Difference between revisions of "Restoration of Ecological Function in Terrestrial Systems Impacted by Invasive Species"

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'''Key Resources''':  
 
'''Key Resources''':  
  
*[[Media:Hobbs2011.pdf | Intervention Ecology: Applying Ecological Science in the Twenty-first Century]]<ref>Hobbs, R.J., Hallett, L.M., Ehrlich, P.R., and Mooney, H.A., 2011. Intervention Ecology: Applying Ecological Science in The Twenty-first Century. BioScience, 61(6), pp. 442–450. [https://doi.org/10.1525/bio.2011.61.6.6 doi: 10.1525/bio.2011.61.6.6] [[Media:Hobbs2011.pdf | Article pdf]]</ref>
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*[//www.enviro.wiki/images/e/e4/Hobbs2011.pdf Intervention Ecology: Applying Ecological Science in the Twenty-first Century]<ref name=":0">Hobbs, R.J., Hallett, L.M., Ehrlich, P.R., and Mooney, H.A., 2011. Intervention Ecology: Applying Ecological Science in The Twenty-first Century. BioScience, 61(6), pp. 442–450. [https://doi.org/10.1525/bio.2011.61.6.6 doi: 10.1525/bio.2011.61.6.6] [//www.enviro.wiki/images/e/e4/Hobbs2011.pdf Article pdf]</ref>
*[[Media:Rogers2017.pdf | Effects of An Invasive Predator Cascade to Plants Via Mutualism Disruption]]<ref>Rogers, H.S., Buhle, E.R., HilleRisLambers, J., Fricke, E.C., Miller, R.H., and Tewksbury, J.J., 2017. Effects of an invasive predator cascade to plants via mutualism disruption. Nature Communications, 8:14557. [https://doi.org/10.1038/ncomms14557 doi: 10.1038/ncomms14557] [[Special:FilePath/Rogers2017.pdf Article pdf|Media:Rogers2017.pdf Article pdf]]</ref>
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*[//www.enviro.wiki/images/a/a1/Rogers2017.pdf Effects of An Invasive Predator Cascade to Plants Via Mutualism Disruption]<ref name=":2">Rogers, H.S., Buhle, E.R., HilleRisLambers, J., Fricke, E.C., Miller, R.H., and Tewksbury, J.J., 2017. Effects of an invasive predator cascade to plants via mutualism disruption. Nature Communications, 8:14557. [https://doi.org/10.1038/ncomms14557 doi: 10.1038/ncomms14557] [//www.enviro.wiki/images/a/a1/Rogers2017.pdf Article pdf]</ref>
*[[Media:Thierry2020.pdf Where to Rewild? A Conceptual Framework to Spatially Optimize Ecological Function]]<ref>Thierry, H., and Rogers, H., 2020. Where to rewild? A conceptual framework to spatially optimize ecological function. Proceedings of the Royal Society B: Biological Sciences, 287:20193017. [https://doi.org/10.1098/rspb.2019.3017 doi: 10.1098/rspb.2019.3017] [//www.enviro.wiki/images/2/21/Thierry2020.pdf Article pdf]</ref>
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*[//www.enviro.wiki/images/2/21/Thierry2020.pdf Where to Rewild? A Conceptual Framework to Spatially Optimize Ecological Function]<ref name=":7">Thierry, H., and Rogers, H., 2020. Where to rewild? A conceptual framework to spatially optimize ecological function. Proceedings of the Royal Society B: Biological Sciences, 287:20193017. [https://doi.org/10.1098/rspb.2019.3017 doi: 10.1098/rspb.2019.3017] <nowiki>[[Media:Thierry2020.pdf | Article pdf]]</nowiki></ref>
  
== Introduction- Invasion Biology ==
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==Introduction- Invasion Biology==
 
Because of the increased ease and frequency of transportation of people and goods across the globe, almost all ecosystems have species introduced by humans that do not share an evolutionary history with the native members of the ecosystem. Only some of these species survive to reproduce, and even fewer cause harm<ref>Williamson, M., and Fitter, A.,1996. The varying success of invaders. Ecology, 77(6), pp. 1661–1666.[https://doi.org/10.2307/2265769 | doi:10.2307/2265769]</ref>. Invasive species are recognized as having been transported to a novel geographic area, establishing in that area, and then causing ecological or economic harm to the systems in that geographic region<ref>Blackburn, T.M., Pyšek, P., Bacher, S., Carlton, J.T., Duncan, R.P., Jarošík, V., Wilson, J.R., and Richardson, D.M., 2011. A proposed unified framework for biological invasions. Trends in Ecology & Evolution, 26(7), pp. 333–339. [https://doi.org/10.1016/j.tree.2011.03.023 doi: 10.1016/j.tree.2011.03.023]
 
