JUST, Vol. V, No. 1, 2017 Trent University

There Were Cats and Rats and Ungulates: Island Colonisation Success of Mammals

Tessa Sarah McBurney

Abstract Islands are particularly susceptible to the severe ecological consequences wrought from the dispersal of invasive species, and introduced mammals have exceeded other vertebrate groups when it comes to posing challenges for native populations. The purpose of this study was to determine what factors affect a mammalian species’ ability to invade islands by comparing how two taxonomically and physiologically unique mammalian orders, Rodentia and Artiodactyla, invade islands and resist eradication. Using data provided by the Threatened Island Biodiversity Database and the Database of Island Invasive Species Eradications, the results of multiple Wilcoxon rank-sum tests demonstrated that rodents and even-toed ungulates are equally capable of invading islands. However, rodent populations were found to be superior in surviving eradication attempts (W = 24, p − value < 0.05). More research is required to understand what makes a species a successful invader to assist in mitigating the negative impacts of invasive species. Keywords Rodents — Even-toed Ungulates — Artiodactyla — Invasive Species — Island Biogeography — Eradications Gzowski College

1. Introduction demic species, the likes of which are not found in continental areas (Jamie et al. 2007). The physical distance from the At a time when biological invasions have reached their high- mainland to the island, across oceanic environments, is what est rate in history, it is crucial to consider how alien species limits the type of species that are able to colonise an island impact native species populations (Reaser et al. 2007). Cur- (Jamie et al. 2007). This means few large mammals are native rently, biological invasions are the second leading cause of to isolated islands (Jamie et al. 2007). However, mammals of biodiversity loss, and are a major factor in the extinctions of varying size have been both intentionally and unintentionally many species (Courchamp et al. 2003). Islands in particular introduced outside of their native range by human dispersal have been experiencing severe ecological consequences from and trade (Clout and Russell 2008). Mammals were some of the dispersal of invasive species (Reaser et al. 2007), and the earliest animals to be introduced to islands by humans for introduced mammals have posed more challenges than any the purpose of livestock or companionship, or accidentally other vertebrate group (Courchamp et al. 2003). For an alien through commensal relationships (a relationship that was ben- or introduced species to be considered invasive it must have eficial to the animals and not adverse for the humans) (Clout established a self-sustaining population and spread rapidly, and Russell 2008; Nogueira et al. 2009; Spear and Chown or had an impact on native organisms (Ricciardi et al. 2013). 2009). The difference between an alien and an introduced species, which are both not native to the area in question, is that the 1.2 Rodentia and Artiodactyla General Traits latter has dispersed via human actions. Variation of body masses between different taxonomic groups may be fundamental to explaining physiological, ecological, 1.1 Island Biogeography and phylogenetic constraints (Smith et al. 2003). Order Ar- As stated in the MacArthur-Wilson Theory of Island Bio- tiodactyla is a taxon that encompasses even-toed ungulates, geography, immigration, speciation, and extinction are af- or hooved animals with an even number of toes, such as fected by two major environmental factors: isolation and deer, boar, cows, and goats. Order Rodentia is the taxonomic area (MacArthur and Wilson 1967; Whittaker et al. 2008). group for rodents and includes: mice, rats, lemmings, shrews, MacArthur and Wilson (1967) predicted that the rate of immi- squirrels, and agouti, among other rodents species. Based on a gration will decline as isolation, or the physical distance from dataset of taxonomic body mass created by Smith et al. (2003), the mainland to the island, increases, and the rate of extinction members of order Artiodactyla generally have a considerably will decline as the area of the island increases (Whittaker et larger body mass than those of order Rodentia. As smaller al. 2008). The relative geographic isolation of islands has organisms, rodents tend to have high reproductive output but allowed for the evolution of a high number of novel and en- die young (Sibly and Brown 2007). Larger mammals, such There Were Cats and Rats and Ungulates: Island Colonisation Success of Mammals — 2/5 as even-toed ungulates, have slower metabolic production per the natural log-transformation did not help the data to meet unit body mass and so produce offspring at a lower rate (Sibly the assumptions, then a non-parametric Wilcoxon rank-sum and Brown 2007). In this regard, body mass is an essential test was used in place of the t-test. factor in the invasive capabilities of mammals. Successful The second objective was evaluated by comparing the establishment of a new colony relies on the number of new failure rates and success rates for human-mediated island recruits added to the population, which is in turn partially eradications of invasive rodents and even-toed ungulates. The dependent on the reproductive output of the species. number of successful and failed