- Research article
- Open Access
Moorean tree snail survival revisited: a multi-island genealogical perspective
© Lee et al; licensee BioMed Central Ltd. 2009
- Received: 4 March 2009
- Accepted: 18 August 2009
- Published: 18 August 2009
The mass extirpation of the island of Moorea's endemic partulid tree snail fauna, following the deliberate introduction of the alien predator Euglandina rosea, represents one of the highest profile conservation crises of the past thirty years. All of the island's partulids were thought to be extirpated by 1987, with five species persisting in zoos, but intensive field surveys have recently detected a number of surviving wild populations. We report here a mitochondrial (mt) phylogenetic estimate of Moorean partulid wild and captive lineage survival calibrated with a reference museum collection that pre-dates the predator's introduction and that also includes a parallel dataset from the neighboring island of Tahiti.
Although severe winnowing of Moorea's mt lineage diversity has occurred, seven of eight (six Partula; two Samoana) partulid tip clades remain extant. The extinct mt clade occurred predominantly in the P. suturalis species complex and it represented a major component of Moorea's endemic partulid treespace. Extant Moorean mt clades exhibited a complex spectrum of persistence on Moorea, in captivity, and (in the form of five phylogenetically distinct sister lineages) on Tahiti. Most notably, three Partula taxa, bearing two multi-island mt lineages, have survived decades of E. rosea predation on Moorea (P. taeniata) and in the valleys of Tahiti (P. hyalina and P. clara). Their differential persistence was correlated with intrinsic attributes, such as taxonomy and mt lineages, rather than with their respective within-island distribution patterns.
Conservation efforts directed toward Moorean and Tahitian partulids have typically operated within a single island frame of reference, but our discovery of robust genealogical ties among survivors on both islands implies that a multi-island perspective is required. Understanding what genetic and/or ecological factors have enabled Partula taeniata, P. hyalina and P. clara to differentially survive long-term direct exposure to the predator may provide important clues toward developing a viable long term conservation plan for Society Island partulid tree snails.
- Captive Population
- Moorean Lineage
- Sister Lineage
- Snail Population
Oceanic islands have never been connected to continental landmasses and receive their terrestrial biotas solely through trans-oceanic dispersal and subsequent in situ diversification . Hot spot archipelagoes, in particular, are fecund cladogenic settings, and these chronologically arrayed island chains frequently accumulate species-rich endemic radiations that are of exceptional interest to evolutionary biologists [2–4]. Because they have evolved in isolation, endemic island species often lack highly developed defensive or competitive abilities [5–7], and this renders them exceptionally vulnerable to introduced continental competitors and predators [1, 8, 9].
One of the most pronounced recent cases of oceanic island mass extirpation has involved the rapid extinction in the wild of the large majority of the 61 described endemic Society Islands partulid tree snails (4 Samoana and 57 Partula species) following the deliberate introduction of the alien carnivorous land snail Euglandina rosea [10–13]. The rationale for the introduction was a biological control program aimed at another alien mollusc, the giant African land snail, Lissachatina fulica, and the predator was released on Tahiti in 1974, on Moorea in 1977, and on other Society Islands in the 1980s and 1990s .
Euglandina rosea's devastating effect on non-target Society Island endemic tree snail populations is best documented for the island of Moorea [10, 15]. Within a decade, all 9 Moorean partulids (7 Partula and 2 Samoana species) were deemed extirpated, but prescient interventions led to the successful establishment of off-island captive populations for most of the island's Partula species in international zoos and universities [15–17]. Five endemic Moorean Partula species (P. taeniata, P. suturalis, P. tohiveana, P. mooreana and P. mirabilis) have been successfully maintained in captivity for over two decades by The Partulid Global Species Management Programme, and two species (P. exigua and P. aurantia) are extinct . No captive populations exist for Society Island Samoana species. In 1994, an experimental reestablishment of captive-reared P. taeniata, P. suturalis and P. tohiveana was attempted by releasing them into a 20 × 20 m2 predator-proof snail field reserve erected in a Moorean valley. However, field maintenance issues led to repeated predator incursions and the experiment was terminated in 1998 .
The loss of the Society Island's endemic tree snails is compounded by their scientific prominence as the subject of classic studies in zoology, population biology and evolutionary genetics for over a century [19–24]. Moorean Partula spp., in particular, were the focus of much of this research, and have been intensively studied by B. Clarke, J. Murray, M. Johnson and their associates over a number of decades. The resulting picture is a complicated one in which six of the seven morphologically and ecologically well-defined Moorean species collectively formed two species complexes: 1) P. taeniata and P. exigua; 2) P. suturalis, P. tohiveana, P. mooreana and P. aurantia. The seventh species, P. mirabilis, could hybridize with either complex . Moorean Partula spp. showed a potential for gene flow, either directly or indirectly, among all seven taxa, resulting in a lack of concordance among morphology, molecules and degree of reproductive isolation [25–28].
