Biol Invasions (2015) 17:3183–3195 DOI 10.1007/s10530-015-0944-x ORIGINAL PAPER Extinction of an introduced warm-climate alien species, Xenopus laevis, by extreme weather events Richard C. Tinsley . Lucy C. Stott . Mark E. Viney . Barbara K. Mable . Matthew C. Tinsley Received: 22 January 2015 / Accepted: 6 July 2015 / Published online: 16 July 2015 Ó The Author(s) 2015. This article is published with open access at Springerlink.com Abstract Invasive, non-native species represent a body size; maximum longevity exceeds 23 years. major threat to biodiversity worldwide. The African Nevertheless, areas of distribution remained limited, amphibian Xenopus laevis is widely regarded as an with numbers\500 in each population. In 2010, only a invasive species and a threat to local faunas. Popula- single individual was captured at each locality and tions originating at the Western Cape, South Africa, further searching failed to record any others in have been introduced on four continents, mostly in repeated sampling up to 2014. We conclude that both areas with a similar Mediterranean climate. Some populations are now extinct. The winters of introduced populations are also established in cooler 2009–2010 and 2010–2011 experienced extreme cold environments where persistence for many decades and drought (December 2010 was the coldest in suggests a capacity for long-term adaptation. In these 120 years and the third driest in 100 years). The cases, recent climate warming might enhance invasion extinction of X. laevis in these areas indicates that even ability, favouring range expansion, population growth relatively long-established alien species remain vul- and negative effects on native faunas. In the cool nerable to rare extreme weather conditions. temperate UK, populations have been established for about 50 years in Wales and for an unknown period, Keywords Invasive species Á Xenopus laevis Á probably [20 years, in England (Lincolnshire). Our Extinction Á Climate change Á Extreme weather field studies over 30 and 10 years, respectively, show that in favourable conditions there may be good recruitment, fast individual growth rates and large Introduction R. C. Tinsley (&) Á L. C. Stott Á M. E. Viney School of Biological Sciences, Life Sciences Building, Two topics are prominent in the current ecological University of Bristol, Bristol BS8 1TQ, UK literature: climate change and invasive species. Recent e-mail: [email protected] climate change has been characterised both by increased warming and by increased frequency of B. K. Mable Institute of Biodiversity, Animal Health and Comparative ‘extreme events’. The latter are illustrated for England Medicine, University of Glasgow, Glasgow G12 8QQ, by the coldest and driest winter for 100 years (2010/ UK 2011), the highest annual rainfall for 100 years (2012), the coldest spring for 50 years (2013), the wettest M. C. Tinsley School of Biological and Environmental Sciences, winter for over 250 years (2013/2014). Overall, 2014 University of Stirling, Stirling FK9 4LA, UK was the warmest year since records began in 1659 123 3184 R. C. Tinsley et al. (The Central England Temperature series; http:// et al. 2009; Solı´s et al. 2010; Vredenburg et al. 2013; www.metoffice.gov.uk/climate/uk), and was also the but see also Tinsley et al. 2015). warmest year ever recorded worldwide (data for In the UK, there have only been two well- 1880–2014) (http://www.noaa.gov). These episodes established populations of X. laevis: in Glamorgan, can be predicted to have profound effects on the fauna Wales, and Lincolnshire, England. A third, on the Isle of affected regions, either releasing environmental of Wight, was introduced in the 1960s but is now checks on life history traits or leading to extinction of probably extinct (Tinsley et al. 2015). The responses species that are vulnerable to perturbation outside of the relevant government environmental authorities narrow environmental boundaries. Invasive non-na- to the extant populations differed in the two regions. In tive species are considered the second biggest threat Wales, there was no formal reaction to the presence of after habitat loss to biodiversity worldwide; damage a breeding colony, and research published during caused by invasive species globally amounts to almost 25 years did not attract conservation concerns. As a 5 % of the world economy (Defra 2008). result, there is a substantial body of ecological findings These themes of climate change and invasive including diet, growth rates, age determination, pop- species may converge in cases of species transfers ulation biology and parasite infection (Tinsley and between different climate zones. Short- and long-term McCoid 1996; Measey and Tinsley 1998; Measey changes in climate parameters may have strong 1998, 2001; Tinsley and Jackson 1998; Tinsley et al. positive or negative effects on the abundance and 2011a, b, 2012). When X. laevis was recorded in distribution of translocated species. The literature Lincolnshire, English Nature (now Natural England) highlights a wide diversity of species