Because of the increased ease and frequency of transportation of people and goods across the globe, almost all ecosystems have species introduced by humans that do not share an evolutionary history with the native members of the ecosystem. Only some of these species survive to reproduce, and even fewer cause harm<ref>Williamson, M., and Fitter, A.,1996. The varying success of invaders. Ecology, 77(6), pp. 1661–1666.[https://doi.org/10.2307/2265769 | doi:10.2307/2265769]</ref>. Invasive species are recognized as having been transported to a novel geographic area, establishing in that area, and then causing ecological or economic harm to the systems in that geographic region<ref>Blackburn, T.M., Pyšek, P., Bacher, S., Carlton, J.T., Duncan, R.P., Jarošík, V., Wilson, J.R., and Richardson, D.M., 2011. A proposed unified framework for biological invasions. Trends in Ecology & Evolution, 26(7), pp. 333–339. [https://doi.org/10.1016/j.tree.2011.03.023 doi: 10.1016/j.tree.2011.03.023]
</ref><ref>Kraus, F., 2008. Alien Reptiles and Amphibians: A Scientific Compendium and Analysis. Springer, Dordrecht, Netherlands. ISBN: 978-1-4020-8945-9/eISBN: 978-1-4020-8946-6 [https://doi.org/10.1007/978-1-4020-8946-6 doi:10.1007/978-1-4020-8946-6]</ref><ref>Kraus, F., 2015. Impacts from Invasive Reptiles and Amphibians. Annual Review of Ecology, Evolution, and Systematics, 46(1), pp. 75–97. [https://doi.org/10.1146/annurev-ecolsys-112414-054450 doi:10.1146/annurev-ecolsys-112414-054450]</ref>. Several attempts have been made by researchers in the field to distinguish “invasive” from “non-native,” “alien” and “exotic”<ref>Colautti, R.I., and MacIsaac, H.J., 2004. A neutral terminology to define ‘invasive’species. Diversity and Distributions, 10(2), pp. 135–141.  [https://doi.org/10.1111/j.1366-9516.2004.00061.x doi:10.1111/j.1366-9516.2004.00061.x] [[Media:Colautti 2004.pdf | Article pdf]]</ref><ref>Richardson, D.M., Pyšek, P., Rejmánek, M., Barbour, M.G., Panetta, F.D., and West, C.J., 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions, 6(2), pp. 93–107. [https://doi.org/10.1046/j.1472-4642.2000.00083.x doi: 10.1046/j.1472-4642.2000.00083.x] [[Media:Richardson2000.pdf | Article pdf]]</ref>.  Invasive species were defined in The President's [https://www.invasivespeciesinfo.gov/executive-order-13112#:~:text=On%20Feb%203%2C%201999%2C%20Executive,11987%20of%20May%2024%2C%201977. Executive Order 13112] (1999) as, “an alien species whose introduction does or is likely to cause economic or environmental harm or harm to human health”. The [https://www.gisp.org/ Global Invasive Species Program] of the [https://www.iucn.org/ International Union for the Conservation of Nature] accepts a similar definition of “invasive alien species” as “This subset of alien species that become established in a new environment, then proliferate and spread in ways that are destructive to native ecosystems, human health, and ultimately human welfare…”<ref>McNeely, J.A., 2000. The future of alien invasive species: changing social views. In: H.A. Mooney and R.J. Hobbs (eds), Invasive Species in a Changing World.  Island Press, Washington, DC, pp. 171–190. ISBN: 978-1559637824.</ref>. Invasive species are one of the greatest threats to ecological and economic well-being of the planet. Developing common definitions was essential given the prevalence and urgency of the impacts.