All Moorean partulid species were thought to be extirpated in the wild by 1987  and, until recently, it looked as if Society Island partulids would survive only in captivity . However, intensive on-going field surveys have detected scattered relict populations on a number of islands, including seven on Moorea. A relict Moorean population of Samoana attenuata has been monitored since 1996 by C. Hickman, and this species also persists on Tahiti [14, 29] and on Raiatea . Six surviving populations of the Moorean endemic Partula taeniata have been detected since 2000. This latter species was formerly distributed throughout the island and exhibited regional variation in shell phenotype , allozyme profile  and mitochondrial (mt) genetic structure [25, 27].
The primary goal of our study was to assess genealogically the remnant wild Moorean partulid populations by placing them in a phylogeographic framework. A single island phylogenetic perspective is insufficient because Samoana attenuata has a multi-island distribution  and Partula taeniata contains divergent mt lineages that collectively form robust taxonomically polyphyletic clades with different subsets of Moorean and Tahitian congeners [25, 34]. Moorea and Tahiti are neighboring islands separated by a mere 17 km of ocean. They are the largest members of the Society Island archipelago's eastern "Windward Islands/Iles du Vent" sub-group and support all of the sub-group's partulid populations. Moorea is the older of the two, and allozyme and morphological analyses have identified it as the source of Tahiti's Partula species , although there may have been some back-migration from Tahiti to southern Moorea . Our goal therefore was to build a combined Moorean/Tahitian phylogeny that incorporated extant wild populations, extant captive populations and historical museum samples, the latter collected by J.B. Burch in 1970, prior to the introduction of Euglandina rosea.
A recent phylogenetic study of Tahitian wild, captive and historical museum tree snails found that at least some members of all five primary historical Tahitian Partula mt clades remain extant, primarily in montane refuge populations . This result was somewhat unexpected, given that three of Tahiti's eight Partula species are extinct . However, Society Island partulid taxonomic designations are predominantly conchological [20, 21], and they are often poorly-corroborated by molecular markers, although this is further complicated by incongruence among genetic marker sets [25–28, 36, 37]. In this present study, we were particularly interested in testing for cryptic genealogical links among surviving Windward Island partulid populations on Moorea and on Tahiti. Our results show that although much of Moorea's tree snail mitochondrial diversity (including one of the primary tip clades) has been lost, a surprisingly representative genealogical sub-sample collectively persists in captivity, in the wild on Moorea and, in the form of five phylogenetically distinct sister lineages, on Tahiti.
Windward Island Overview
Combining our novel data (82 distinct haplotypes from 161 snails) with preexisting mt COI datasets [30, 36, 37] produced a total Windward Island genotyped partulid sample size of 457 snails. Although this malacofauna has experienced extreme extinction pressure in recent decades, access to museum and captive specimens enabled us to incorporate genotypes from six extinct species (three Moorean) as well as from the five extirpated species (four Moorean) that persist in captivity . Consequently, we have almost complete nominal species taxonomic representation: 16 out of the 17 Windward Island taxa listed in a recent study  in addition to the endemic Tahitian Samoana burchi. The missing species, Partula cytherea, has not been seen since its 1920's discovery on a remote Tahitian interior mountain slope  and it is now presumed extinct .
Moorean Clade 1
Moorean Clade 1 lineages initially appeared to be restricted to that island because no constituent haplotypes had been encountered in Lee et al's [36, 37] extensive genotyping of Tahitian wild, captive and historical museum tree snails. However, four Tahitan snails from a recently discovered extant population of Partula clara in Tiapa Valley (unsampled by Burch in 1970) all shared a haplotype that surprisingly nested firmly within Moorean Clade 1, sister to a Moorean Puutu Valley population of P. exigua (Figure 2). Crampton recognized the Tiapa (Aoua, in his terminology) Valley population as a distinct subspecies, P. clara incrassa, stating that it was extraordinarily distinct from nominal conspecifics in adjacent valleys in that it had longer thinner shells, peculiar color morphs including unique banded mutants, thinner shells and lips and some specimens with a trace of a pillar tooth . Our extant wild Tiapa Valley snails are conchologically indistinguishable from Crampton's voucher specimens of P. c. incrassa (see Additional File 1) and the haplotype they carry is phylogenetically distinct from all other Tahitian partulids (Figure 1), including members of the primary P. clara/hyalina clade in adjacent valleys . Snails bearing Moorean Clade 1 mitochondria therefore appear to have established a discrete founder population in this Tahitian valley, where they now represent the only surviving partulids (T. Coote pers. observ.), and this clade remains tenuously extant on both Moorea (P. taeniata) and Tahiti (P. c. incrassa), as well as in captivity.
