Bodey, T.W.; S. Bearhop, and R. A. McDonald. InvasionsIsland and stable invasives: isotope analysis eradication – informing ecology and and management management
Invasions and stable isotope analysis – informing ecology and management
T. W. Bodey1, S. Bearhop1, and R. A. McDonald2 1Centre for Ecology and Conservation, University of Exeter Cornwall Campus, Penryn, Cornwall, TR10 9EZ, UK.
INTRODUCTION Stable isotope analysis (SIA) has increasingly been used across different localities. Such methods require stable to answer ecological questions about organisms, including isotopic ratios from the consumer’s tissue (hair, feathers, those relating to diet and migration patterns (Dalerum and whiskers, claw, blood, liver, bone etc), and also the stable Angerbjorn 2005; West et al. 2006; Crawford et al. 2008; isotope ratios of potential prey, local geology or rainfall Inger and Bearhop 2008). This focus has in turn led to an patterns (e.g., West et al. 2006). Mixing models (Phillips increase in the number of chemical elements used and the and Gregg 2003) are often applied to interpret these results variety of ecological questions addressed (Fry 2006). Finer and, more recently, Bayesian solutions to these analyses resolution to SIA has been aided by recent advances in have been developed (Parnell et al. 2010). statistical modelling (Phillips and Eldridge 2006; Parnell et al. 2010; Jackson et al. 2011). Stable isotope analyses Advantages of using SIA have only recently been applied to invasion biology. This short review examines how SIA can be an additional tool Many species are difficult or expensive to study in the to assist with the management of invasive species. We first field because of their behaviour or location. For example, discuss the ways SIA can be applied, then show how it can the nocturnal and neophobic behaviour of rats (Rattus spp.), assist with studies of invasion biology as well as refining coupled with difficulties with accessing invaded islands can approaches to eradication campaigns. prevent detailed year-round study. Furthermore, the use of conventional techniques such as radio telemetry or scat Basics of stable isotope analysis analysis are a time consuming, labour intensive and costly method of measuring the ecological impacts of invasive Many chemical elements can have more than one species. By comparison, SIA is relatively cheap because isotopic form of differing molecular mass. Examination of time and effort required in the field can be reduced. This the stable isotopic ratios of the various forms of oxygen, is because behavioural information can be gathered over hydrogen, sulphur and strontium have all helped to multiple time scales through the analysis of multiple tissue provide unique insights into the ecology and biology of types from an individual after a single capture event. Since plants and animals (e.g., Crawford et al. 2008), but the different tissue types are replaced at different rates, the two most commonly used are stable isotopes of carbon proteins within them will be synthesised at different times. (C) and nitrogen (N). The former (the ratio of 13C to 12C, 13 The proteins then reflect aspects of the animal’s ecology at expressed as δ C). can be used to discriminate among these different points. For example, stable isotope signatures different sources of primary production. The derivation of from liver cells reflect the animal’s diet over previous days, such ratios can potentially identify an animal’s foraging those of muscle reflect the diet over preceding weeks to location. For example, there is a difference between months, and those of hair for longer still (Kurle 2009). marine and terrestrial sources, where marine signatures are 13 The length of time represented by isotopes in tissues also enriched with C compared to terrestrial ones (Fry 2006). varies with the metabolic activity of the animal concerned. Stable nitrogen isotope ratios, (15N to 14N, expressed as 15 Replacement processes are more rapid in species with δ N) can also vary spatially, but are much more useful as a higher metabolic rates, so that, for example, mice have means for determining the trophic level at which an animal faster replacement rates than rats (MacAvoy et al. 2006). is feeding. Organisms become progressively enriched in 15N at higher trophic levels due to preferential retention Single tissues such as claws, whiskers and hair can of the heavier isotope during tissue synthesis (Fry 2006). also be used to derive a time series of past behaviour. The As a result there is a stepwise style enrichment between protein in these tissues is metabolically inert after it has consumer and prey, meaning that animals feeding at higher been synthesised, so provides a continual record which can trophic levels within a food web have higher δ15N in their be ‘read’ along its length, going back in time the nearer tissues than those feeding at lower trophic levels.. a sample is to the distal end of the tissue (Bearhop et al. 2003; Cherel et al. 2009). In sum, SIA of multiple tissues of With the increasing use of SIA, methods have been an individual animal can rapidly provide a detailed record developed to quantify the importance of multiple food of diet and potential foraging locations over different time sources or determine the probability of animals moving scales.