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</ref><ref>Kraus, F., 2008. Alien Reptiles and Amphibians: A Scientific Compendium and Analysis. Springer, Dordrecht, Netherlands. ISBN: 978-1-4020-8945-9/eISBN: 978-1-4020-8946-6 [https://doi.org/10.1007/978-1-4020-8946-6 doi:10.1007/978-1-4020-8946-6]</ref><ref>Kraus, F., 2015. Impacts from Invasive Reptiles and Amphibians. Annual Review of Ecology, Evolution, and Systematics, 46(1), pp. 75–97. [https://doi.org/10.1146/annurev-ecolsys-112414-054450 doi:10.1146/annurev-ecolsys-112414-054450]</ref>. Several attempts have been made by researchers in the field to distinguish “invasive” from “non-native,” “alien” and “exotic”<ref>Colautti, R.I., and MacIsaac, H.J., 2004. A neutral terminology to define ‘invasive’species. Diversity and Distributions, 10(2), pp. 135–141.  [https://doi.org/10.1111/j.1366-9516.2004.00061.x doi:10.1111/j.1366-9516.2004.00061.x] [//www.enviro.wiki/images/5/58/Colautti_2004.pdf Article pdf]</ref><ref>Richardson, D.M., Pyšek, P., Rejmánek, M., Barbour, M.G., Panetta, F.D., and West, C.J., 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions, 6(2), pp. 93–107. [https://doi.org/10.1046/j.1472-4642.2000.00083.x doi: 10.1046/j.1472-4642.2000.00083.x] [//www.enviro.wiki/images/8/80/Richardson2000.pdf Article pdf]</ref>.  Invasive species were defined in The President's [https://www.invasivespeciesinfo.gov/executive-order-13112#:~:text=On%20Feb%203%2C%201999%2C%20Executive,11987%20of%20May%2024%2C%201977. Executive Order 13112] (1999) as, “an alien species whose introduction does or is likely to cause economic or environmental harm or harm to human health”. The [https://www.gisp.org/ Global Invasive Species Program] of the [https://www.iucn.org/ International Union for the Conservation of Nature] accepts a similar definition of “invasive alien species” as “This subset of alien species that become established in a new environment, then proliferate and spread in ways that are destructive to native ecosystems, human health, and ultimately human welfare…”<ref>McNeely, J.A., 2000. The future of alien invasive species: changing social views. In: H.A. Mooney and R.J. Hobbs (eds), Invasive Species in a Changing World.  Island Press, Washington, DC, pp. 171–190. ISBN: 978-1559637824.</ref>. Invasive species are one of the greatest threats to ecological and economic well-being of the planet. Developing common definitions was essential given the prevalence and urgency of the impacts.
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Efforts focused on early detection and rapid response are preferable to trying to control a species once it has established<ref>Simberloff, D., Martin, J.-L., Genovesi, P., Maris, V., Wardle, D.A., Aronson, J., Courchamp, F., Galil, B., García-Berthou, E., Pascal, M., Pyšek, P., Sousa, R., Tabacchi, E., and Vilà, M., 2013. Impacts of biological invasions: what’s what and the way forward. Trends in Ecology & Evolution, 28(1), pp. 58–66. [https://doi.org/10.1016/j.tree.2012.07.013 doi: 10.1016/j.tree.2012.07.013]</ref>. However, in many cases, it can be difficult to identify potential invasive species until they have started causing obvious detrimental effects.
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Once a species has been identified as invasive, there are some key questions that need to be asked and answered to attempt restoration of ecological function within an ecosystem. The return of ecosystems to their original state may not be financially feasible or even technically possible due to extinctions, invasive species, or climate change, but these ecosystems still have tremendous value<ref name=":0" />, and managing them to maximize that value requires an understanding of how these systems function. In places where the cause of species loss and species endangerment are still present and the invasive species removal appears intractable, managers may need to utilize the strategy of “intervention ecology” (Figure 1)<ref name=":0" />, restoring function within these novel systems without attempting to restore the original ecosystem<ref>Marris, E. (2011). Rambunctious Garden: Saving Nature in a Post-wild World. Bloomsbury, New York. ISBN: 978-1-6081-9454-4/eISBN: 978-1-6081-9455-1</ref>.
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[[File: ThierryFig1.png|thumb|650px|left | Figure 1. When an invasive species cannot be eradicated, and disrupts important ecological processes, then, an intervention ecology approach is required to restore function and stability to the system.]]
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A well-known example of an invasive species that caused detrimental effects to an entire ecosystem, where the intervention ecology approach is now being applied, is the [[wikipedia:Brown_tree_snake|brown treesnake]] (''Boiga irregularis'') on the island of Guam. The snake was introduced to the island at the end of WWII, likely a stowaway aboard U.S. military cargo ships. Within approximately 40 years the snake had spread throughout the entire island and eliminated 9 of the 11 species of native forest birds<ref name=":3">Savidge, J.A., 1987. Extinction of an Island Forest Avifauna by an Introduced Snake. Ecology 68(3), pp. 660–668. [https://doi.org/10.2307/1938471 doi: 10.2307/1938471]</ref><ref>Wiles, G.J., Bart, J., Beck, R.E., and Aguon, C.F., 2003. Impacts of the Brown Tree Snake: Patterns of Decline and Species Persistence in Guam’s Avifauna. Conservation Biology, 17(5), pp. 1350–1360. [https://doi.org/10.1046/j.1523-1739.2003.01526.x doi: 10.1046/j.1523-1739.2003.01526.x]</ref>. While the brown treesnake may be the most infamous, other introduced species also have detrimental effects on Guam’s ecosystems. Rats (Rattus sp.), [[wikipedia:Wild_boar|feral pigs]] (''Sus scrofa''), and [[wikipedia:Philippine_deer|Philippine deer]] (''Rusa mariannae'') are well-established and numerous arthropod pests, including the little fire ant and coconut rhinoceros beetle are taking a noticeable toll on local species. 