Moorean Clade 2
Moorean Clade 3
Both Partula aurantia and P. m. propinqua are now presumed extinct. Two P. suturalis subspecies survive in captivity. They were originally sourced from one central valley (P. s. vexillum: Fareaito; see topological placement in Figure 1) and two southern valleys (P. s. vexillum: Vaianai; P. s. strigosa: Maatea), but none of the genotyped captive specimens bore Moorean Clade 3 mt lineages (Figure 4). It would appear that Moorean Clade 3, a major endemic component of the island's historical partulid mt tree space, may well be extinct.
Moorean Clade 4
Viewed from a single-island perspective, Moorean Clade 4 seems relatively unimportant: it lacks on-island sister lineages, represents a minor component of the island's historical partulid mt tree space, had a restricted original distribution and is not represented in captive populations (Figures 1, 5; ). However, taking a multi-island perspective revealed these Moorean Partula taeniata mt lineages to be part of a larger mt clade with a substantial Windward Island, and regional archipelagic distribution. Moorean Clade 4 has a robust and exclusive sister relationship with a major Tahitian mt lineage comprising two nominal species, Partula hyalina and P. clara (Tahitian Clade 5; Figures 1, 5; with the exception of the Tiapa Valley population of P. c. incrassa, Figure 2). Tahitian P. hyalina and P. clara snails have also proven to be differentially resistant to Euglandina rosea predation. Although these two nominal taxa collectively represented only circa 5% of historical Tahitian valley Partula spp. populations , they now form 100% of the surviving populations in numerous Tahitian valleys , the latest estimate being 33 valleys (T. Coote, unpubl. observ.). Multiple 1970-era Tahitian haplotypes were recovered from genotyped extant wild and captive Tahitian P. hyalina and P. clara snails and also from extant P. hyalina anthropogenic founder populations in the Cook and Austral Islands, two neighboring hot spot archipelagoes (Figure 5; [36, 37]). Regional wild snail populations bearing members of this phylogenetically-distinctive mt lineage (Moorea 4 + Tahiti 5) therefore survive tenuously in the presence of Euglandina rosea on Moorea and on Tahiti and thrive in its absence on the Cook and Austral archipelagoes (Figure 5; ).
Moorean Clade 5
Moorean Clade 5 is now apparently extirpated in the wild, but a constituent haplotype survives in a captive P. mirabilis population, originally sourced from Fareaito Valley (Figure 6). Taking a multi-island perspective, Moorean Clade 5 is part of a larger and phylogenetically-distinctive Windward Island mt lineage that incorporates an exclusive Tahitian sister clade: Tahiti 1 (Figures 1, 6; ) and that collectively has a taxonomic composition consistent with Murray et al's  mt RFLP genotype "P". Tahiti Clade 1 contained two nominal species, P. affinis and P. otaheitana, had an island-wide distribution, and two known populations persist: P. affinis in captivity and a remnant montane population of P. otaheitana on Mt. Atara (Figure 6; ). Unlike the two other nested Moorean/Tahitian Partula spp. clades (Figures 2, 5), snails bearing this multi-island mt lineage appear incapable of surviving in Windward Island valleys in the presence of Euglandina rosea.
Moorean Clade 6
Topological details of the Samoana clade also corroborated earlier allozyme studies that revealed strikingly different phylogenetic profiles among co-occurring Samoana and Partula taxa . These distinctions included the much lower collective genetic diversity levels of Samoana species (compare relative generic treespaces in Figure 1) and their more pronounced mt phylogenetic cohesiveness (all three Samoana species were reciprocally monophyletic, including the multi-island taxa; Figure 8). Samoana and Partula lineages therefore appear to have experienced quite distinct patterns of cladogenesis in the Windward Islands and, post Euglandina rosea introduction, they also have experienced differential patterns of extirpation and survival. This is a particularly interesting result, given that these three taxa were originally much scarcer than co-occurring Partula species in the Society Islands .
