0.00 | 0.66 | 0.22 | |
Fis | -0.47 | NA | NA | NA | -0.09 | -0.28 | |
L23 | Ar | 1.00 | 1.80 | 1.00 | 1.00 | 3.86 | 3.00 |
He | 0.00 | 0.20 | 0.00 | 0.00 | 0.82 | 0.20 | |
Fis | NA | 0.00 | NA | NA | 0.30 | 0.15 | |
L24 | Ar | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 |
He | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | |
Fis | NA | NA | NA | NA | NA | NA | |
All | Ar | 1.71 | 1.46 | 1.02 | 1.25 | 2.07 | 2.32 |
He | 0.24 | 0.17 | 0.01 | 0.09 | 0.39 | 0.18 | |
Fis | -0.03 | 0.29 | 0.00 | 0.50 | 0.03 | 0.16 |
Fst values for each pairwise population comparison (below the diagonal) and their significance levels (above the diagonal). The indicative adjusted nominal level (5%) for multiple comparisons is 0.005. Fst values that reveal a significant genetic differentiation are in bold.
Montserrat | Saba | Saint Lucia | Grenadines | Guiana | |
---|---|---|---|---|---|
Montserrat | – | 0.01 | 0.005 | 0.005 | 0.005 |
Saba | 0.104 | – | 0.005 | 0.035 | 0.005 |
Saint Lucia | 0.806 | 0.909 | – | 0.005 | 0.005 |
Grenadines | 0.670 | 0.777 | 0.555 | – | 0.005 |
Guiana | 0.392 | 0.467 | 0.738 | 0.529 | – |
The ML tree based on ND4 sequences had the highest log likelihood of – 2861.13 (Fig.
The Saba-Montserrat-Venezuela populations formed a monophyletic group that is the sister group of the populations from French Guiana and Brazil, this group is, in turn, the sister group of the group of St. Lucia-Grenadines that was previously described as two endemic subspecies Iguana iguana sanctaluciae for the endemic population of St. Lucia and Iguana iguana insularis for the population of the Grenadines (
From these genetic data and the following morphological data, it is clear that the endemic iguanas from Saba and Montserrat form a distinct evolutionary entity that we recognize as a new species which is formally describe below accompanied by a taxonomic analysis.
The Maximum Likelihood (ML) tree of the ND4 sequences of iguanas. The percentage of trees in which the associated taxa clustered is shown next to the branches, as bootstrap support (BS ≥ 70) for ML and Maximum Parsimony (MP) topologies respectively. Sequences amplified by the authors of this study were indicated by colored diamond-shaped marks. Marks are colored based on the sampling sites. Sequences from published studies were labelled by their NCBI GenBank access numbers (Fig.
The Median-Joining (MJ) network of the ND4 sequences of iguanas. The sequences amplified by the authors of this study and the corresponding haplotypes from published studies were labelled from “Hap_1” to “Hap_10” (details in Table
Haplotypes used in MJ network. Sequences amplified by the authors of this study and corresponding haplotypes from published studies were labelled from “Hap_1” to “Hap_10”. HM352505 haplotype found in the 7 specimens from Montserrat and the 6 specimens from Saba corresponds to “Hap_4”.
Origins of the specimens used for the network | |
BRA: Brazil | |
GRE: Grenadines | |
GUI: French Guiana | |
MON: Montserrat | |
STL: St. Lucia | |
SUR: Suriname | |
VEN: Venezuela | |
DEL: Iguana delicatissima (Anguilla, Dominica, St. Eustatius) | |
Hap_1: | 2 [IGU78GUI, IGU79GUI] |
Hap_2: | 2 [IGU82GUI, JQ340914BRA] |
Hap_3: | 1 [IGU84GUI] |
Hap_4: | 22 [IGU88MON, IGU89MON, IGU92MON, IGU93MON, SABA01, SABA02, SABA03, SABA04, SABA07, HM352505_M1, HM352505_M2, HM352505_M3, HM352505_M4, HM352505_M5, HM352505_M6, HM352505_M7, HM352505_S1, HM352505_S2, HM352505_S3, HM352505_S4, HM352505_S5, HM352505_S6] |
Hap_5: | 2 [SABA05, SABA06] |
Hap_6: | 8 [IGU58STL, IGU63STL, AF217782_1, AF217782_2, AF217782_3, AF217782_4, AF217782_5, AF217782_6] |
Hap_7: | 1 [IGU65STL] |
Hap_8: | 1 [IGU73GRE] |
Hap_9: | 2 [IGU75GRE, IGU76GRE] |
Hap_10: | 1 [IGU77GRE] |
1[JQ340913BRA]; 4[HM352500_1SUR, HM352500_2SUR, HM352500_3SUR, HM352500_4SUR]; 1[HM352501VEN]; 7[AF217783_1DEL, AF217783_2DEL, AF217783_3DEL, AF217783_4DEL, AF217783_5DEL, AF217783_6DEL, AF217783_7DEL] |
A species of Iguana, with a distinctive melanistic phenotype, with a black dewlap, huge tubercular nape scales, the absence of horns on the snout.