Pages 148-151 In: Veitch, C. R.; Clout, M. N. and Towns, D. R. (eds.). 2011. Island invasives: eradication and management. 148IUCN, Gland, Switzerland. Bodey et al.: Invasions and stable isotope analysis
Demonstrating the impacts of invasive invasion as they did not consume the hybrid plant. Thus species while the invasive plant structurally altered the ecosystem, its resources were not efficiently broken down, resulting in The accumulated knowledge of a species’ impacts bottom up alteration of the food web (Brusati and Grosholz elsewhere remains the best predictor of their likely effects 2009). at new locations (Simberloff 2003). However, a business case for the eradication or control of invasive species will Energetics modelling combined with SIA was used often still require site-specific information. to demonstrate dramatic changes in a food web on the Channel Islands, California following the introduction Direct predatory impacts of feral pigs (Sus scrofa) (Roemer et al. 2002). The pigs Stable isotope analyses can be used to examine the diet provided an abundant food resource for golden eagles of invasive predators. While this provides an integrated (Aquila chrysaetos), which increased in number. Increased picture of an animal’s diet, SIA cannot be used to predation by eagles reduced the population of island fox differentiate between predated and scavenged food items. (Urocyon littoralis). This in turn allowed island skunk For example, Stapp (2002) demonstrated that ship rats (Spilogale gracilis amphiala) populations to increase (Rattus rattus) in the Shiant Islands, UK consumed seabird following reduced competition from foxes. The SIA also flesh, but could not demonstrate predatory behaviour from demonstrated the low level of marine input from seabirds this result. Although proof of predatory behaviour may not to the eagles’ diets and their concentration, in particular, on necessarily be derived from SIA, it has advantages over introduced terrestrial prey. conventional methods such as stomach content or scat Isotope studies are particularly useful for determining analyses, which may over-represent indigestible material the effects of introduced fish, possibly because other or under-represent items that leave little visual trace. The techniques used for terrestrial vertebrates are often not most informative approach can be to combine SIA with applicable to aquatic species. SIA studies revealed how other methods to strengthen the conclusions that can be introduced salmonid species such as Oncorhynchus drawn (Hobson et al. 1999). For example, Harper (2007) spp., Salmo spp., and Salvelinus spp. altered food webs used experimental removal of ship rats and a predatory by reducing prey fish abundance. This led to increased bird, weka (Gallirallus australis), alongside isotopic and consumption of zooplankton by the invasive fish, and so to conventional diet analysis to examine the importance of a reduction in their own trophic level (e.g., Vander Zanden sooty shearwater (Puffinus griseus) in each species’ diet. et al. 1999). Introduced trout can also affect terrestrial Caut et al. (2008) used a combination of SIA, stomach food webs by consuming insects that would otherwise contents and direct observations to reveal the impact constitute important prey resources for terrestrial species. of ship rats on breeding seabirds on Surprise Island, For example, trout introduced into previously fish-free New Caledonia. They also showed how, in the absence lakes competed with the critically endangered mountain of seabirds, rats switched prey to green turtle (Chelonia yellow-legged frog (Rana muscosa) for emergent insect mydas) hatchlings. Hobson et al. (1999) were similarly prey (Finlay and Vredenburg 2007). Adult frogs feed on able to demonstrate the seasonal importance of breeding lake shores, and their consumption of emergent insects seabirds in the diet of brown rats R. norvegicus on Langara plays a key role in transferring energy between aquatic Island, British Columbia, and also the extent to which and terrestrial environments. Differences in isotopic different individuals relied on this resource. Such plasticity values between benthic and pelagic prey revealed how fish in the consumption of seabirds by individual brown rats altered aquatic food webs by consuming large numbers of was also found when they fed on least auklets (Aethia benthic insects, largely restricting the supply of these to pusilla) at Kiska Island, Alaska (Major et al. 2007). terrestrial environments. The importance and frequency of energy transfer between aquatic and terrestrial systems is Impacts on trophic structure increasingly recognised (e.g., Knight et al. 2005), and SIA The way that invasive species disrupt food webs and is an ideal tool for examining such linkages. transform community structure has also been revealed through the use of SIA (e.g., Vander