One of the primary challenges faced in constructing a meaningful phylogeny of a largely extirpated fauna concerns the issue of comprehensiveness; how confident are we that our historical reference samples contain the primary Moorean endemic lineages? Although our taxonomic sample of Windward Island Partulidae was almost complete, this in itself was insufficient because of the poor correlation of nominal taxonomy with molecular markers . Nevertheless, our novel results were in good agreement with previous independent mt characterizations of these taxa [25, 27, 28, 34], both within Moorea (e.g., geographic distributions and taxonomic composition of the primary clades) and among the two islands, apart from a small number of relatively minor issues such as the presence of the Tahitian species Partula nodosa within the primary Windward Island mt RFLP lineage . We are therefore confident that our historical reference Moorean dataset probably contains the primary Moorean lineages and that it can be used to assess what fraction of the island's endemic mt treespace has survived in captivity and/or in the wild.
Our Windward Island dataset yields a novel, and somewhat complex, multi-island genealogical perspective on Moorean partulid survival. Only one of eight historical Moorean partulid tip clades (six Partula spp.; two Samoana spp.) is extinct. Unfortunately, the extinct lineage (Moorea Clade 3) encompassed the bulk of the P. suturalis species complex, and lacked Tahitian sister lineages (Figures 1, 4). The seven extant clades exhibited a heterogeneous spectrum of persistence: on Moorea, in captivity and also on Tahiti (Moorean Clade 1); on Moorea, with sister lineages on Tahiti, on other archipelagoes, and in captivity (Moorea Clade 4); on Moorea, with sister lineages on Tahiti (S. attenuata); on Moorea (Moorea Clade 2); in captivity, with sister lineages on Tahiti and also in captivity (Moorea Clade 5); sister lineages on Tahiti (S. diaphana); in captivity (Moorea Clade 6).
Our assessment of Moorean partulid survival comes with an obvious caveat concerning its broader utility; do these results have relevance to understanding historical Moorean partulid whole organism genealogies, and their present day conservation status? Fortunately, this did not appear to be an issue for Windward Island Samoana species where there was excellent taxonomic/mt lineage congruence (Figure 8). However, Society Island partulid taxonomy may be poorly corroborated by molecular markers and, in addition, different nuclear (allozymes and nRNA) and organellar genetic marker sets may also be incongruent [25–28, 36, 37]. Although we cannot address this issue directly using allozymes or high-resolution nuclear markers, two lines of indirect data indicate that our museum, captive and remnant wild mt genealogies do have broader biological and conservation significance. First, the taxonomic composition of our clades is in good agreement with the results of Moorean breeding experiments , e.g., reproductive compatibility of P. taeniata and P. exigua; compatibility of P. suturalis and P. aurantia; incompatibility of P. mooreana and P. tohiveana with P. suturalis, compatibility of P. mirabilis with both P. taeniata and P. suturalis. Second, the ability of Partula spp. populations to persist on Moorea and in Tahitian valleys in the long-term presence of Euglandina rosea appears to be correlated with both taxonomy and mt phylogeography.
Gerlach  proposed that impaired predator performance at altitude would allow the persistence of Society Island partulids in montane refuges and we see evidence of this in Tahiti where substantial montane populations preserve multiple mt clades that have been extirpated at lower altitudes
Predation models predict extirpation of Partula spp. populations within 3 years of initial Euglandina rosea contact . Snails bearing four Moorean mt lineages (Clades 2, 3, 5 (+ its sister clade Tahiti 1) and 6) meet this prediction in that they have not persisted in the presence of the predator, surviving in the wild only in insulated micro-habitats such as the Opunohu Bay mangrove fern enclave (Moorea Clade 2; Figure 3) or in a high altitude montane refuge (Tahiti Clade 1; Figure 6; ). In contrast, snail populations bearing one of two multi-island mt lineages (Moorea Clade 1; Moorea 4 & Tahiti 5) have successfully survived three decades of direct exposure to the predator on Moorea and in many Tahitian valleys.
It is unclear at present what biological attributes, genetic and/or ecological, underlie this differential persistence: Crampton [20, 21] documented relatively higher fecundities in Partula hyalina and P. clara (Tahiti Clade 5), but not in P. taeniata (Moorean Clades 1, 4). Detailed field studies of the surviving populations are urgently required and these may yield clues toward developing a viable long-term conservation plan for Society Island partulid tree snails. Goodacre's mt population study of P. taeniata historical populations documented the presence of a pronounced cline involving a western haplogroup (probably our Moorean Clade 4) and an island-wide haplogroup (probably our Moorean Clade 1) in northwestern valleys that was not corroborated by variation in 6 polymorphic allozyme loci . It is therefore possible that surviving P. taeniata populations bearing these two mt clades may share common sets of hypothetical nuclear genome-encoded "resistance" traits, but this remains to be determined. Irrespective of the underlying mechanisms, the differential resilience exhibited by P. taeniata, P. hyalina and P. clara identifies them as the most promising captive candidate lineages for future Windward Island reestablishment attempts.