The name was chosen to emphasize the most conspicuous feature of this new taxon, from melano meaning black and derma meaning skin.
Common local names are: Melanistic Lesser Antilles iguana, Saban Black iguana
Choice of the holotype and the paratype.
The choice of our type specimens and the way we conducted the description of the type and the paratype attempt to best meet the criteria proposed by (
(1) The Saba and Montserrat populations survived for a long time in a period when the risk of extinction was lower than today. Nevertheless, the iguanas were hunted for food, killed by cats and dogs, and their habitats destroyed by livestock and natural events. Today, in Saba, the main risk for this small endemic population, which seems to be far from the carrying capacity of the island, is the arrival of invasive common iguanas from South and Central America that have a rapidly expanding population in Saint Maarten. In Montserrat, the same risk exists. Volcanic eruptions are also a major threat to these populations, as evidenced by the eruption of the Soufrière Hills in Montserrat in 1995 and the following years, which destroyed about a third of the island.
Hybridization with closely related lineages may in-fact be the greatest risk and could very likely lead to extinction of endemic lineages, as is the case for Iguana delicatissima in Guadeloupian Archipelago (
(2)
(3) We have no precise idea of the size of the iguana population in Saba and Montserrat. Rough estimates based on density in some surveyed areas yield 100–300 adults and subadults for each island. In theory, it is always possible to catch a senile non-breeding male and prepare it in good conditions act as a voucher that will be available in a Museum collection for future study. But, for technical reasons, when the first author was in Saba in 2012, it was not possible to collect such an individual. Roadkill animals are often in poor conditions (broken, flattened, rotten) and in most cases cannot be studied and preserved in a zoological reference collection. The same remarks apply to the Montserrat population.
(4) Since diagnostic characteristics are mainly visible in adult individuals and are not measurements, we chose for the holotype of this new taxon specimen
(Fig.
This individual from Saba was not measured in detail because of the risk of spoiling the specimen. It is an adult female of approximately 26.3 cm SVL and a tail length of approximately 66.4 cm and a total length of 92.7 cm (measurements and photographs by Joseph Martinez,
Holotype of Iguana melanoderma sp. nov. A Dorsal view B lateral view C dorsal view of the head D lateral view of the head.
The subtympanic plate is round, with a dark patch in the posterior part. The anterior, upper, and lower parts of the subtympanic plate are surrounded by black pigment. Most labial and sublabial scales have dark coloration on their anterior side. The lower labial scales, before the subtympanic plate, are arranged in a series of five pairs of scales of quite similar size and located one in front of the other. The tubercular nape scales are numerous, well developed, grey, and aligned in rows.
This specimen is partially discolored, with a slight carpet pattern, the stripes on the tail are almost invisible in the photographs, but according to (
The dewlap is black in its lower part, and there are nine small, triangular yellowish gular spikes. The tympanum is brown. There is a conspicuous black spot between the eye and the tympanum. The snout and the top of the head are light, not black. The dorsal spikes are greenish and black.
(Fig.
Paratype of Iguana melanoderma sp. nov. A Left side view of the head B right side view of the head.
This individual is only a head of a small adult male based on the size of the dorsal spikes. This head presents the typical characteristics of this taxon: large grey scales on the tubercular nape, black spot between the eye and the tympanum, and labial and sublabial scales with black patches on the anterior part. There are five pairs of scales before the subtympanic plate almost completely black, a black dewlap, and a flat head with a light snout (photographs by Joseph Martinez,
On the Windward side of Saba for the holotype and on Old Road Bluff, west coast of Montserrat for the paratype (Figs
Iguana melanoderma is distinguished from all other iguana lineages by the following combination of characteristics. This description is mainly based on adult iguanas observed in the field with the most developed diagnostic characteristics.