Zanden et al. 1999; Differences in niche width Croll et al. 2005). Changes in trophic level can be seen 15 Comparisons of niche width at individual and population through examination of changes in δ N within a species levels can be explored with stable isotopes (e.g., Bearhop over time, as was demonstrated for the invasive carnivorous et al. 2006) and then used to predict the potential spread Argentine ant (Linepithema humile) in California. Initially, and range of an invader. Invasive species often show high invading ants occupied a similar trophic level to those in plasticity of niche width in terms of habitat use, feeding their native habitats, where they fed on other ants. However, ecology or behaviour (Hayes and Barry 2007). For example, once established, the ants shifted to a lower trophic position a recent study in southern Sweden demonstrated that as they consumed more plant material following severe invasive signal crayfish Pacifastacus( leniusculus) have a reductions in native ant prey populations (Tillberg et al. potential niche width almost twice the size of the native 2007). At a whole-island scale, Croll et al. (2005) used European crayfish (Astacus astacus). However, signal SIA to measure the importance of marine nitrogen input crayfish often used a similarly sized niche to European from seabirds to Aleutian Island plant communities. They crayfish within a given habitat (Olssonet al. 2009). Isotopic found that on islands where invasive arctic foxes (Alopex analyses also revealed greater plasticity in invasive plants. lagopus) had destroyed the seabird populations, plant The invasive tree Schinus terebinthifolius in Hawaii had communities were transformed from grasslands to shrub/ δ13C values indicating a much greater capacity to adjust its forb communities because of reduced soil fertility. physiology to variation in soil water availability, and more Invasive plants can also modify food webs. Stable efficient water conservation, than the native trees to which isotopes (δ15N) demonstrated that invertebrates that it was compared (Stratton and Goldstein 2001). persisted within areas invaded by the Spartina alterniflora Differences between multiple invasive species have x foliosa hybrid in San Francisco Bay, USA were also been examined with SIA, revealing how distinctions consuming this invader (Levin et al. 2006). However, other in habitat and diet utilisation allow multiple invasions of invertebrates such as amphipods, which are an important an ecosystem. Rudnick and Resh (2005) demonstrated prey item for many predators, were less tolerant to habitat that while Chinese mitten crabs (Eriocheir sinensis) and
149 Island invasives: eradication and management red swamp crayfish Procambarus ( clarkii) primarily samples were used to generate a simple dietary time series. consumed plant material, crabs principally fed on aquatic This revealed the continual importance of marine food algae, whereas crayfish consumed terrestrially-derived sources to the population as a whole while the eradication material. Likewise, Harper (2006) demonstrated how three progressed. Intra-sexual and intra-island differences were invasive species of rats (ship rat, Pacific rats (R. exulans) also found, and this again demonstrated that combining and brown rat) on Pearl Island, New Zealand varied in their SIA with knowledge of prey distributions and gut analysis food resources and in their competitive ability to use them, was crucial. For example, the presence at one locality of allowing all three species to coexist on this small island. an additional terrestrial prey item, the introduced field vole (Microtus agrestis), is likely to have contributed to Assessing priorities different behavioural patterns. Lastly, SIA of diets can aid the prioritisation of The use of SIA to inform eradication campaigns could eradications. Once Roemer et al. (2002) demonstrated the greatly benefit invasive species management by revealing threat that golden eagles posed to Channel Island foxes, focal areas of foraging, habitats or areas in which animals eagles were translocated elsewhere and the best method may concentrate their time, and plasticity of responses for pig removal was implemented to avoid endangering to different trophic webs. The technique can help to the remaining foxes (Caut et al. 2006). In contrast, refine methodologies and protocols, highlight areas for a combination of SIA, gut analyses and trapping led trap placement and assist with focussing of resources, Quillfeldt et al. (2008) to conclude that a large breeding potentially creating ecological traps for the target species. population of thin-billed prions (Pachyptila belcheri) on New Island, Falkland Islands, was not significantly impacted by invasive mice, ship rats and feral cats. Thus Caveats and conclusions other islands within the archipelago could be prioritised for Stable