Conservation efforts directed toward Moorean and Tahitian partulids have typically operated within a single island frame of reference [14, 18, 29]. However, there is an increasing appreciation among conservation biologists for the importance of evolutionary and ecological processes in effective conservation planning  and the multi-island genealogical relationships of Moorean partulid taxa (Figure 1), specifically the presence of five phylogenetically-distinct sister lineages on Tahiti, provide a broader Windward Island evolutionary perspective on Moorean tree snail survival. Our results imply that, for many endemic partulid lineages, it may be apt to consider Moorea and Tahiti in a more integrated fashion, where proposed conservation initiatives on one of the islands are evaluated within a collective Windward Island genealogical context. This may be especially pertinent in the case of the genealogically-linked surviving lineages of P. taeniata, P. hyalina and P. clara, but it is also potentially relevant for conservation measures involving Thaitian montane refuges where snails with robust phylogenetic ties to extirpated Moorean lineages still persist (Figure 6). Multi-island genealogical perspectives will probably prove to be of proactive conservation value not only for Windward Island partulids, but also for the critically endangered terrestrial biotas of many other Pacific hot spot archipelagoes [47, 48].
J.B. Burch and associates sampled Moorean partulids in October 1970 at 13 stations (Figure 9). Specimens of all nominal Moorean partulid species except for Partula tohiveana and Samoana attenuata were airmailed alive to the University of Michigan Museum of Zoology (UMMZ) where foot tissues were lyophilized and shells retained as vouchers. We selected 125 lyophilized Moorean individuals for genotyping based on Crampton's species and subspecies-level taxonomy (Figure 10; Additional File 3). From 1980 to 1985, emergency field sampling of six populations (Figure 9) led to the establishment of a number of captive Moorean tree snail lines [15, 17]. Sixteen captive snails representing five Moorean Partula species [P. mirabilis, P. mooreana, P. tohiveana, P. taeniata (subspecies P. t. nucleoli, and P. t. simulans) and P. suturalis (subspecies P. s. vexillum and P. s. strigosa)] were supplied by the International Partulid Conservation Programme for genotyping. From 2002–2006, a small number of biopsied tissue samples were obtained from extant Moorean populations, preserved in 95% ethanol and forwarded for genotyping (Figure 10). These included a specimen of Samoana attenuata from immediately below the Afareaito Partula Reserve in the upper Oponuhu Valley and specimens of newly discovered Partula taeniata populations from a variety of locations: Maatea, Haumi and Moruu valleys; a mangrove fern habitat in Opunohu Bay; and two temporally distinct (2002, 2006) samples from just below (1150 m) the summit (1207 m) of Mt. Tohiea, the highest point on the island (Figure 9, Additional File 3). Biopsies from newly discovered extant Tahitian populations of P. clara (Tiapa Valley), S. attenuata (Haapupni Valley) and putative S. burchi (Mt. Atara, Mt. Aorai) and S. diaphana (Mt. Aorai, Mt. Pihaaiateta) that were not included in previous studies [36, 37] were also genotyped.
Total genomic DNA was isolated using a DNeasy Tissue Kit (Qiagen) according to the manufacturer's instructions. A 655 nucleotide (nt) mt COI target fragment was amplified with GoTaq DNA Polymerase (Promega, Madison, WI) using the ''universal'' primer pair LCO1490/HCO2198  and a negative control (no template) was included in each amplification run. After 2 min denatuation at 95°C, an initial annealing temperature of 65°C was decreased by 2°C/cycle (30 sec denaturing at 95°C, 40 sec annealing and 1 min extension at 72°C) until the final annealing temperature (45°C) was reached and subsequently maintained for an additional 30 cycles. Double-stranded products were isolated on 1% agarose gels, excised over UV light, and extracted using a QIAquick gel extraction kit (Qiagen, Valencia, CA). Both strands of the amplified fragments were directly cycle-sequenced, using the PCR primers, by the University of Michigan's Sequencing Core Facility. All DNA sequences obtained have been deposited in GenBank (EU832996–EU833099).
