Biological Invasions

, Volume 14, Issue 3, pp 735–742 | Cite as

Genetic population assignment reveals a long-distance incursion to an island by a stoat (Mustela erminea)

Original Paper

Abstract

When new individuals from a pest species are detected after an eradication programme, it is important to determine if these individuals are survivors from the eradication attempt or reinvaders from another population, as this enables managers to adjust and improve the methodologies for future eradications and biosecurity. Rangitoto/Motutapu Islands in the Hauraki Gulf (New Zealand) had a multispecies mammalian pest eradication conducted in 2009. A year after this eradication a single stoat was trapped on the island. Using genetic population assignment we conclude that this individual was a reinvader, which probably swam a minimum distance of 3 km from the adjacent mainland. This swimming distance is greater than any previously known stoat incursions. Our results suggest that the original population on these islands was from natural dispersal rather than anthropogenic introduction and that it had some limited ongoing mixing with the mainland population. These findings highlight the invasion/reinvasion potential of stoats across large stretches of water, and will necessitate ongoing biosecurity indefinitely for these islands. The study also highlights the utility of genetic assignment techniques for assessing reinvasion, and emphasizes the need for pre-eradication genetic sampling of all pest species to enable such analyses to be carried out.

Keywords

Conservation Eradication Island Microsatellite New Zealand Reinvasion 

Introduction

Eradicating invasive species and preventing reinvasion is a common goal for ecological restoration programs and this is often easier to achieve on islands because of their isolation (Courchamp et al. 2003; Towns and Broome 2003; Clout and Russell 2008). When pests reappear after an eradication attempt, determining whether they are survivors or re-invaders can have important implications for management: either quarantine or eradication procedures may need to be modified. When there is a long time between eradication and the reappearance of pests it can usually be assumed that the new individuals are re-invaders, but when pests reappear soon after “eradication” it may not be clear whether they are re-invaders or survivors of a failed eradication attempt (Abdelkrim et al. 2005; Abdelkrim et al. 2007; Russell et al. 2008).

Genetic techniques can provide vital information on the origin of invasive species populations, the underlying genetic population structure, and the levels of dispersal within and between populations (Robertson and Gemmell 2004; Rollins et al. 2006; Schwartz et al. 2007). Genetic population assignment provides a method for determining an individual’s source population, and is now a widely used tool in ecology (Davies et al. 1999). These assignment methods compute the probability of finding the genotype of a given individual within each of a sampled set of populations, and can be used to select or exclude populations as possible sources for the individual (Manel et al. 2005). In situations where pests have been detected post-eradication, these genetic techniques have been successfully used to determine the origin of these individuals (Kim et al. 2010; Abdelkrim et al. 2007; Russell et al. 2010).

Stoats (Mustela erminea) were introduced to New Zealand in 1884 (Thomson 1922) to control rabbits (Oryctolagus cuniculus). Since then stoats have had well-documented catastrophic effects on native New Zealand birds (King and Powell 2007). They are the primary nest predator in both alpine grasslands and beech forests (Smith et al. 2008) and they are a primary agent of decline for over half of all forest birds of New Zealand currently threatened or significantly declining (Innes et al. 2010). They pose one of the highest invasion risks to islands (Elliott et al. 2010; Veale et al. in press). There are numerous eye witness accounts of stoats swimming hundreds of meters from shore (Wodzicki and Bull 1951; Fitzgerald 1978; King and Moors 1979) and swimming is believed to be their primary island invasion pathway (Taylor and Tilley 1984; Veale et al. in press). The best-documented series of invasions have been on Maud Island 900 m offshore in the Marlborough Sounds where there have been three separate invasions by pregnant female stoats since 1982, resulting in a total of 18 stoats caught on the island. The first of these invasions extirpated the South Island Saddleback (Philesturnus caruncalatus) population on the island (King and Powell 2007). Due to the dramatic effects of stoat invasion, maintaining the stoat free status of islands is important for ecological restoration programs on New Zealand islands (Atkinson 2001; Parkes and Murphy 2003; Bellingham et al. 2010).