isotope analyses have transformed our eradication programmes ahead of New Island. understanding of numerous ecological questions about native species. There is a natural progression from these to Informing invasive species management its use for quantifying and resolving the effects of invasive In addition to determining the effects of invaders, SIA species, and then to inform eradication campaigns. can also help with formulating a response to invasions. By Unsurprisingly though, the use of SIA comes with some understanding the food used and locations from which it caveats. For example, there may be difficulties with has been obtained, behavioural patterns can be identified interpreting the origins of food from multiple sources, that enhance the chances of successfully eliminating a variation in assimilation rates of isotopes into tissues both population. An example of this approach was proved for between individuals and species, and resolving the output of invasive American mink (Neovison vison) in the Outer complicated statistical models (Crawford et al. 2008; Inger Hebrides, UK (Bodey et al. 2010). Stable isotopes can et al. 2008; Kurle 2009). Furthermore, additional work is also help shape eradication protocols alongside a suite required if we are to advance our understanding of turnover of standard techniques. For example, the likely outcomes rates and growth times of specific animal tissues. On the of species eradication such as the disruption of trophic other hand, while such information may be interesting, it interactions, or the ecological release of other species, may be beyond the information needed for an eradication can be assessed more thoroughly prior to any eradication programme. Thus, the few complexities with interpretation attempt as was carried out on a whole island basis prior are not sufficient to prevent the incorporation of stable to ship rat removal from Surprise Island, New Caledonia isotopes into management programmes. Given the value (Caut et al. 2009). of adaptive management for the control or eradication of invasive species, SIA provides an additional tool with The logistics of eradicating common invasive mammals considerable potential to inform management options. from small islands are now well understood. Successful eradications have continued to increase in size and When combined with other methods, SIA can maximise complexity (Towns and Broome 2003: Veitch et al. 2011). the information obtained from culled individuals, enable However, increases in scale are accompanied by increased rapid data accumulation, and thus inform areas of risks, including a higher risk of failure from unexpected uncertainty as quickly as possible. Furthermore, it can challenges. While appropriate prior planning is of course aid preliminary studies on the feasibility of eradications, essential, an adaptive management approach (Park 2004), inform operations as they progress, and inform models of which seeks improvements as progress continues, is potential outcomes. Additionally, collection of samples often the most effective method for tackling these risks. such as fur, feathers and blood for SIA can be through The extent to which detailed knowledge about a species’ non-lethal means, enabling its use to measure behavioural ecology is required before an eradication campaign begins and dietary changes in endangered species pre- and is debatable, particularly as the time taken to fully explore post-eradication. Stable isotopes may also shed light on such questions may distract effort away from an efficient subsequent restoration attempts. For example, Gratton and eradication campaign (Simberloff 2003). Denno (2006) used changes in stable isotope values to show how disrupted trophic interactions were reconstituted Bodey et al. (2010) used SIA of diets of captured after removal of the invasive Phragmites australis and American mink early in an eradication attempt in order restoration of Spartina alterniflora in a coastal saltmarsh. to reveal temporal patterns in mink behaviour that might Stable isotopes can efficiently provide information at both assist the campaign. This approach identified that precise the population and individual level from relatively small knowledge about what prey mink were consuming or when samples on species that may otherwise be difficult to study. it was consumed was not necessary. Instead, the most They can be used to examine behavioural and ecological useful information for the campaign was whether prey changes, and to describe the dietary and habitat plasticity of was marine or terrestrial in origin, and the relative time invasive species. They thus have great potential to inform of consumption, coupled with background information on management options, and should be seen as a powerful prey distributions. Individual variation in whisker and liver addition to the eradication toolkit.