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==Identifying the Impacts of Non-native Species on the Ecosystem==
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When a species has been identified in an ecosystem, it is essential to determine how it has impacted the stability, composition, and diversity of the ecosystem. This may be done by comparing changes over time, if data exist from prior to the invasion, or comparing across space if comparable areas exist nearby. Experiments that compare areas where the invasive is excluded to areas where it is present (aka ‘exclosure experiments’) may also shed light on how the system would operate in the absence of the invader.  
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Invasive species may cause the decline or extirpation of native species that provide essential ecological functions in the ecosystem. For example, the [http://ky-caps.ca.uky.edu/hemlock-woolly-adelgid Hemlock Woolly Adelgid] (''Adelges tsugae''), an invasive insect from Asia, has led to the destruction of up to 80% of the hemlock trees in the Eastern United States, which then impacted overall forest composition. In Florida, the [[wikipedia:Python_molurus|burmese python]] (''Python molurus'') became a destructive invasive species in less than 20 years by causing severe declines in mammal populations through predation<ref>Hoyer, I.J., Blosser, E.M., Acevedo, C., Thompson, A.C., Reeves, L.E., and Burkett-Cadena, N.D., 2017. Mammal decline, linked to invasive Burmese python, shifts host use of vector mosquito towards reservoir hosts of a zoonotic disease. Biology Letters, 13(10):20170353.[https://doi.org/10.1098/rsbl.2017.0353 doi: 10.1098/rsbl.2017.0353] [//www.enviro.wiki/images/c/c2/Hoyer2017.pdf Article pdf]</ref>.
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Invasive species also cause problems for human health and economies. They can be disease vectors, such as the [http://cisr.ucr.edu/asian_tiger_mosquito.html Asian tiger mosquito] (''Aedes albopictus''), which can transmit [[wikipedia:Dengue_fever|Dengue Fever]] and [[wikipedia:Chikungunya|Chikungunya]]. Invasive species can impact local and even large economies<ref>Crowl, T.A., Crist, T.O., Parmenter, R.R., Belovsky, G., and Lugo, A.E., 2008. The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment, 6(5), pp. 238–246. [https://doi.org/10.1890/070151 doi: 10.1890/070151] [//www.enviro.wiki/images/b/b7/Crowl2008.pdf Article pdf]</ref><ref name=":1">Pimentel, D., Zuniga, R., and Morrison, D., 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52(3), pp. 273–288. [https://doi.org/10.1016/j.ecolecon.2004.10.002 doi: 10.1016/j.ecolecon.2004.10.002]</ref>. Brown treesnakes on Guam climb onto powerlines or into transistor stations, and are linked to nearly 200 power outages per year costing approximately $4.5 million<ref>Fritts, T.H. (2002). Economic costs of electrical system instability and power outages caused by snakes on the island of Guam. International Biodeterioration & Biodegradation, 49(2-3), pp. 93–100. [https://doi.org/10.1016/S0964-8305(01)00108-1 doi: 10.1016/S0964-8305(01)00108-1]</ref>. Species may also impact economically important animals and plants<ref name=":1" />.
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The nearby islands of Saipan, Rota, and Tinian, together with Guam, comprise the inhabited southern islands of the Mariana Island archipelago. Saipan, Tinian, and Rota have flora and fauna similar to Guam but do not have the invasive snake. Comparing Guam, Saipan, Rota, and Tinian offers a unique accidental experiment to test the effects of an invasive predator and its cascading effects on a forest system, particularly through the loss of native forest birds and their accompanying ecological roles. We use this as an example for designing restoration approaches to restore function to a system with an intractable invasive species problem. 
