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Changing Invaders: Trends of Gigantism in Insular Introduced Rats

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Changing Invaders: Trends of Gigantism in Insular Introduced Rats Environmental Conservation (2018) 45 (3): 203–211 C Foundation for Environmental Conservation 2018 doi:10.1017/S0376892918000085 Changing invaders: trends of gigantism in insular THEMATIC SECTION Humans and Island introduced rats Environments ALEXANDRA A.E. VAN DER GEER∗ Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands Date submitted: 7 November 2017; Date accepted: 20 January 2018; First published online 14 March 2018 SUMMARY within short historical periods (Rowe-Rowe & Crafford 1992; Michaux et al. 2007;Renaudet al. 2013; Lister & Hall 2014). The degree and direction of morphological change in Additionally, invasive species may also alter the evolutionary invasive species with a long history of introduction pathway of native species by mechanisms such as niche are insufficiently known for a larger scale than the displacement, hybridization, introgression and predation (e.g. archipelago or island group. Here, I analyse data for 105 Mooney & Cleland 2001; Stuart 2014; van der Geer et al. island populations of Polynesian rats, Rattus exulans, 2013). The timescale and direction of evolution of invasive covering the entirety of Oceania and Wallacea to test rodents are, however, insufficiently known. Data on how whether body size differs in insular populations and, they evolve in interaction with native species are urgently if so, what biotic and abiotic features are correlated needed with the increasing pace of introductions today due to with it. All insular populations of this rat, except globalized transport: invasive rodent species are estimated to one, exhibit body sizes up to twice the size of their have already colonized more than 80% of the world’s island mainland conspecifics. Body size of insular populations groups (Atkinson 1985). is positively correlated with latitude, consistent with Here, I present data from a ubiquitous invasive species, thermoregulatory predictions based on Bergmann’s the Polynesian rat (R. exulans), which provides an excellent rule. Body size is negatively correlated with number proxy to measure and model evolutionary changes for several of co-occurring mammalian species, confirming an reasons. First, it vastly extended its geographic range through ecological hypothesis of the island rule. The largest rats human-mediated transport (Roberts 1991)(Fig. 1)andis are found in the temperate zone of New Zealand, as well currently a commensal in islands of the Lesser Sunda as on mammalian species-poor islands of Polynesia Archipelago, the Moluccas, Sulawesi, the Philippines, New and the Solomon Islands. Carnivory in the form of Guinea, New Zealand and practically all inhabited Pacific predation on nesting seabird colonies seems to promote islands (Corbet & Hill 1992; Musser & Carleton 2005), 1.4- to 1.9-fold body size increases. and has recently also been recorded in Taiwan and the Keywords: body size evolution, invasive species, islands, island southern Ryukyu Islands (Motokawa et al. 2001). Second, the rule, kiore, Rattus exulans, Polynesia introduction of this species has a large temporal range, starting c. 3500 years ago (Roberts 1991; Wilmshurst et al. 2008). Third, it is not limited to urban and agricultural areas, but also INTRODUCTION occurs in disturbed forests (e.g. Rabor 1977; Danielsen et al. Humans have been transporting vertebrates to islands 1994) and primary forests without native rodents (Heaney worldwide since prehistoric times. This has more often et al. 1989), as well as in dry deciduous forests, mangrove than not impacted native flora and fauna (Russell et al. forests and lowland coastal forests (Molur et al. 2005). It is 2017), and Darwin (1859) remarked in this context, ‘Let an adept climber and builds nests in small trees and hedges it be remembered how powerful the influence of a single (Thomson 1922), and especially the canopy of coconut palms introduced tree or mammal has shown to be.’ The successful provide nesting and feeding opportunities (Wegmann et al. introduction of such exotics has often led to the extinction 2011). Its native range is the tropics and subtropics, but its of native species (Atkinson 1989; Groombridge et al. 1992; colonization success elsewhere shows that it thrives equally Courchamp et al. 2003; Long, 2003), especially on small, well in temperate maritime climates. Lastly, rats in general isolated islands. Invasive rats (Rattus rattus, Rattus norvegicus, have the potential to show evolutionary changes within a Rattus exulans) are likely responsible for the greatest number relatively short time span due to their high reproduction rate. of extinctions on islands (Towns et al. 2006). Not only do The combination of large geographic and temporal scales they compete ecologically with native species, they also evolve thus makes the Polynesian rat an ideal species to test potential evolutionary pathways in invasive species. For most islands, there was only a single colonization event (Barnes et al. 2006). ∗Correspondence: Alexandra A.E. van der Geer email: alexandra. The colonization history can be traced using rat haplogroup [email protected] mtDNA (Matisoo-Smith & Robins 2004), archaeological and Supplementary material can be found online at https://doi.org/ genetic data and linguistic evidence of the Polynesians (Lipson 10.1017/S0376892918000085 et al. 2014). Populations in Oceania were first established some This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 27 Sep 2021 at 01:31:36, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0376892918000085 204 van der Geer A. A. E. Figure 1 Diagrammatic map showing simplified routs of human migration (after Roberts 1991; Austin 1999). The dispersal of the Polynesian rat (Rattus exulans) has been facilitated by humans since prehistoric times. Populations in Oceania were introduced about 3000–3500 years ago (Roberts 1991; Austin 1999), in Hawaii about 1200–1700 years ago (Kirch 2001) and in New Zealand about 800 years ago (Matisoo-Smith et al. 1999). Light grey (orange in online version): native and introduced range of the Polynesian rat. White: areas without Polynesian rats. 3000–3500 years ago (Roberts 1991), whereas Hawaii, New usage, opening up the possibility to evolve in a new direction Zealand and Rapa Nui (Easter Island) were reached much (Gillespie 2009). later (c. 1190–1290 CE; Wilmshurst et al. 2011). The rats’ The null hypothesis is that body size of introduced differing morphologies among the various islands were long populations of the Polynesian rat cannot be predicted noted (e.g. Motokawa et al. 2004) and are reflected in the long based on the following variables: island size (a proxy for list of junior synonyms (e.g. Mus maorium) and subspecies species and habitat diversity); latitude (a proxy for mean status such as Rattus exulans negrinus for the Negros small environmental temperatures and a weak correlate of primary field rat. productivity); number of mammalian species (a measure of My aim is to test whether the body size of insular ecological interactions); and maximum elevation (a measure populations of the Polynesian rat varies in correlation with of topographic relief, habitat diversity and the influence biotic and abiotic variables. Here, I take samples from the of anthropogenic activities, which tend to dominate lower entire introduced and native range. This vast geographic elevations). range ensures the presence of a large variety of islands with various geographic features, with and without mammalian competitors and predators. MATERIALS AND METHODS The hypothesis is that body size evolution of this introduced mammal on the various islands complies with predictions Dataset based on the island rule, a graded trend according to which Extensive collections of the Polynesian rat are available, populations of small-sized species evolve larger body sizes on representing the entire introduced range. The dataset includes islands (gigantism) (sensu Foster 1964; Van Valen 1973). The 105 populations (n = 587) of this species introduced island rule, or island syndrome, was originally formulated onto islands and six mainland populations (n = 16) for native species and populations, but appears to apply to from Southeast Asia (Vietnam, Laos, peninsular Malaysia, populations of introduced commensal rats as well (e.g. Russell Thailand, Myanmar and Sumatra) for comparison from the et al. 2011; van der Geer et al. 2018). According to an ecological following institutes: AMNH (American Museum of Natural interpretation of the trend (Lomolino et al. 2012, 2013;van History, New York), AMS (Australian Museum, Sydney), der Geer et al. 2013), the direction and degree of size change AWMM (Auckland War Memorial Museum), LRNZ depends on a combination of biotic and abiotic factors, with (Landcare Research, Lincoln), FMNH (Field Museum of an especially important role for co-occurring mammalian Natural History, Chicago), MNZ (Museum of New Zealand species. In species-rich systems, competition and predation Te Papa Tongarewa, Wellington), RMNH.MAM (Naturalis are expected to result in diversification and ecological Biodiversity Center, Leiden; formerly Rijks Museum voor displacement among resident species (native as well as long-
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