Iguana melanoderma belongs to the Common Green Iguana phenotype (in contrast to the Iguana delicatissima phenotype) with its large subtympanic plate, the arrangement of sublabial scales, the rectangular shape of the dewlap, the shape and the distribution of the gular spikes, its flat head, its tubercular nape scales, and its banded tail (
The most distinctive morphological trait of this new taxon is its general color: adults from Saba and Montserrat iguanas are melanistic. There is a tendency for individuals to become blacker with age (Fig.
Comparison of morphological features of the head. A Young adult male. 1. Subtympanic plate with pink in the center. 2. Lower sublabial scales arranged in pairs of nearly identical size. 3. Black anterior edge of the lower sublabial scales. 4. Black border around the subtympanic plate. 5. Prominent nostrils. 6. Black spot between the eye and the tympanum. 7. Absence of horn and light snout. 8. Dark brown eye. 9. Triangular gular spikes. 10. Fewer than 10 gular spikes extended in the upper part of the lower dewlap. 11. High number of aligned nape tubercles. 12. Prominent light-grey tubercles. 13. Light greyish-green coloration on the neck. 14. High light-grey dorsal spines. 15. Dewlap half black. 16. Dorsal part of the limb with light-green scales becoming black with the extension of melanin from the anterior edge to the posterior edge of the scales. B Old male of Iguana melanoderma (Saba). 1. Large all-black subtympanic plate. 2. Extension of the black pigment on the sublabial scales. 3. Black coloration of the labial and upper sublabial scales. 4. Black coloration between the tympanum and the subtympanic plate. 6. Extension of the black spot around the eye and on the posterior labial and sublabial scales.7. Snout turning dark grey. 9, 10. Gular spikes turning dark grey with extension of black patches. 12. Dark grey nape tubercles. 13. Black coloration on the neck. 14. Dorsal spikes turning black. 15. Dewlap completely black. 16. Black upper face of the limb.
The dorsal carpet pattern of young adults Iguana melanoderma. A Montserrat B Saba. The dorsal coloration is formed by darker more or less interrupted dorso-ventral bands (brown, dark grey) on a lighter ground. This pattern disappears in old individuals. The black patch between the eye and the tympanum is already visible.
There is always a black spot between the brown to grey-brown eye and the tympanum. In fully grown adults, the subtympanic plate is 2 to 2.5 times the height of the tympanum. Its color varies from light pink to dark pink with a proportion of black coloration ranging from hardly black to all black. The tympanum can be completely black. The labial and sublabial scales have the same coloring as the subtympanic plate. The lower labial scales, anterior to the subtympanic plate, are arranged in 3–5 pairs of scales of fairly similar size, one in front of the other, and do not form a mosaic of small scales. The head is usually black on the sides (tympanum, eye, subtympanic and posterior labial and sublabial parts), whereas the snout and the top of the head are light to dark grey, and in some individuals these parts are nearly entirely black.
The dewlap is completely black in adults, as in Iguana iguana sanctaluciae (Fig.
The dorsal parts of the limbs are more or less black, and the black is more developed in older individuals extending over the ventral face of the limb. Some specimens have entirely black head and legs whereas the body is dark green. This body coloration is the result of a black anterior part and a lighter posterior part of most scales while some others are black or dark green. The spikes of the dorsal crest range from light to dark grey; the central part can be black. Some individuals have entirely black dorsal and caudal crests.
The nuptial coloration is present in both sexes, but more vivid and more developed in males than in females. Breeding adults sometimes become reddish-orange over the entire body (
The iguanas from Saba and Montserrat begin their lives with discontinuous light, medium and dark green dorsolateral bands and patches, some of which are underlined by white markings without black on the head and limbs. The black spot between the eye and the tympanum is present in one-year-old individuals, but it is very small and poorly developed. The proportion of the areas covered by these different green markings varies in hatchlings. In juveniles and subadults, this pattern then gradually changes to an ornate arrangement, called a carpet pattern by
A Old adult from Montserrat B old adult from Saba. In these old individuals the carpet pattern is absent. The head is almost entirely black, except for the top and the snout. The dewlap, neck, dorsal spikes, and forelimb are black. Dorsal and lateral coloring is more variable, ranging from entirely black to a mosaic of black, brown, and dark green scales.
There are no nasal horns. The tubercular nape scales are numerous, prominent, ranging from light to dark grey, and are often aligned in many rows. The cheek scales usually do not overlap.
Montserrat iguanas are similar to those of Saba. Overall, they appear less melanistic, but some individuals are as black as those of Saba. The head appears to be flatter and more elongated in Montserrat than in Saba, but more data are needed to assess putative morphological divergence between the two populations.