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It took several decades after the introduction of the brown treesnake to Guam for it to be identified as the culprit behind bird declines, and even longer to identify the cascading ecological effects of bird loss. Because the islands to the north of Guam have similar forests but still retain their bird populations, it was possible to set up comparative studies to determine impacts. Since 5 of the bird species were frugivores, the loss of seed dispersal stands out as a major impact on the forests of Guam<ref>Caves, E.M., Jennings, S.B., HilleRisLambers, J., Tewksbury, J.J., and Rogers, H.S., 2013. Natural Experiment Demonstrates That Bird Loss Leads to Cessation of Dispersal of Native Seeds from Intact to Degraded Forests. PLoS One, 8(5), e65618. [https://doi.org/10.1371/journal.pone.0065618 doi: 10.1371/journal.pone.0065618] [//www.enviro.wiki/images/8/8a/Caves2013.pdf Article pdf]</ref>. With reduced seed dispersal, seeds fall underneath their parent tree unhandled by frugivores, which results in a lower chance of germination<ref name=":2" />. In addition, treefall gaps are filled almost exclusively by the trees adjacent to the gap, which has led to reduced species richness in treefall gap seedling communities<ref name=":5">Wandrag, E.M., Dunham, A.E., Duncan, R.P., and Rogers, H.S., 2017. Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings. Proceedings of the National Academy of Sciences 114(40), pp. 10689–10694. [https://doi.org/10.1073/pnas.1709584114 doi: 10.1073/pnas.1709584114] [//www.enviro.wiki/images/1/14/Wandrag2017.pdf Article pdf]</ref>. In addition, spiders are more numerous in Guam compared to the other islands, presumably due to a lack of vertebrate predators<ref>Rogers, H., Lambers, J.H.R., Miller, R., and Tewksbury, J.J., 2012. ‘Natural Experiment’ Demonstrates Top-Down Control of Spiders by Birds on a Landscape Level. PLoS One, 7(9):e43446. [https://doi.org/10.1371/journal.pone.0043446 doi: 10.1371/journal.pone.0043446] [//www.enviro.wiki/images/7/71/Rogers2012.pdf Article pdf]</ref>. The full impact of the snake is still being uncovered.
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==Preventing Further Degradation by Managing the Invasive Species==
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Once a species has been identified as being invasive in an ecosystem, it is essential to act as quickly as possible in order to prevent further impacts. In some systems, eradication may be impossible, in which case control methods should aim at containing the population. This step is challenging and calls for the cooperation of many actors such as scientists, policy holders and funding agencies to identify methods to control the invasive species across the landscape.
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Many tools exist and are being developed to manage invasive species<ref>Wittenberg, R., and Cock, M.J., 2001. Invasive alien species: a toolkit of best prevention and management practices. CAB International, Wallingford, Oxon, UK. ISBN: 0 85199 569 1 [https://doi.org/10.1079/9780851995694.0000 doi: 10.1079/9780851995694.0000]</ref>, but the specific tools to use depend on the species and habitat. Mechanical control methods, such as hunting and invasive plant removal, are manually intensive and can be costly if an invasive species has reached high densities. Chemical control methods such as application of herbicides and pesticides have proven effective but are often costly and may be socially unpalatable<ref name=":1" />.
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Sterilization and gene drive techniques are being developed for use in invasive species control. Sterilization involves sterilizing either males or females of a species and releasing those sterilized individuals into a population where they are mating but not physically able to produce offspring. Sterilization has been used successfully to suppress fruit fly populations<ref>
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Zacharopoulou, A., Augustinos, A.A., Drosopoulou, E., Tsoumani, K.T., Gariou‐Papalexiou, A., Franz, G., Mathiopoulos, K.D., Bourtzis, K., and Mavragani‐Tsipidou, P.,2017. A review of more than 30 years of cytogenetic studies of T ephritidae in support of sterile insect technique and global trade. Entomologia Experimentalis et Applicata, 164(3), pp. 204–225. [https://doi.org/10.1111/eea.12616 doi: 10.1111/eea.12616] [//www.enviro.wiki/images/a/ad/Zacharopoulou_2017.pdf Article pdf]</ref>  and has shown some success in pilot studies targeting mosquitoes<ref>Lees, R.S., Gilles, J.R., Hendrichs, J., Vreysen, M.J., and Bourtzis, K., 2015. Back to the future: the sterile insect technique against mosquito disease vectors. Current Opinion in Insect Science, 10, pp.156–162. [https://doi.org/10.1016/j.cois.2015.05.011 doi: 10.1016/j.cois.2015.05.011] [//www.enviro.wiki/images/2/21/Lees2015.pdf Article pdf]</ref>. Gene drive approaches manipulate a genome to increase the likelihood specific alleles will be inherited<ref>
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Champer, J., Buchman, A., and Akbari, O.S., 2016. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nature Reviews Genetics, 17, pp. 146-159.  [https://doi.org/10.1038/nrg.2015.34 doi: 10.1038/nrg.2015.34] [//www.enviro.wiki/images/f/fd/Champer2016.pdf Article pdf]</ref>. Gene drive control methods are being pursued for rats and some other invasive species<ref>Harvey-Samuel, T., Ant, T., and Alphey, L., 2017. Towards the genetic control of invasive species. Biological Invasions, 19, pp. 1683–1703. [https://doi.org/10.1007/s10530-017-1384-6 doi: 10.1007/s10530-017-1384-6] [[Media:Harvey2017.pdf | Article pdf]</ref><ref>Leitschuh, C.M., Kanavy, D., Backus, G.A., Valdez, R.X., Serr, M., Pitts, E.A., Threadgill, D., and Godwin, J., 2018. Developing gene drive technologies to eradicate invasive rodents from islands. Journal of Responsible Innovation, 5(S1), pp. S121–S138. [https://doi.org/10.1080/23299460.2017.1365232 doi: 10.1080/23299460.2017.1365232] [//www.enviro.wiki/images/6/6f/Leitschuh2018.pdf Article pdf]</ref>, but remain controversial because of uncertainty of its safety and fears that effects may reach beyond target populations<ref>Esvelt, K.M., and Gemmell, N.J., 2017. Conservation demands safe gene drive. PLoS Biology, 15(11), e2003850. [https://doi.org/10.1371/journal.pbio.2003850 doi: 10.1371/journal.pbio.2003850] [//www.enviro.wiki/images/8/85/Esvelt2017.pdf Article pdf]</ref>.  