eradications of island invaders Considering the current impact of invasive species, espe- were collected from the Database of Island Invasive Species cially introduced mammals, on native species populations, an Eradications (Invasive Species Specialist Group 2016; Ap- important question to ask is: What factors affect a mammalian pendix: Table 3; Table 4). These were each divided by the species’ success in invading islands? Being able to answer total number of eradication attempts that took place for each this question could lead to the discovery of more effective species in both orders to ensure that success and failure rates control measures for managing island colonisations of inva- were correctly measured. Although successes and failures can sive mammals. This study sought to answer this question by typically be compared without using rates, because they sum comparing how effectively the members of two taxonomically to the total number of attempts, this is not the case in this study. and physiologically disparate mammalian orders, Rodentia The database included more eradication attempt statuses than and Artiodactyla, colonise islands. To assess the success of in- those coded as successes and failures because many eradica- vasive colonisation, effectiveness was measured as the number tion attempts were still ongoing or the results were unknown. of islands colonised by members of each order and the number While the database did not provide a definition for success or of human-mediated eradications of alien island colonies of failure, this study assumes that a successful eradication is one both orders. The objectives of this study were to determine if where the island has hitherto remained free of the eradicated the orders were equally: organism after the eradication attempt, in accordance with Courchamp et al. (2003). A failed eradication is one where 1. Successful at colonising islands. the eradication attempt did not work or where the island was 2. Able to withstand human-mediated eradications of alien recolonised by the invasive species. Eradication attempts that island colonies. were not listed as successes or failures were not counted in this study and only species that have island populations where The hypothesis for the first objective was that the two eradications have been attempted were included in the data mammalian orders were not equally successful at colonising set. The data were tested against the same assumptions as islands. It was predicted that members of order Rodentia the first objective, and then depending on the results, either would be more effective at colonising islands than members independent two sample t-tests or Wilcoxon rank-sum tests of order Artiodactyla, due to small body size and generalist were used to compare both the failure and success rates of tendencies in diet and habitat. The hypothesis for the second island eradications between the two mammalian orders. objective was that the orders were not equally able to with- All data were analysed using RStudio (Version 0.00.903; stand eradications of alien island colonies. It was predicted Allaire 2016). Island size data were examined in order to that invasive colonies of order Artiodactyla species would be rule out island size as a confounding variable before either less able to withstand eradication attempts than alien colonies the island or eradication data were analysed (Appendix Table of order Rodentia species, due to a generally larger body size 5; Table 6). For each rodent and even-toed ungulate species and more specialist dietary tendencies. If both predictions that invaded an island, the median island area was calculated were supported, members of order Rodentia would be consid- using the area of the largest and smallest islands invaded by ered more effective islands invaders. each particular species. Then these data were explored to see if they met the assumptions of homogeneity of variance 2. Materials and Methods and normality. If the data did not meet these assumptions they were natural log-transformed prior to statistical analysis. The number of islands that have been colonised by rodents and Based on these results, an independent two sample t-test or a even-toed ungulates were recorded from the Threatened Is- Wilcoxon rank-sum test was used to verify that there was no land Biodiversity Database (Invasive Species Specialist Group difference between the areas of islands colonised by Rodentia 2016; Appendix: Table 1; Table 2). Only species in each order species and those colonised by Artiodactyla species. An a pri- that were found to invasively colonise islands were included ori significance level of 0.05 was used for all of the statistical in the analysis. Before addressing the first objective, the data analyses. were explored to ensure the assumptions of normality and ho- mogeneity of variance were met. If one of these assumptions was not met, then the data were natural log-transformed before 3. Results running a statistical test. An independent two sample t-test The prediction that members of order Rodentia would be was used to determine if there was a difference in the number more effective at colonising islands than members of order of islands colonised by rodents and even-toed ungulates. If Artiodactyla was not supported by the results of the Wilcoxon There Were Cats and Rats and Ungulates: Island Colonisation Success of Mammals — 3/5