Rangitoto Island (2,321 ha, 174°52′E, 36°47′S) and Motutapu Island (1,560 ha, 174°55′E, 36°45′S) are in the Hauraki Gulf 3 km offshore from Auckland City, New Zealand (Fig. 1). Rangitoto is entirely forested, but Motutapu was cleared and converted to pasture in the late nineteenth century and is currently farmed. They are linked to each other by a causeway and both islands are popular public reserves visited by regular ferry services and private recreational boats. Prior to 2009 these islands supported a range of invasive mammals including mice (Mus musculus), ship rats (Rattus rattus), hedgehogs (Erinaceus europaeus), rabbits, feral cats (Felis catus) and stoats. Stoats had been present on Rangitoto since at least 1939 (Andrew Sharpe personal communication), though they had rarely been observed until the mid 1990s, when they became more regularly seen, around the time of a successful possum and wallaby eradication (Shirley Collins pers comm.). The swimming range of stoats is commonly believed to be 1.5 km (Taylor and Tilley 1984; Mckinlay 1997). Since Rangitoto/Motutapu is 3 km offshore most authors have assumed that stoats were deliberately introduced there, although no record exists of any such introduction.
Fig. 1

Map of the Auckland region, showing islands mentioned in the text and the distances between Rangitoto/Motutapu and nearby land

In July 2009 an attempt was made to remove the full suite of invasive mammals from the island including stoats. Standard aerial brodifacoum baiting methods were used for rodents, combined with subsequent trapping and shooting for predators that had not succumbed to secondary poisoning. After the poison operation, spotlighting, dog teams and trapping detected no live stoats, and only a single stoat carcass was found. No stoat sign was detected for the next 11 months, but in July 2010 a single adult male stoat was caught in a trap on Rangitoto almost a year after the poison drop. Given the dramatic potential effects of stoat reinvasion, it is important to determine if this stoat survived the poison drop and avoided trapping and detection for a year, or alternatively if it reinvaded from another source population.

Materials and methods

Sampling

Stoat trapping was not undertaken on Rangitoto or Motutapu prior to the aerial poisoning operation as there was a perceived risk of creating trap-shy animals (Richard Griffiths pers. comm.). Non-invasive genetic sampling in the month leading up to the eradication obtained 260 hair samples from across Rangitoto/Motutapu using hair tubes (see Gleeson et al. 2010 for methods). Hair samples were sub-sampled for genotyping, selecting samples with large amounts of hair (to ensure ease of genotyping), and the greatest geographic spread (to maximize the number of stoats detected). Along with these hair samples, two pre-eradication tissue samples were obtained: one from a stoat caught incidentally in a rat trap a month before the poison bait drop, and another from the single stoat carcass found immediately after the poison operation.

There are two possible source populations for immigrant stoats to Rangitoto/Motutapu, the mainland and Waiheke Island (Fig. 1). Neighboring Rakino, Motukorea and Motuihe Islands are all stoat free, having had successful multispecies eradications. Stoats captured by local environmental groups from around the Auckland region were also obtained and frozen for genetic sampling. These trapping programs were located at Tawharanui, Ark in the Park, Kawakawa Bay and on Waiheke Island.

Genetics

At least ten hairs per sample were isolated from each hair tube sample (samples were collected from distinct clumps to ensure only single individuals contributed). Tissue samples were dissected in the laboratory, where 50 mg of muscle tissue and caudal skin were removed. DNA was then isolated from both sample types, using a Bio-Rad AquaPure Genomic Tissue Kit (Cat# 732-6343) following the manufacturer’s protocol, and re-suspended in 100 μl of supplied buffer.