The resulting chromatograms were edited by comparing both strands using Sequence Navigator 1.0.1 (Applied Biosystems, Foster City, CA). COI sequences were aligned easily due to an absence of indels. Maximum likelihood (ML) analyses were performed using PAUP*4.0b10  under the TVM+I+G model of sequence evolution, the best-fit model selected by Akaike Information Criterion implemented in Modeltest 3.7 . Likelihood parameters [base frequencies (A = 0.3300, C = 0.1064, G = 0.1354, T = 0.4282); rate matrix (1.1933, 27.6197, 1.8944, 0.4618, 27.6197, 1); shape of gamma distribution = 1.2494; proportion of invariable sites = 0.5742] found in Modeltest were used and heuristic searches were employed by using a neighbor-joining starting tree and nearest neighbor interchange (NNI) branch swapping. The partulid genus Eua, restricted to central Pacific islands in Samoa, American Samoa and Tonga, was used as the outgroup . Initial searches found two ML trees with a log-likelihood (ln L) value of -9968.9197. Both trees were further used as starting trees for another round of heuristic search and a single ML tree (ln L = -9967.6214) was recovered.
Bayesian posterior probabilities and parsimony bootstrap were employed to measure nodal support. Parsimony bootstrapping  was done with the "fast" stepwise-addition option for heuristic searches (1000 replicates) using PAUP*. Bayesian analyses were performed using MrBayes 3.1.2  set for the GTR+Γ+I model. Model parameters were treated as unknown and were estimated for each analysis. Four chains were run simultaneously for 1,000,000 generations and trees were sampled every 100 cycles. Posterior probability values were estimated by generating a 50% majority rule consensus tree after the burn-in period of 2,000 using PAUP*.
This work was supported by NSF DEB-0425984 award to D. Ó Foighil and J.B. Burch and by a La Direction de l'Environnement de Polynésie Française grant to T. Coote. Collection of the museum specimens was supported by NSF awards GB-3974 and GB-6450 (1965–71) to Y. Kondo. J. Murray identified the extant Mt. Tohiea Partula taeniata simulans specimen and G. Lindsay lyophilized the Burch Moorean snail samples in 1970. Our thanks to B. Holland who kindly supplied the tissue biopsy and photograph of the Mt. Pihaiateta Samoana diaphana specimen and the Academy of Natural Science Philadelphia for a loan of Crampton's Partula clara incrassa voucher specimens.
- Paulay G: Biodiversity on oceanic islands – its origin and extinction. Am Zool. 1994, 34: 134-144.View ArticleGoogle Scholar
- Baldwin BG, Sanderson MJ: Age and rate of diversification of the Hawaiian silversword alliance. Proc Natl Acad Sci USA. 1998, 95: 9402-9406. 10.1073/pnas.95.16.9402.PubMed CentralView ArticlePubMedGoogle Scholar
- Gillespie RG, Roderick GK: Arthropods on islands: evolution and conservation. Ann Rev Entomol. 2002, 47: 595-632. 10.1146/annurev.ento.47.091201.145244.View ArticleGoogle Scholar
- Trewick SA, Cowie RH: Theme Issue "Evolution on Pacific islands: Darwin's legacy". Philos Trans R Soc B. 2008, 363: 3289-34654. 10.1098/rstb.2008.0127.View ArticleGoogle Scholar
- Carlquist S: Island Biology. 1974, New York: Columbia University PressView ArticleGoogle Scholar
- Solem A: Biogeographic significance of land snails. Historical Biogeography, Plate Tectonics, and The Changing Environment. Edited by: Gray J, Boucot AJ. 1979, Corvallis: Oregon State University Press, 277-287.Google Scholar
- Vermeij GJ: Inequality and the directionality of history. Am Nat. 1999, 153: 243-253. 10.1086/303175.View ArticleGoogle Scholar
- Hadfield MG, Miller SE, Carwile AH: The decimation of endemic Hawai'ian tree snails by alien predators. Am Zool. 1993, 33: 610-622.View ArticleGoogle Scholar
- Pimm SL, Moulton MP, Justice LJ: Bird extinctions in the central Pacific. Philos Trans R Soc B. 1994, 344: 27-33. 10.1098/rstb.1994.0047.View ArticleGoogle Scholar