In Saba, Iguana melanoderma lives on cliffs (Fig.
In Montserrat, Iguana melanoderma have been reported in a variety of habitats, mostly in coastal residential areas. In 1995, before the eruption of the Soufrière Hills, iguanas could be seen in the then capital, Plymouth, along the seawall defenses just above high tide (M. Morton, personal observation).
In Montserrat, there are far fewer records from mesic forest (
According to
The volcanic island of Montserrat is 102 km2. In 1995, the dormant volcano of the Soufrière Hills became active. Catastrophic eruptions in 1997 rendered two thirds of the south of the island uninhabitable and led to the creation of an exclusion zone (Fig.
The island of Saba is about 13 km2 and rises to an altitude of 877 m a.s.l. on Mt Scenery. This peak forms the summit of a dormant 400 ka-year-old volcano (
The superposition of the geological map (
As such, the Saban Black Iguana is mainly present on the Windward side, from sea level to about 500 m a.s.l. (hilltop at the Level 514 m) (Fig.
In the US Virgin Islands (St. Thomas, St. Croix, St. John) and the British Virgin Islands (BVI: Tortola) as well as on the coastal islands of Venezuela, and on the coast in the vicinity of Cumana, there are also melanistic iguanas (
Such a discontinuous distribution of this new species is puzzling. It can be explained by: [1] the natural dispersal from northern Venezuela (mainland and coastal islands) where iguanas with the same melanistic phenotype are found, as in Margarita, Los Roques and La Blanquilla, [2] human dispersion by pre-Columbian Indians, [3] recent dispersal by Modern Man, [4] convergent evolution, [5] the regression of a wider distribution area, or [6] a combination of the previous hypotheses.
To successfully colonize an island, iguanas must first arrive on that island by natural or human means, occupy an available ecological niche, or if not, be able to successfully compete with the local species. Based on what we know about the competition between Iguana delicatissima and Iguana iguana (
The first iguanas were collected in Saba by F. Laglois in 1879 (
Saba and Montserrat are separated by 150 km. Between the two is the Christopher Bank or St. Kitts Bank (St. Eustatius, St. Kitts, Nevis) which was inhabited in historical times by Iguana delicatissima perhaps with the exception of St. Kitts (
In Saba, a pre-ceramic occupation dating from 3300 BP with dense midden deposits, mainly land crabs and birds, located at 400 m a.s.l., in the tropical forest, was studied by
The similarity in morphology and coloration of these two populations (
According to
The Pleistocene natural deposits of Marie-Galante do not contain the remains of Iguana delicatissima nor Iguana iguana while many other reptiles, now extinct, are present. Iguana delicatissima appears on this island with Amerindians artifacts that suggest human introduction (
Based on our data and those of
The five differences (5/818 = 0,6 %) between the haplotype (HM352505) of Saba-Montserrat and the haplotype of Venezuela (HM352501) suggest differentiation, with a genetic divergence, approximated by a molecular clock of 1.29 million years for every 1% sequence divergence, at the ND4-Leu Locus (
Hap_4 (GB HM352505), the most common haplotype, is shared by these two insular populations, but Saba also has its own haplotype (Hap_5) (Fig.
Montserrat consists of three major volcanic centers: to the north are the heavily eroded Silver Hills (ca. 2.6–1.2 Ma); in the center are the Centre Hills (ca. 950–550 ka), also extinct and crossed by deep erosive canyons; and to the south is the massif comprising the South Soufrière Hills (ca. 135–125 ka) and the Soufrière Hills (ca. 170 ky to present) (
Saba’s oldest rocks are about 400 ky years but most of the volcanic deposits were produced in the last 70,000 years and have increased the size of the island on the edge of Mt Scenery. The last eruption is dated to 280 years BP and covers Amerindian artifacts but underlies those of the European settlers who colonized the island in 1640. European settlers may have been attracted to the island because of the presence of grassland instead of tropical rainforest caused by an eruption shortly before European settlement (
A bottleneck hypothesis and/or founder effect to explain the low genetic diversity of these insular iguanas is congruent with the fact that of the 16 common microsatellite loci used in this study, 9 are monomorphic in Saba while 8 are monomorphic in Montserrat with twice as many individuals. For example, the Iguana delicatissima population of Petite Terre (Guadeloupian Archipelago) has 8/15 monomorphic microsatellite loci and the Chancel Islet population 6/15. In both populations, serious bottlenecks have recently occurred (
Results based on microsatellite markers revealed a higher level of genetic diversity in Montserrat iguanas than in Saba iguanas. Montserrat iguanas show a genetic signature close to that of iguanas from French Guiana (Fig.