All samples were genotyped at seventeen microsatellite loci (Table 1). A total of 28 hair samples were genotyped from the pre-eradication Rangitoto/Motutapu population, along with the two tissue samples. Twenty samples combined from the three mainland sites and six samples from Waiheke Island were also genotyped.
Table 1

Variable microsatellite loci used for stoat genotyping

Loci names

References

MER005, MER030, MER022, MER041, MER009, MER082

Fleming et al. (1999)

MVI057

O’Connell et al. (1996)

WE3, WE7, WE8

Huang et al. (2007)

MLUT27, MLUT32

Cabria et al. (2007)

MAI

Davis and Strobeck (1998)

MEL1, MEL4

Bijlsma et al. (2000)

RI011, RI019

Beheler et al. (2005)

PCR amplifications were performed in 25-μl reactions containing 1 μl of DNA extract, 1× PCR buffer with MgCl2 (50 mM Tris/HCl, 10 mM KCl, 5 mM [NH4]2SO4, 2 mM MgCl2, pH 8.3), 200 μM of each dNTP, 10 μM of each primer, and 2 μl of FastStart Taq DNA Polymerase (Roche Diagnostics). Amplification conditions on a GeneAmp PCR System 9,700 thermocycler (Applied Biosystems) were: initial denaturation at 95°C for 4 min; 10 touchdown cycles of 20 s at 94°C, 20 s at 62–58°C, 20 s at 74°C; 40 cycles of 20 s at 94°C, 20 s at 58°C, 20 s at 74°C, and a final extension of 40 min at 72°C. The 5′-end of the forward primer of each pair was fluorescently labelled with either 6FAM, NED, or VIC dyes (Applied Biosystems) and amplification products were separated using capillary electrophoresis (ABI PRISM 310). Alleles were sized relative to an internal size standard (GS-350 ROX) using GENESCAN 3.1 (Applied Biosystems). The genotype profiles were analysed using the software GENOTYPER Version 2.5 (Applied Biosystems).

Genotyping for the hair samples was carried out using a step-wise protocol of exclusion that has been shown elsewhere to ensure rigorous and conservative determination of identity (Paetkau 2003; Weaver et al.2005). We required a perfect match between two PCR amplifications in order to accept that genotype in order to eliminate PCR errors resulting in either allelic drop-out or false alleles. Any samples that differed by one locus were checked for any potential errors as either scoring or amplification errors (Paetkau 2003). If these differences could not be explained by errors in scoring/typing, samples were then subjected to a further round of PCR and scoring (Poole et al. 2001; Mowat and Paetkau 2002). We used the software package Genalex 6.4 (Peakall and Smouse 2006) to estimate PID and PID-sib among full siblings as that provides an upper limit to the probability that pairs of individuals will share genotypes (Taberlet and Luikart 1999).

Statistical analysis

For the three populations we calculated allele frequencies, observed heterozygosities, and mean number of alleles per locus as summaries of genetic diversity. Our assignment methods rely on assumptions of Hardy–Weinberg proportions and no linkage disequilibrium, so we checked these in each population using Fisher’s exact tests. We also estimated FIS and FST for each population. All calculations were performed in Arlequin 3.5 (Excoffier and Lischer 2010).

For genetic assignment analysis, we used GeneClass2 (Piry et al. 2004), implementing the Bayesian assignment criterion of Rannala and Mountain (1997). This criterion was recommended by Cornuet et al. (1999) as the best of a set of assignment criteria, and they specifically demonstrated high assignment accuracy for samples as small as ours. For the post-eradication Rangitoto stoat, the criterion gives a posterior probability of finding this stoat’s genotype in the pre-eradication Rangitoto/Motutapu Island population (survivor hypothesis), and of finding the stoat’s genotype in either the mainland or Waiheke Island populations (reinvader hypotheses). We present the assignment results graphically following the methodology of Russell et al. (2010). The two-dimensional scatterplot created displays the clustering of samples, and the orders of magnitude spanning the posterior probabilities. This information is lost by compressing the two-dimensional points into the one one-dimensional score values provided by GeneClass2.