- Clarke B, Murray J, Johnson MS: The extinction of endemic species by a program of biological control. Pac Sci. 1984, 38: 97-104.Google Scholar
- Cowie RH: Evolution and extinction of Partulidae, endemic Pacific island snails. Philos Trans R Soc B. 1992, 335: 167-191. 10.1098/rstb.1992.0017.View ArticleGoogle Scholar
- Cowie RH: Can snails ever be effective and safe biocontrol agents?. Int J Pest Manage. 2001, 47: 23-40. 10.1080/09670870150215577.View ArticleGoogle Scholar
- Coote T, Loève E: From 61 species to five: endemic tree snails of the Society Islands fall prey to an ill-judged biological control programme. Oryx. 2003, 37: 91-96. 10.1017/S0030605303000176.View ArticleGoogle Scholar
- Coote T: Partulids on Tahiti: differential persistence of a minority of endemic taxa among relict populations. Am Malacol Bull. 2007, 22: 83-87. 10.4003/0740-2783-22.1.83.View ArticleGoogle Scholar
- Murray J, Murray E, Johnson MS, Clarke B: The extinction of Partula on Moorea. Pac Sci. 1988, 42: 150-153.Google Scholar
- Tonge S, Bloxam Q: A review of the captive-breeding programme for Polynesian tree snails Partula spp. Internat Zoo Yearbook. 1991, 30: 51-59. 10.1111/j.1748-1090.1991.tb03465.x. [http://www3.interscience.wiley.com/journal/119371532/abstract?CRETRY=1&SRETRY=0]View ArticleGoogle Scholar
- Pearce-Kelly P, Clarke D, Walker C, Atkin P: A conservation programme for the partulid tree snails of the Pacific Region. Mem Natl Mus Victoria. 1997, 56: 431-433.Google Scholar
- Coote T, Clarke D, Hickman CS, Murray J, Pearce-Kelly P: Experimental release of endemic Partula species, extinct in the wild, into a protected area of natural habitat on Moorea. Pac Sci. 2004, 58: 429-434. 10.1353/psc.2004.0028.View ArticleGoogle Scholar
- Garrett A: The terrestrial Mollusca inhabiting the Society Islands. Nat Sci Phila (Ser. 2). 1884, 9: 17-114.Google Scholar
- Crampton HE: Studies on the variation, distribution and evolution of the genus Partula. The species inhabiting Tahiti. Carnegie Inst Wash Pub. 1916, 228: 1-311.Google Scholar
- Crampton HE: Studies on the variation, distribution and evolution of the genus Partula. The species inhabiting Moorea. Carnegie Inst Wash Pub. 1932, 410: 1-335.Google Scholar
- Murray J, Clarke B: The genus Partula on Moorea: speciation in progress. Proc R Soc B. 1980, 211: 83-117. 10.1098/rspb.1980.0159.View ArticleGoogle Scholar
- Murray J, Clarke B, Johnson MS: Adaptive radiation and community structure of Partula on Moorea. Proc R Soc B. 1993, 252: 205-211. 10.1098/rspb.1993.0147.View ArticleGoogle Scholar
- Johnson MS, Murray J, Clarke B: The ecological genetics and adaptive radiation of Partula on Moorea. Oxford Surv Evolut Biol. 1993, 9: 167-236.Google Scholar
- Murray J, Stine OC, Johnson MS: The evolution of mitochondrial DNA in Partula. Heredity. 1991, 66: 93-104. 10.1038/hdy.1991.12.View ArticleGoogle Scholar
- Clarke B, Johnson MS, Murray J: Clines in the genetic distance between two species of island land snails: how "molecular leakage" can mislead us about speciation. Philos Trans R Soc B. 1996, 351: 773-784. 10.1098/rstb.1996.0072.View ArticleGoogle Scholar
- Goodacre SL: Genetic variation in a Pacific Island land snail: population history versus current drift and selection. Proc R Soc B. 2001, 268: 121-126. 10.1098/rspb.2000.1339.PubMed CentralView ArticlePubMedGoogle Scholar
- Goodacre SL: Population structure, history and gene flow in a group of closely related land snails: genetic variation in Partula from the Society Islands of the Pacific. Mol Ecol. 2002, 11: 55-68. 10.1046/j.0962-1083.2001.01422.x.View ArticlePubMedGoogle Scholar
- Coote T, Loève E, Meyer JY, Clarke D: Extant populations of endemic partulids on Tahiti, French Polynesia. Oryx. 1999, 33: 215-222.View ArticleGoogle Scholar
- Lee T, Meyer JY, Burch JB, Pearce-Kelly P, Ó Foighil D: Not completely gone: two partulid tree snail species persist on the highest peak of Raiatea, French Polynesia. Oryx. 2008, 42: 615-619. 10.1017/S0030605308001427.View ArticleGoogle Scholar