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Acknowledgements Knight, T. M.; McCoy, M. W.; Chase, J. M.; McCoy, K. A. and Holt, R. D. 2005. Trophic cascades across ecosystems. Nature 437: 880-883. We thank Orea Anderson, Franck Courchamp, Rosalind Kurle, C. M. 2009. Interpreting temporal variation in omnivore foraging Kennerley, Dave Towns and an anonymous reviewer for ecology via stable isotope modelling. Functional Ecology 23: 733-744. useful comments on previous drafts. Levin, L. A.; Neira, C. and Grosholz, E. D. 2006. Invasive cordgrass modifies wetland trophic function.Ecology 87: 419-432. References MacAvoy, S.; Arneson, L. and Bassett, E. 2006. Correlation of metabolism Bearhop, S.; Furness, R.W.; Hilton, G.M.; Votier, S.C. and Waldron, S. with tissue carbon and nitrogen turnover rate in small mammals. 2003. A forensic approach to understanding diet and habitat use from Oecologia 150: 190-201. stable isotope analysis of (avian) claw material. Functional Ecology 17: 270-275. Major, H. L.; Jones, I. L.; Charette, M. R. and Diamond, A. W. 2007. Variations in the diet of introduced Norway rats (Rattus norvegicus) Bearhop, S.; Phillips, R. A.; McGill, R.; Cherel, Y.; Dawson, D. A. and inferred using stable isotope analysis. Journal of Zoology 271: 463– Croxall, J. P. 2006. Stable isotopes indicate sex-specific and long-term 468. individual foraging specialisation in diving seabirds. Marine Ecology Progress Series 311: 157–164. Olsson, K.; Stenroth, P.; Nystrom, P. and Granel, W. 2009. Invasions and niche width: does niche width of an introduced crayfish differ from a Bodey T. W.; Bearhop S.; Roy S. S.; Newton J. and McDonald R. A. native crayfish?Freshwater Biology 54: 1731-1740. 2010. Behavioural responses of invasive mink Neovison vison to an eradication campaign, revealed by stable isotope analysis Journal of Park, K. 2004. Assessment and management of invasive alien predators. Applied Ecology 47: 114-120. Ecology and Society 9: 12. Brusati, E. D. and Grosholz, E. D. 2009. Does invasion of hybrid cordgrass Parnell, A.; Inger, R.; Bearhop, S. and Jackson, A.L. 2010. Source change estuarine food webs? Biological Invasions 11: 917-926. partitioning using stable isotopes: coping with too much variation. PLoS ONE 5(3): e9672. Caut, S.; Roemer, G. W.; Donlan, C. J. and Courchamp, F. 2006. Coupling Stable Isotopes with Bioenergetics to Estimate Interspecific Interactions. Phillips, D. L. and Eldridge, P. M. 2006. Estimating the timing of diet Ecological Applications 16: 1893-1900. shifts using stable isotopes. Oecologia 147: 195-203. Caut, S.; Angulo, E. and Courchamp, F. 2008. Dietary shift of an invasive Phillips, D. L. and Gregg, J. W. 2003. Source partitioning using stable predator: rats, seabirds and sea turtles. Journal of Applied Ecology 45: isotopes: coping with too many sources. Oecologia 136: 261–269. 428-437. Quillfeldt P.; Schenk I.; McGill R. A. R.; Strange I. J.; Masello J. F.; Caut, S.; Angulo, E. and Courchamp, F. 2009. Avoiding surprise effects Gladbach A.; Roesch V. and Furness R. W. 2008. Introduced mammals on Surprise Island: alien species control in a multi-trophic level coexist with seabirds at New Island, Falkland Islands: abundance, perspective. Biological Invasions 11: 1689-1703. habitat preferences, and stable isotope analysis of diet. Polar Biology 31: 333-349. Cherel, Y.; Kernaleguen, L.; Richard, P. and Guinet, C. 2009. Whisker isotopic signature depicts migration patterns and multi-year intra- and Roemer, G. W.; Donlan, C. J. and Courchamp, F. 2002. Golden eagles, inter-individual foraging