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In the case of invasive brown treesnakes on Guam, the snakes already occupied the majority of the island by the time management began, so management efforts were directed at control rather than eradication. The snake had spread throughout the entire island by the time it was linked to the loss of birds in the mid-1980’s. Dr. Julie Savidge ruled out other suspected agents such as disease and pathogens, and temporally and geographically aligned the spread of the snake with the disappearance of birds across the island<ref name=":3" />, making a convincing case that the snake was the culprit. However, she still faced difficulties convincing others that a single species of introduced snake was responsible for the alarming disappearance of native birds, so control of the snake didn’t start occurring until 1993. The goal of control has largely been to keep the snakes from establishing on other islands, such as Hawaii. Initial control methods implemented included snake trapping, visual searching, and detector dogs to inspect cargo and planes leaving the island, and concrete barriers to quarantine cargo originating from Guam on snake-free islands<ref>Clark, C., Clark, L., and Siers, S., 2018. Brown Tree Snakes: Methods and Approaches for Control. In:  W.C. Pitt, J.C. Beasley, and G.W Witmer (eds), Ecology and Management of terrestrial vertebrate invasive species in the United States. CRC Press, Boca Raton, FL. pp. 107–134. eISBN: 978-1-3151-5707-8 [https://doi.org/10.1201/9781315157078 doi: 10.1201/9781315157078] [//www.enviro.wiki/images/a/aa/Clark2018.pdf Chapter pdf]
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</ref>. Recently a chemical control method has been developed. This method consists of dropping dead mice with an attached acetaminophen tablet (a toxin for brown treesnakes) from helicopters to the forest canopy where snakes will encounter and consume them. These “mouse-drops” need to occur at regular intervals over a prolonged period to ensure all snakes in an area will be affected<ref>
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Siers, S.R., Barnhart, P.D., Shiels, A.B., Rabon, J.A., Volsteadt, R.M., Chlarson, F.M., Larimer, J.R., Dixon, J.C., and Gosnell, R.J., 2018. Monitoring Brown Treesnake Activity Before and After an Automated Aerial Toxicant Treatment. Final Report QA-2621. USDA, APHIS, WS, NWRC. Hilo, HI. [//www.enviro.wiki/images/5/5a/Siers2018.pdf Report pdf]</ref>. Areas may be enclosed with snake barriers in order to prevent incursion and reach eradication. The barriers erected for this purpose in Guam also serve as effective exclosures for invasive deer and pigs. Researchers are also trying to predict indirect effects of invasive control that may require further management, such as increases in invasive small mammals with the eradication of snakes or increases in weedy plant species with the eradication of ungulates.
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==Restoring Degraded Ecological Functions in the Ecosystem  ==
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[[File: ThierryFig2.png|thumb|650px|right | Figure 2. Conceptual framework for restoring ecological functions in an ecosystem. First, it is essential to identify the ecological services that need to be restored and the species that may be able to provide those services. The next step is to conduct a landscape-level evaluation of the potential spatial distribution of both the service and its provider. Then, both should be combined to identify optimal rewilding areas. Finally, societal constraints should be taken into account to develop effective management strategies and policies.]]
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In an ideal situation, the invasive species would be eradicated, and then native species restored across the landscape, in turn restoring ecological function. However, complete eradication is often impossible. Instead, invasive population reduction or local eradication combined with restoration of native species or surrogate species within protected areas may be possible. In this section, we describe a proposed conceptual framework (Figure 2) to use when planning invasive control and rewilding scenarios for the purposes of restoring ecological functions.