that may become began a programme in 2003 to eliminate the colony. invasive following introduction to new geographical Their approach excluded any allowance for compiling or climate regions (e.g. Davis 2009). Some amphib- baseline population data: the over-riding priority was ians have notoriety as invasive species, especially cane for immediate removal. So, ecological studies have toads (Rhinella marina) and North American bullfrogs been limited. In 2008, the Welsh Government adopted (Lithobates catesbeianus) (Stuart et al. 2008). The new plans following the Invasive Non-Native Species African clawed frog, Xenopus laevis, has been impor- Framework Strategy for Great Britain (Defra 2008) tant in biomedical research for over 80 years: this and an eradication programme began in 2010 in species, native to southern Africa, was employed in collaboration with the Environment Agency, Wales human pregnancy diagnosis until the 1960s and is and the Countryside Council for Wales. currently a model organism for research (Cannatella Our fieldwork, beginning in 1981 in Wales and and de Sa´ 1993; Gurdon 1996; Tinsley 2010; Furman 2001 in Lincolnshire, continued in 2010 with the et al. 2015). Release or escape into the wild of expectation that the populations in both areas would laboratory animals together with others kept as pets number several hundred individuals. However, initial has contributed to establishment of widely-distributed observations suggested that both populations might alien populations, now including the USA, Ascension have become almost or completely extinct. To Island, Chile, UK, France, Italy, Portugal and Japan confirm this, intensive searches were undertaken in (Tinsley and McCoid 1996; Lobos and Measey 2002; 2010 and 2011, aiming to survey habitats over a wide Crayon 2005; Kobayashi and Hasegawa 2005; Lobos area on multiple occasions. This account reports the and Jaksic 2005; Fouquet and Measey 2006; Faraone evidence for the conclusion that X. laevis is extinct at et al. 2008; Rebelo et al. 2010; Measey et al. 2012; both sites and interprets the likely causative factors in Lillo et al. 2013; Lobos et al. 2013). These introduc- relation to exceptional weather conditions, acting in tions are considered a threat to local faunas (e.g. conjunction with specific habitat and population Lafferty and Page 1997; Lillo et al. 2011; Amaral and characteristics. The half-century history of this alien Rebelo 2012). Recent concerns focus on the alleged species in the UK has wider conservation significance involvement of X. laevis in worldwide spread of the for assessing the ability of warm-climate introduced fungal pathogen Batrachochytrium dendrobatidis species to persist during climate fluctuations occur- implicated in extinction of vulnerable anuran species ring over decades and, especially, to survive rare (Weldon et al. 2004; Fisher and Garner 2007; Goka extreme events. 123 Extinction of an introduced warm climate alien species 3185 Methods and background Location and environmental conditions Fieldwork approach Habitat characteristics are important for understand- ing the environments in which introduced X. laevis Xenopus laevis were caught with funnel traps baited persisted in the UK and in which they ultimately went with raw meat (usually ox liver), partially submerged extinct; we provide details of the sites to illustrate in water to allow access to air by captured animals prevailing conditions. (details in Tinsley et al. 2015). Traps were set at around darkness (20:00–22:00 h), inspected at dawn Wales (04:00–05:30 h) and then typically re-set for the following day. Each period when a trap was in situ The fieldwork area centres on the Alun valley, near during the day or night is referred to below as a ‘trap- Bridgend, adjacent to the Bristol Channel (Fig. 1). A session’. Typically, on each fieldwork visit, trapping plateau of Liassic limestone (40–90 m a.s.l.) supports was repeated over several consecutive sessions (up to pasture farmland from which the river Alun descends 6 in succession in the Lincolnshire ditch and into a wooded valley in Carboniferous limestone. The Croescwtta pond) with traps set at high density drainage experiences extremes of water flow: after (usually 1.5–2 m apart). In addition, some animals prolonged periods without rain the river disappears in Lincolnshire were caught in torchlight at night into underground fissures and the riverbed is dry, but using long-handled pond nets. Numbers of X. laevis heavy rain produces torrential floods, often 1–2 m cited in the text and figures refer to adults and deep. The area has stone-built livestock watering juveniles captured (not projections of population ponds constructed in the 19th century, typically over a size); tadpole numbers were not recorded. Animals spring or seepage that maintains permanent water even caught in Wales contributed to a mark-recapture during drought. One such site is a pond at Croescwtta programme carried out over 30 years using two farm (Fig. 1k), area 110 m2, located about 400 m up- methods for individual identification.