Figure 1. A boxplot of the average size of islands invasively colonised Figure 2. A boxplot of the number of islands invasively colonised by by orders Artiodactyla (red) and Rodentia (blue). The median average orders Artiodactyla (red) and Rodentia (blue). The median number of island size, represented by the black line, is not significantly different colonised islands, represented by the black line, is not significantly between the two orders. Whereas the Artiodactyla data is fairly different between the two orders. The interquartile range is small for symmetrical, the Rodentia data is skewed right with a large both orders, although there are outliers present in both the interquartile range. There are also outliers present in the Artiodactyla Artiodactyla and Rodentia data. data. rank-sum test. The prediction that invasive colonies of order Artiodactyla species would be less able to withstand eradica- tion attempts than order Rodentia species was not statistically supported by the Wilcoxon rank-sum test for success rate, but was statistically supported for failure rate. First, the effect of island size as a covariate was tested. The p-value was found to be greater than the a priori set 0.05 significance level, so the null hypothesis that there was no difference between the average sized islands colonised by the two orders was accepted (n=74; W=647.5, p-value=0.7284; Figure 3. A boxplot of the success rate of eradications on islands Appendix: Fig.4). invasively colonised by orders Artiodactyla (red) and Rodentia (blue). After ruling out island area as a confounding variable, The median number of colonised islands, represented by the black the first objective, to determine if the orders are equally suc- line, is not significantly different between the two orders. The interquartile range is large for order Artiodactyla, and there is an cessful at colonising islands, was addressed. The F test to outlier present in the Rodentia data. compare two variances found the variances to be unequal and the Shapiro-Wilk normality test also indicated the data were non-normal (n=74; Artiodactyla: W = 0.4188, p-value = W=52, p-value=0.6805; Fig. 2). 2.113x10−11; Rodentia: W = 0.4544, p-value = 4.096x10−10) The same statistical methods were used to test the differ- . The data were natural log-transformed and the natural log- ence between failed island eradications of invasive even-toed transformed data were found to have equal variances. How- ungulate and rodent species. The variances were found to be ever, the data were still not normal, so a Wilcoxon rank-sum unequal and the data were not normally distributed. After nat- test was used in place of a t-test with the non-normal natural ural log-transforming the data, the variances were improved, log-transformed data. The results of the Wilcoxon rank-sum but still not equal, and neither the order Rodentia nor the order test indicated the null hypothesis should be accepted (W=707, Artiodactyla data were normal. A Wilcoxon rank-sum test was p-value=0.7684). Therefore, there was no evidence that there conducted using the natural log-transformed non-normal data. was a significant difference between the number of islands Rodents had a higher mean eradication failure rate (0.2244) colonised by rodents and even-toed ungulates (Fig. 1). than even-toed ungulates (0.0108), a difference which is sta- For successful island eradications of invasive even-toed tistically significant (n=22; W=24, p-value=0.0084; Fig. 3). ungulates and rodents, the data were found to have equal variances, however, the order Artiodactyla data were found to be non-normal. As a result, the data were natural log- 4. Discussion transformed, which made the data from both orders non- The hypothesis for the first objective, that members of or- normal. Thus, a Wilcoxon rank-sum test was used as a non- ders Rodentia and Artiodactyla were not equally successful at parametric test with the original non-transformed data. Based colonising islands, was not supported by the statistical analy- on the results of the Wilcoxon rank-sum test there was no sis. The hypothesis for the second objective, that the orders difference in the success rate of island eradications between were not equally able to withstand eradications of alien island members of order Rodentia and order Artiodactyla (n=22; colonies, was supported by the analysis of the eradication There Were Cats and Rats and Ungulates: Island Colonisation Success of Mammals — 4/5

is possible that particular rodent species are more effective at invasively colonising islands than even-toed ungulate species. The results of the second objective, which established that the two orders were not equally able to withstand eradica- tion of alien island colonies, are supported by studies which demonstrate that rodents are among the most widespread island-colonised invasive species (Shiels and Drake 2011). Additionally, invasive rodents are challenging to manage ef- fectively (Shiels and Drake 2011), which is partly attributable to the risk of reinvasion posed by rodent species (Clout and Russell 2007). While there have been many successful eradi- Figure 4. A boxplot of the failure rate of eradications on islands cations of rodents from islands, there have also been several invasively colonised by orders Artiodactyla (red) and Rodentia (blue). The median number of colonised islands, represented by the black reinvasions that have occurred up to ten