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===Identifying the Key Ecosystem Function Providers===
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The degradation of an ecosystem is often caused by the extirpation of ecological functions provided by keystone or foundational species. If these functionally important species are not entirely extirpated from the system, the first step is to identify strategies for increasing the population, via conserving or enhancing essential habitats for these species and controlling the invasive species. In an ideal situation, one would be able to conduct an ecological function analysis to assess the abundance of the species required to provide sufficient ecological function<ref>
 +
Brodie, J.F., Redford K. H., and Doak, D.F., 2018. Ecological Function Analysis: Incorporating Species Roles into Conservation. Trends in Ecology and Evolution, 33(11), pp.840–850. [https://doi.org/10.1016/j.tree.2018.08.013 doi: 10.1016/j.tree.2018.08.013] [[Media:Brodie2018.pdf | Article pdf]}</ref>. On the other hand, if these species are already extinct from the ecosystem, then rewilding will be necessary to restore the extirpated ecological functions. Rewilding can be defined as introducing locally extinct or ecologically similar species to perform ecosystem functions analogous to those of extinct species<ref>Seddon, P.J., Griffiths, C.J., Soorae, P.S., and Armstrong, D.P., 2014. Reversing defaunation: Restoring species in a changing world. Science, 345(6195), pp. 406–412. [https://doi.org/10.1126/science.1251818 doi: 10.1126/science.1251818]</ref><ref>Sobral-Souza, T., Lautenschlager, L., Morcatty, T.Q., Bello, C., Hansen, D., and Galetti, M., 2017. Rewilding defaunated Atlantic Forests with tortoises to restore lost seed dispersal functions. Perspectives in Ecology and Conservation, 15(4), pp. 300–307. [https://doi.org/10.1016/j.pecon.2017.08.005 doi: 10.1016/j.pecon.2017.08.005] [//www.enviro.wiki/images/3/33/Sobral2017.pdf  Article pdf]</ref><ref name=":4">Svenning, J.-C., Pedersen, P.B., Donlan, C.J., Ejrnæs, R., Faurby, S., Galetti, M., Hansen, D.M., Sandel, B., Sandom, C.J., and Terborgh, J.W., 2016. Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research. Proceedings of the National Academy of Sciences, 113(4), pp. 898–906. [https://doi.org/10.1073/pnas.1502556112 doi: 10.1073/pnas.1502556112] [//www.enviro.wiki/images/c/c7/Svenning2016.pdf  Article pdf]</ref> . In some cases, the species that has been extirpated can be found in ther systems. This is the most favorable case, with the possibility of translocating populations back into the ecosystem from these other sources. In other cases, if the species is globally extinct, rewilding can be done by selecting a species that can perform the same ecological function. This requires a great deal of caution, however, since predicting the extent of possible impacts on an ecosystem is very difficult. Many case studies have underlined the risks of such an approach<ref name=":4" />.
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[[File: ThierryFig3.png|thumb|500px|left | Figure 3. Seed dispersal kernels of five avian seed dispersers and 15 tree species on Saipan. Each panel represents a modelled species-specific interaction. For each interaction, we show standard dispersal curves, median and 99th percentile dispersal distances (numbers in top right of panel), and probability of seed dispersal greater than 500 m (filled dots represent probabilities greater than 0 and hollow dots represent probability = 0). The final column represents potential seed dispersal in two dimensions for bird species dispersing that given plant species (Rehm et al.,2019).]]
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The first step towards restoring a functional ecosystem in Guam was to identify frugivorous species that were effective seed dispersers<ref name=":6">Rehm, E.M., Chojnacki, J., Rogers, H.S., and Savidge, J.A., 2018. Differences among avian frugivores in seed dispersal to degraded habitats. Restoration Ecology, 26(4), pp. 760–766. [https://doi.org/10.1111/rec.12623 doi: 10.1111/rec.12623]</ref> . Nearby islands to Guam were unaffected by the brown treesnake and host avian communities similar to those historically present in Guam. This allowed us to prioritize reintroducing native species over introducing non-native species to Guam, and to assess which native frugivores were the most effective dispersers. We conducted studies to evaluate the effect of gut passage on germination of native forest tree species, and to study the movement of the candidate avian frugivore species (Figure 3)<ref>Rehm, E., Fricke, E., Bender, J., Savidge, J., and Rogers, H., 2019. Animal movement drives variation in seed dispersal distance in a plant–animal network. Proceedings of the Royal Society B, 286(1894):20182007. [https://doi.org/10.1098/rspb.2018.2007 doi: 10.1098/rspb.2018.2007] [//www.enviro.wiki/images/7/7d/Rehm2019.pdf Article pdf]</ref>. The Micronesian Starling was identified as an ideal candidate for rewilding because of its extensive diet, probability of dispersing seeds a long distance, and propensity for crossing from native to degraded forest, and thus assisting with forest regeneration<ref name=":6" />. Other strong candidates for rewilding are the [[wikipedia:Mariana_fruit_dove|Mariana Fruit Dove]] (''Ptilinopus roseicapilla'') and the [[wikipedia:Mariana_fruit_bat|Mariana Fruit Bat]] (''Pteropus mariannus''), because they also disperse many tree species. Furthermore, [[wikipedia:Micronesian_starling|Micronesian Starlings]] and Mariana Fruit Bats are still present in small populations on the island of Guam, even in the presence of the brown treesnake. Restoration of seed dispersal can be accomplished through a combination of increasing the population and extending the range of the two extant species and rewilding the extirpated species<ref name=":2" /><ref name=":5" /><ref>Wandrag, E.M., Dunham, A.E., Miller, R.H., and Rogers, H.S., 2015. Vertebrate seed dispersers maintain the composition of tropical forest seedbanks. AoB Plants, 7. [https://doi.org/10.1093/aobpla/plv130 doi: 10.1093/aobpla/plv130] [//www.enviro.wiki/images/e/e9/Wandrag2015.pdf Article pdf]</ref>. 
