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      Foliar Nutritional Quality Explains Patchy Browsing Damage Caused by an Invasive Mammal

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          Abstract

          Introduced herbivores frequently inflict significant, yet patchy damage on native ecosystems through selective browsing. However, there are few instances where the underlying cause of this patchy damage has been revealed. We aimed to determine if the nutritional quality of foliage could predict the browsing preferences of an invasive mammalian herbivore, the common brushtail possum ( Trichosurus vulpecula), in a temperate forest in New Zealand. We quantified the spatial and temporal variation in four key aspects of the foliar chemistry (total nitrogen, available nitrogen, in vitro dry matter digestibility and tannin effect) of 275 trees representing five native tree species. Simultaneously, we assessed the severity of browsing damage caused by possums on those trees in order to relate selective browsing to foliar nutritional quality. We found significant spatial and temporal variation in nutritional quality among individuals of each tree species examined, as well as among tree species. There was a positive relationship between the available nitrogen concentration of foliage (a measure of in vitro digestible protein) and the severity of damage caused by browsing by possums. This study highlights the importance of nutritional quality, specifically, the foliar available nitrogen concentration of individual trees, in predicting the impact of an invasive mammal. Revealing the underlying cause of patchy browsing by an invasive mammal provides new insights for conservation of native forests and targeted control of invasive herbivores in forest ecosystems.

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          Most cited references 13

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          Introduced species and their missing parasites.

          Damage caused by introduced species results from the high population densities and large body sizes that they attain in their new location. Escape from the effects of natural enemies is a frequent explanation given for the success of introduced species. Because some parasites can reduce host density and decrease body size, an invader that leaves parasites behind and encounters few new parasites can experience a demographic release and become a pest. To test whether introduced species are less parasitized, we have compared the parasites of exotic species in their native and introduced ranges, using 26 host species of molluscs, crustaceans, fishes, birds, mammals, amphibians and reptiles. Here we report that the number of parasite species found in native populations is twice that found in exotic populations. In addition, introduced populations are less heavily parasitized (in terms of percentage infected) than are native populations. Reduced parasitization of introduced species has several causes, including reduced probability of the introduction of parasites with exotic species (or early extinction after host establishment), absence of other required hosts in the new location, and the host-specific limitations of native parasites adapting to new hosts.
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            The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal.

            Plants contain a variety of chemical defenses that strongly affect feeding rates in captive mammals, but their effects on the fitness of wild herbivores are largely unknown. This is because the complexity of defensive compounds, and herbivores' counteradaptations to them, make their effects in the wild difficult to measure. We show how tannins interact with protein to produce spatial variation in the nutritional quality of eucalypt foliage, which is related to demography in a wild population of a marsupial folivore, the common brushtail possum (Trichosurus vulpecula Kerr). Tannins reduced the digestibility of nitrogen (N) in vitro, creating variation in available N concentrations among the home ranges of individual possums in an otherwise homogeneous habitat. This was strongly correlated with reproductive success: females with better quality trees in their home range reproduced more often and had faster-growing offspring. These results demonstrate a powerful mechanism by which spatial variation in plant chemistry may control herbivore population dynamics in nature.
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              Predicting folivorous primate abundance: validation of a nutritional model.

              Understanding the determinants of animal abundance has become more vital as ecologists are increasingly asked to apply their knowledge to the construction of informed management plans. However, there are few general models are available to explain variation in abundance. Some notable exceptions are studies of folivorous primates, in which the protein-to-fiber ratio of foods has been shown to predict biomass. Here we examine the generality of Milton's [American Naturalist 114:363-378, 1979] protein/fiber model by providing a detailed analysis of diet selection in black-and-white colobus monkeys (Colobus guereza), and applying the model to populations shown to be stable; an assumption not previously examined. Based on observations of two groups of black-and-white colobus in Kibale National Park, Uganda, and one group in a forest fragment, we documented that the animals selected young leaves that had more protein, were more digestible, and had a higher protein-to-fiber ratio than mature leaves. The mature leaves did not differ from young leaves with respect to secondary compounds or mineral content (with the exceptions of copper and zinc). All of the colobus groups selected foods with a high protein-to-fiber ratios. However, one group also selected more digestible foods, and in another group, foraging efforts were positively related to zinc and negatively related to potassium. Previous studies that examined Milton's protein/fiber model did not demonstrate that the study populations were stable. If some populations were not at carrying capacity, then the correlations drawn between food availability and/or quality and folivore biomass may have been spurious. To address this issue, we censused a series of forest fragments in 1995 and again in 2000. We found that the populations in these fragments had declined from 165 in 1995 to 119 animals in 2000. However, based on evidence of population stability and lack of forest disturbance, we concluded that five of the original populations were stable. The biomass of these populations was related to the protein-to-fiber ratio of the fragment's trees. Combining our data with published data, we demonstrate that the protein-to-fiber ratios of mature leaves available to these folivorous primates accounted for 87% of the variance in their biomass. Copyright 2004 Wiley-Liss, Inc.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                12 May 2016
                2016
                : 11
                : 5
                Affiliations
                [1 ]Research School of Biology, The Australian National University, Acton, ACT 2601, Australia
                [2 ]Landcare Research, PO Box 69040, Lincoln, 7640, New Zealand
                College of Agricultural Sciences, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HRW WJF WAR MCB EPH. Performed the experiments: HRW. Analyzed the data: DS HRW. Contributed reagents/materials/analysis tools: MCB WAR EPH. Wrote the paper: HRW WJF DS.

                [¤a]

                Current address: Department of Biology, University of York, York, YO10 5DD, United Kingdom

                [¤b]

                Current address: Institute for Applied Ecology, University of Canberra, Bruce, ACT 2601, Australia

                Article
                PONE-D-16-03889
                10.1371/journal.pone.0155216
                4865184
                27171381
                © 2016 Windley et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 4, Tables: 4, Pages: 16
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003524, Ministry of Business, Innovation and Employment;
                Award ID: C09X0909
                Funded by: funder-id http://dx.doi.org/10.13039/501100000923, Australian Research Council;
                Award ID: DP0986142
                Award Recipient :
                Funded by: Australian Postgraduate Award
                Funding was provided by the Ministry of Business, Innovation and Employment, Contract no: C09X0909 to Landcare Research, and the Australian Research Council (DP0986142) to WJF. HRW was a recipient of an Australian Postgraduate Award. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Marsupials
                Opossums
                Biology and Life Sciences
                Organisms
                Plants
                Trees
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Plant-Herbivore Interactions
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Plant-Herbivore Interactions
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Animal Interactions
                Plant-Herbivore Interactions
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Herbivory
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Herbivory
                Earth Sciences
                Seasons
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Biology and Life Sciences
                Plant Science
                Dendrology
                Biology and Life Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Terrestrial Environments
                Forests
                Custom metadata
                Data are publicly accessible on a website hosted by Landcare Research Ltd. doi: 10.7931/J23N21BW ( http://dx.doi.org/10.7931/J23N21BW). The license on the data is no more restrictive than CCBY 4.0.

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