Results

From the 28 hair samples genotyped from the pre-eradication Rangitoto/Motutapu population, 14 haplotypes were detected. Discriminatory power between individuals was high (PID = 5.8 × 10−9 and PID-sib = 1.6 × 10−4) therefore hair samples with identical haplotypes were regarded as recaptures of the same individual. The 14 individual haplotypes from the hair samples combined with the two tissue haplotypes (neither of which matched any hair samples) gave a pre-eradication genetic sample size of 16 stoats (Fig. 2).
Fig. 2

Map of Rangitoto Is. & Motutapu Is., showing the locations of hair samples genotyped from individual stoats (numbers 1–14). Dots indicate hair-sampling tube locations. Also shown are the locations of the two tissue samples (A and B) and the location of the post-eradication capture (star)

All individuals from the three populations were genotyped for 17 loci. The mainland population had the highest genetic diversity, in terms of heterozygosity, number of alleles and number of private alleles (Table 2). Significant genetic differentiation was found between the pre-eradication Rangitoto/Motutapu population and the two other populations (FST >0.05; Table 3).
Table 2

Genetic properties of the three sampled populations

 

Mainland

Rangitoto/Motutapu

Waiheke

No. of gene copies

40

32

12

No. of loci

17

17

17

Missing data

0

0

0

No. of polymorphic loci

17

16

14

Mean heterozygosity/locus

0.588

0.492

0.455

Mean no. of alleles/locus

3.941

3.176

2.412

Private alleles

20

4

0

Table 3

F-statistics for the pre-eradication Rangitoto/Motutapu population and the two potential source populations

 

Mainland

Rangitoto/Motutapu

Waiheke

Mainland

0.133

0.113

0.16

Rangitoto/Motutapu

 

0.16

0.151

Waiheke

  

−0.87

Diagonal values are FIS, off-diagonal values are FST

All individuals of known origin were assigned correctly to their source population (Figs 3, 4), and as a leave-one-out procedure was used to place samples of known origin, this served to cross-validate the assignment procedure. Data for all but one stoat lay outside the dashed lines, thus under the Bayesian assignment criterion of Rannala and Mountain (1997), they had a GeneClass2 assignment score of 0.9 or greater for the favoured population, and 0.1 or below for the other population. The one exception was still assigned correctly, but had a few less common alleles leading to a less certain assignment.
Fig. 3

Log posterior probability plot for stoats from the pre-eradication Rangitoto/Motutapu population and the mainland population. Triangles indicate pre-eradication stoats, circles indicate mainland stoats, and the post-eradication stoat is indicated by a diamond. Points below the solid diagonal line have greater posterior probability of belonging to the mainland than to Rangitoto/Motutapu. Points outside the dashed diagonal lines have over nine times greater posterior probability of belonging to one population than the other

Fig. 4

Log posterior probability plot for stoats from the pre-eradication Rangitoto/Motutapu population and the Waiheke Island population. Triangles indicate pre-eradication stoats, squares indicate Waiheke Island stoats and the post-eradication stoat is indicated by a diamond. Points below the solid diagonal line have greater posterior probability of belonging to Waiheke Island than to Rangitoto/Motutapu Is. Points outside the dashed diagonal lines have over nine times greater posterior probability of belonging to one population than the other

From the log posterior genotype probability plots, the post-eradication stoat caught on Rangitoto clearly grouped genetically with the mainland stoats, and did not group with the pre-eradication Rangitoto/Motutapu samples (Fig. 3) (Geneclass score >0.99). Indeed it is less similar to the pre-eradication samples than over half of the mainland samples, and had alleles not present in the pre-eradication population sample. It also clearly did not group with the Waiheke Island stoat population (Fig. 4), which was genetically distinct from both the pre-eradication Rangitoto/Motutapu population, and the mainland population.