- Clarke B: Balanced polymorphism and regional differentiation in land snails. Evolution and the Environment. Edited by: Drake ET. 1968, New Haven: Yale University Press, New Haven, 351-368.Google Scholar
- Clarke B, Murray J: Ecological genetics and speciation in land snails of the genus Partula. Biol J Linn Soc. 1969, 1: 31-42. 10.1111/j.1095-8312.1969.tb01810.x.View ArticleGoogle Scholar
- Kondo Y: Samoana of the Society Islands (Pulmonata: Partulidae). Malac Rev. 1973, 6: 19-33.Google Scholar
- Goodacre SL, Wade CM: Patterns of genetic variation in Pacific island land snails: the distribution of cytochrome b lineages among Society Island Partula. Biol J Linn Soc. 2001, 73: 131-138. 10.1111/j.1095-8312.2001.tb01351.x.View ArticleGoogle Scholar
- Johnson MS, Murray J, Clarke B: An electrophoretic analysis of phylogeny and evolutionary rates in the genus Partula from the Society Islands. Proc R Soc B. 1986, 227: 161-177. 10.1098/rspb.1986.0017.View ArticleGoogle Scholar
- Lee T, Burch JB, Jung Y, Coote T, Pearce-Kelly P, Ó Foighil D: Tahitian tree snail mitochondrial clades survived recent mass-extirpation. Curr Biol. 2007, 17: R502-R503. 10.1016/j.cub.2007.05.006.View ArticlePubMedGoogle Scholar
- Lee T, Burch JB, Coote T, Fontaine B, Gargominy O, Pearce-Kelly P, Ó Foighil D: Prehistoric inter-archipelago trading of Polynesian tree snails leaves a conservation legacy. Proc R Soc B. 2007, 272: 2907-2914. 10.1098/rspb.2007.1009.View ArticleGoogle Scholar
- Cooke CM, Crampton HE: New species of Partula. B P Bishop Mus Occ Papers. 1930, 9: 3-5.Google Scholar
- Kondo Y: Partulidae: preview of anatomical revision. Nautilus. 1968, 81: 73-77.Google Scholar
- Johnson MS, Murray J, Clarke B: Parallel evolution in Marquesan partulid land snails. Biol J Linn Soc. 2000, 69: 577-598. 10.1006/bijl.1999.0386.View ArticleGoogle Scholar
- Goodacre SL, Wade CM: Molecular evolutionary relationships between partulid land snails of the Pacific. Proc R Soc B. 2001, 268: 1-7. 10.1098/rspb.2000.1322.PubMed CentralView ArticlePubMedGoogle Scholar
- Wade CM, Mordan PB, Clarke B: A phylogeny of the land snails (Gastropoda: Pulmonata). Proc R Soc B. 2001, 268: 413-422. 10.1098/rspb.2000.1372.PubMed CentralView ArticlePubMedGoogle Scholar
- Johnson MS, Murray J, Clarke B: High genetic similarities and low heterozygosities in land snails of the genus Samoana from the Society Islands. Malacologia. 1986, 27: 97-106.Google Scholar
- Gerlach J: The ecology of the carnivorous snail Euglandina rosea. D. Phil. thesis. 1994, Oxford University, Oxford, UKGoogle Scholar
- Gerlach J: Predator, prey and pathogen interactions in introduced snail populations. Anim Conserv. 2001, 4: 203-209. 10.1017/S136794300100124X.View ArticleGoogle Scholar
- Mace GM, Purvis A: Evolutionary biology and practical conservation: bridging a widening gap. Mol Ecol. 2008, 17: 9-19. 10.1111/j.1365-294X.2007.03455.x.View ArticlePubMedGoogle Scholar
- Cowie RH, Holland BS: Molecular biogeography and diversification of the endemic terrestrial fauna of the Hawaiian Islands. Philos Trans R Soc B. 2008, 363: 3363-3376. 10.1098/rstb.2008.0061.View ArticleGoogle Scholar
- Gillespie RG, Claridge EM, Goodacre SL: Biogeography of the fauna of French Polynesia: diversification within and between a series of hot spot archipelagos. Philos Trans R Soc Lond B. 2008, 363: 3335-3346. 10.1098/rstb.2008.0124.View ArticleGoogle Scholar
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhork R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994, 3: 294-299.PubMedGoogle Scholar
- Swofford DL: PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. 2003, Sunderland, MA: Sinauer AssociatesGoogle Scholar
- Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14: 817-818. 10.1093/bioinformatics/14.9.817.View ArticlePubMedGoogle Scholar
- Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985, 39: 783-791. 10.2307/2408678.View ArticleGoogle Scholar
- Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.