strategies in fur seals. Biology Letters 5: 830- feral pigs, and insular carnivores: how exotic species turn native 832. predators into prey. Proceedings of the National Academy of Sciences of the USA 99: 791-796. Crawford, K.; McDonald, R. A. and Bearhop, S. 2008. Applications of stable isotope techniques to the ecology of mammals. Mammal Review Rudnick, D. and Resh, V. 2005. Stable isotopes, mesocosms and gut 38: 87-107. content analysis demonstrate trophic differences in two invasive decapod crustacean. Freshwater Biology 50: 1323-1336. Croll, D. A.; Maron, J. L.; Estes, J. A.; Danner, E. M. and Byrd, G. V. 2005. Introduced predators transform subarctic islands from grassland Simberloff, D. 2003. How much information on population biology is to tundra. Science 307: 1959-1961. needed to manage introduced species? Conservation Biology 17: 83- 92. Dalerum, F. and Angerbjorn, A. 2005. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia Stapp, P. 2002. Stable isotopes reveal evidence of predation by ship rats 144: 647-658. on seabirds on the Shiant Islands, Scotland. Journal of Applied Ecology 39: 831-840. Finlay, J. C. and Vredenburg, V. T. 2007. Introduced trout sever trophic connections in watersheds: consequences for a declining amphibian. Stratton, L. C. and Goldstein, G. 2001. Carbon uptake, growth and Ecology 88: 2187-2198. resources-use efficiency in one invasive and six native Hawaiian dry forest tree species. Tree Physiology 21: 1327-1334. Fry, B. 2006. Stable Isotope Ecology. New York, Springer Science + Business Media. Tillberg C. V.; Holway D. A.; LeBrun E.g., and Suarez A. V. 2007. Trophic ecology of invasive Argentine ants in their native and introduced ranges. Gratton, C. and Denno, R. F. 2006. Arthropod food web restoration Proceedings of the National Academy of Sciences of the USA 104: following removal of an invasive wetland plant. Ecological Applications 20856-20861. 16: 622-631. Towns, D. R. and Broome, K. G. 2003. From small Maria to massive Harper, G. 2006. Habitat use by three rat species (Rattus spp.) on an island Campbell: forty years of rat eradications from New Zealand islands. without other mammalian predators. New Zealand Journal of Ecology New Zealand Journal of Zoology 30: 377-398. 30: 321-333. Vander Zanden M. J.; Casselman J. M. and Rasmussen J. B. 1999. Stable Harper, G. 2007. Detecting predation of a burrow-nesting seabird by isotope evidence for the food web consequences of species invasions in two introduced predators, using stable isotopes, dietary analysis and lakes. Nature 401: 464-467. experimental removals. Wildlife Research 34: 443-453. Veitch, C. R.; Clout, M. N. and Towns, D. R. (eds.). 2011. Island invasives: Hayes, K. R. and Barry, S. C. 2007. Are there any consistent predictors of eradication and management. IUCN, Gland, Switzerland. invasion success? Biological Invasions 10: 483-506. West, J. B.; Bowen, G. J.; Cerling, T. E. and Ehleringer, J. R. 2006. Stable Hobson, K. A.; Drever, M. C. and Kaiser, G. W. 1999. Norway rats as isotopes as one of nature’s ecological recorders. Trends in Ecology and predators of burrow-nesting seabirds: insights from stable isotope Evolution 21: 408-414. analyses. Journal of Wildlife Management 63: 14-25. Inger, R. and Bearhop, S. 2008. Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. Jackson, A. L.; Inger, R.; Parnell, A. C. and Bearhop, S. 2011. Comparing isotopic niche widths among and within communities: SIBER - Stabe Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595- 602.
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