Discussion

Using genetic assignment methods we have demonstrated clear discrimination between mainland and island populations despite relatively small sample sizes. With this strong genetic signal, we were able to confidently assign the post-eradication Rangitoto stoat to the mainland population. This supports the hypothesis that this stoat arrived from the mainland, presumably by swimming a distance of at least 3 km. Our results show there is a risk of reinvasion of Rangitoto/Motutapu and many other islands around New Zealand that were previously thought to be outside the swimming range of stoats. Subsequent to this incursion on Rangitoto, stoats have been detected and caught on Kapiti Island (New Zealand), which is a distance of 5.2 km offshore. While it is not possible to know with certainty the invasion pathway, it is plausible that stoats arrived there by swimming, extending the risk to islands further offshore.

An alternative hypothesis as to how the reinvading stoat arrived on Rangitoto is that it was a stowaway. This hypothesis seems unlikely given that stoats have never been recorded on boats, nor have they been detected on islands that are clearly not reachable by swimming yet have high levels of boat activity, such as Great Barrier Island (15.7 km from the mainland). Stoats are good swimmers, and their distribution on islands is correlated only with two factors that affect swimming dispersal (distance offshore and island area), and is not correlated with any anthropogenic factors such as wharfs or human activity (Veale et al. in press).

While this apparent stoat re-invasion means it will be necessary to maintain ongoing surveillance, the fact that the stoat was caught suggests that the current trapping program is adequate. The stoat captured post eradication was caught in a coastal trap near a likely entry point, in a relatively sheltered area of Rangitoto, and near the closest point to the mainland. The fact that the stoat is likely to have come from a developed suburban area is somewhat surprising, although not unheard of. It has been previously found that domestic cats in suburban areas near forested parks in Auckland occasionally prey upon stoats (Gillies 1998), and stoats have been seen in the larger forested parks on Auckland’s North Shore (pers. comm. Mel Galbraith).

The genetic differentiation between the pre-eradication Rangitoto/Motutapu population and the mainland population suggests that these populations were relatively isolated before the eradication. Genetic population assignment would have been less successful if there had been more significant gene flow between them. This indicates either that incursions are relatively infrequent, or that incursions are rarely successful, with new individuals not likely to survive and reproduce because the island is already at carrying capacity (Granjon and Cheylan 1989). The genetic results do provide compelling evidence that the Rangitoto stoat population was founded by natural dispersal rather than a deliberate introduction, and that there has been some ongoing immigration from the mainland, given the relatively high genetic diversity observed. This supposition is supported by historical information, as during the period that stoats could have been introduced, the owners of Motutapu were introducing game birds, and rabbit levels were relatively low (Thomson 1922). Given these factors it seems highly unlikely that stoats would have been deliberately introduced.

Pre-eradication sampling was critical in enabling population assignment in this case. The hair tube sampling conducted immediately prior to the eradication was fortuitous as no pre-eradication sampling had been planned. We urge all pest managers undertaking eradication projects to include the collection of a spatially representative sample of all target species pre-eradication. The genetic lab-work need not be performed until there is a subsequent detection. The minor cost of pre-eradication sampling is outweighed by the potential cost of unfocused remedial action. In this case we have learnt that eradication of stoats from large islands using secondary poisoning via rodents is possible, but that ongoing trapping will be required to keep this particular island stoat-free.

Notes

Acknowledgments

We thank Rachel Fewster and Andrea Byrom for their assistance in the planning and analysis of this project. Thanks to Richard Griffiths (Department of Conservation) and his team on Rangitoto/Motutapu, and Ark in the Park, Weka Watch, Auckland Council and Rob Morton for stoat samples. Also thanks to the hair tube team: Adam Field, Amy Holliday, Anya Elgort, Chloe McLaren, Daniel Laird, Josh Guilbert, Katrina Parry, Louis Scarrold, Oliver Hannaford, Owen Lee and Stan Woodhouse.

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Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Centre for Biodiversity and Biosecurity, School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  2. 2.Ecological Genetics LaboratoryLandcare ResearchAucklandNew Zealand

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