years after the eradi- line, is significantly different between the two orders, with order cation, particularly with rats (Clout and Russell 2007). This is Rodentia having a higher rate of failed eradications. The interquartile thought to be due to the high dispersal ability of order Roden- range is small for order Artiodactyla, and there are outliers present in the data for both orders. tia species (Clout and Russell 2007). This supports the results of both the eradication success and failure rate analyses, as dispersal ability would not affect how susceptible a species failure rate data, but not the eradication success rate data. Ro- is to being eradicated, which would account for even-toed dents were found to have a higher average failure rate than ungulates and rodents having the same average success rate even-toed ungulates, which suggests that species from order of eradications. However, it could impact the average erad- Rodentia are at least somewhat better able to withstand island ication failure rate as dispersal ability would allow rodents eradications than order Artiodactyla species. Although there to recolonise islands that have already undergone eradication are no differences between the two orders in terms of island attempts, which may account for why rodents were found to colonisation ability and the island eradication success rate, have a higher average number of failed eradication attempts this suggests that overall order Rodentia is more successful at than even-toed ungulates. The recolonisation of islands by invasive colonisation of islands than order Artiodactyla. rodents has been observed several times, including the re- Even though rodents were found to be better overall island colonisation of Italian islands by Black rats post eradication invaders than even-toed ungulates, the results for the first ob- attempts (Capizzi et al. 2010). In this way, members of order jective were surprising based on the existing literature. Rats, Rodentia may be better able to withstand human mediated including Norway rats (Rattus norvegicus), Black rats (Rattus eradication attempts, and thus, be more successful overall at rattus), and Polynesian rats (Rattus exulans), are cited to be invasively colonising islands. among the most successful invasive mammal species having Some possible limitations of this study include the avail- invaded 80% of islands in the world (Caut et al. 2008). Ad- ability of data concerning the details of the invaded islands. ditionally, House mice (Mus musculus) are considered to be Due to the importance of island size and isolation when it one of the most far-reaching invasive mammals on the planet comes to immigration and establishing populations (Whit- (Angel et al. 2009). However, a list of the most successful taker et al. 2008), it was determined that these factors should introduced mammals, measured by the number of introduc- both be ruled out as potential cofounding variables when at- tions and the risk posed to native populations, includes: three tempting to isolate the island invasion abilities of rodents and rat species, one mouse species, rabbits, cats, goats, pigs, and even-toed ungulates. Island size was eliminated as a con- cattle (Courchamp et al. 2003). This cites both rodents and founding variable early in the study when no difference was even-toed ungulates as top mammalian invaders, and is sup- found in the median island areas colonised by species in order ported by the results of the first statistical test of this study Rodentia and Artiodactyla. However, a better method may which indicates that the orders were equally successful at be to determine whether there is a difference between the colonising islands. This is a point of interest because the most average island size colonised by each species in each order, successful introduced mammals include various species from and although this was not considered in the current study, it several different orders which suggests that at least initial is recommended that it be accounted for in future research. colonising ability may be species dependent rather than a trait Unlike island size, the potential effect of isolation could not at the taxonomic level of order. This is further supported by a be ruled out as a confounding variable because data on the rel- study conducted by Clout and Russell (2008) where only 1.8% ative isolation of the islands were not included in the database of rodent species were classified as successful invaders, but (Invasive Species Specialist Group 2016). While island isola- 13% of the genus Rattus were included in this category. This tion could be a potential confounding variable in this study, it could explain the far outliers found in the order Rodentia data can be argued that it does not necessarily apply to all invasive in this study. While order Rodentia in its entirety may not be species. This is because many invasive species are introduced more effective at invading islands than order Artiodactyla, it to islands through human-mediated dispersal, which can oc- There Were Cats and Rats and Ungulates: Island Colonisation Success of Mammals — 5/5 cur over large distances. 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Appendix etary shift of an invasive predator: rats, seabirds and sea Raw data tables can be found at trentu.ca/just in additional turtles. Journal of Applied Ecology 45:428-437. materials for this article