According to
For example, Cyclura nubila nubila differs by less than 1% from the ND4 sequence of C. nubila caymanensis . The same level of divergence is also found between C. cychlura cychlura and C. cychlura inornata which are considered valid subspecies (
According to
Clade II of (
• Iguana iguana iguana (French Guiana and Brazil);
• Iguana iguana sanctaluciae (St. Lucia);
• Iguana iguana insularis (St. Vincent and Grenadines);
• Iguana melanoderma (north-eastern Venezuela, Venezuelan coastal islands, Saba-Montserrat Puerto Rico Bank, Virgin Islands, St. Croix Bank).
According to
• Iguana insularis insularis comb. nov. of the Grenada Bank (including the Grenadines);
• and Iguana insularis sanctaluciae comb. nov. from Saint Lucia.
Naming species and subspecies in the South American clade has not resolved phylogenetic relationships with continental iguanas. For example, the formation of the Isthmus of Panama which was previously thought to be 2.5 My old (
The description of Iguana melanoderma, with its morphological and genetic diagnostic characteristics, will enable conservationists to differentiate between endemic and exotic iguanas. For example, the IUCN Red List (
As the range of invasive iguanas increases worldwide (
The Saba Conservation Foundation (SCF) is responsible for nature management on the island for the local government and runs programs for the Saban Black Iguana by reducing defoliation by goats through the restriction of the number of free-ranging domestic animals (
We found no evidence of genetic introgression in the Saban Black Iguana population; the samples studied for genetic analysis, collected in 2011, have all the characteristics of this new taxon. However, according to a photograph published in the book by
Moreover, it is clear from the Google photographs of iguanas taken in the Virgin Islands that the invasive iguana (Iguana rhinolopha) is also present and hybridization is occurring as shown by the presence of intermediate phenotypes in these islands and by genetic data (
Iguana iguana is listed in CITES Appendix II, but export quotas exist for many countries for pet trade and products (leather, meat). No distinction is made between native and introduced populations, or between continental and insular populations (
Priority actions for the conservation of the species Iguana melanoderma are biosecurity [1], minimization of hunting [2], and habitat conservation [3]. The maritime and airport authorities of both islands must be vigilant about the movements of iguanas, or their sub-products, in either direction, even if the animals remain within the same nation’s territory. Capacity-building and awareness-raising should strengthen the islands’ biosecurity system and could enhance pride in this flagship species.
Key stakeholders in conservation efforts are the Dutch Caribbean Nature Alliance (DCNA), the Saba Conservation Foundation (SCF), the Montserrat National Trust (MNT) and the UK Overseas Territories Conservation Forum (UKOTCF).
The DCNA is already involved in the conservation of Iguana delicatissima on St Eustatius
In conclusion, the pioneering work of
All Saba samples were collected by the Natural Reserve of St. Barthélemy in collaboration with the Saba National Park (2011). St. Lucia samples were provided by M. Morton (Durrell Wildlife Conservation Trust) and the Forestry Service of St. Lucia. All samples were collected with the authorization of the local nature conservation authorities. Special thanks also offered to F. Catzefis (CNRS, Montpellier, France) and Benoît de Thoisy (Institut Pasteur, Cayenne, French Guiana), who provided samples from French Guiana.
Moreover, the NGO Sea and Learn on Saba, a mainly locally sponsored foundation, invited the first author in 2012 to present the first results of this study in 2012 with Karl Kestel and Julien Le Quellec (St. Barthélemy Nature Reserve). Samples from Montserrat were exported and imported under CITES permit No. EX16–37 19/4/2016.
The genetic study was part of BV’s Master’s degree. This project was funded by the Direction Régionale de l’Environnement et du Logement de Martinique, as well as by the Natural Reserve of St. Barthélemy for Saba and St. Lucia iguanas. These sponsors play no role in the design of this study, the collection and analysis of data, the decision to publish, or the preparation of the manuscript. The genetic analyses were initially conducted at Genindexe by BV in La Rochelle (France) and completed by David Schikorski in Genindexe-Labofarm (France), which also funded part of this study.
Pictures and measurements of the
We are indebted to Robert Powell and an anonymous referee for their thorough, in depth, and thoughtful reviews of the manuscript, as well as to the subject editor and the editor-in-chief for the publication of this work.
We thank Chris Austin for English improvement on the final version of this manuscript.