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===Identifying Key Areas in Need of Restoration===
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Restoration projects, and thus rewilding scenarios, are often limited in terms of financial resources. Future funding often relies on successful rewilding efforts, so projects should attempt to maximize success. To do so, rewilding should be spatially optimized to aim at restoring functions at key locations within the landscape. Misplacing rewilded species within the landscape can not only potentially lead to insufficient ecological function benefits but could also lead to negative ecological effects.  For example, pollinators and seed dispersers may pollinate or disperse non-native plants, exacerbating the ecological problems.  Thus, it is essential to understand the spatial pattern of lost ecological function, along with the habitat and desired and undesired effects of the rewilded species.
 +
 
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[[File: ThierryFig4.png|thumb|500px|right| Figure 4. Visual representation of scores assigned to different areas (here cells) of a landscape with (a) a service score representing areas that should be prioritized for functional restoration and (b) a reintroduction score for areas where rewilding would maximize functional restoration. Colors represent landcover types.]]
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In the case of Guam, an important goal is to reintroduce seed dispersal of native plant species across the island. Therefore, our first decision was that native forest should be prioritized since it provides the source of native seeds. We first focused on the dispersal behavior and the seed gut passage time of the one remaining native avian frugivore species– [[wikipedia:Micronesian_starling|Micronesian starlings]] (''Aplonis opaca''). Some of the important criteria that were taken into account were:
 +
 
 +
*Landcover type: represents different levels of forest degradation. Some landcover types were considered too degraded to benefit from seed dispersal.
 +
*Distance to native forest and density of surrounding native forest: represents the probability of starlings efficiently dispersing native seeds into the focal area.
 +
 
 +
Using this information, we identified areas across the island where the restoration of seed dispersal should be prioritized (Figure 4a)<ref name=":7" />.
 +
 
 +
===Identifying Potential Habitats for The Function Providers===
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In combination to the previously identified areas of interest for restoring ecological function, it is necessary to identify all potential areas that could successfully host the reintroduction of the desired service providers<ref>Hirzel, A.H., and Le Lay, G., 2008. Habitat suitability modelling and niche theory. Journal of Applied Ecology, 45(5), pp. 1372–1381. [https://doi.org/10.1111/j.1365-2664.2008.01524.x doi: 10.1111/j.1365-2664.2008.01524.x] [[Media:Hirzel2008.pdf | Article pdf]</ref>. Thus, habitat suitability should be mapped across the studied ecosystem. Habitat models allow evaluating the quality of habitat for a species within the studied landscape. These models can take into account a wide variety of parameters such as landcover, elevation, water availability, tolerance to disturbed habitats, and climate. Published methodologies are available as guidance to conceptualize a habitat suitability index that fits the biology of a wide range of function providers<ref>Donovan, M.L., Rabe, D.L., and Olson, C.E., 1987. Use of Geographic Information Systems to Develop Habitat Suitability Models. Wildlife Society Bulletin, 15(4), pp. 574–579.</ref><ref>
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Rondinini, C., Di Marco, M., Chiozza, F., Santulli, G., Baisero, D., Visconti, P., Hoffmann, M., Schipper, J., Stuart, S.N., and Tognelli, M.F. (2011). Global habitat suitability models of terrestrial mammals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 366(1578), pp. 2633–2641. [https://doi.org/10.1098/rstb.2011.0113 doi: 10.1098/rstb.2011.0113] [//www.enviro.wiki/images/4/45/Rondinini2011.pdf  Article pdf]</ref><ref>Van Horne, B., and Wiens, J.A., 1991. Forest bird habitat suitability models and the development of general habitat models. Fish and Wildlife Research, 8. [https://apps.dtic.mil/sti/citations/ADA322800 ADA322800] [//www.enviro.wiki/images/5/55/VanHorne1991.pdf  Report pdf]</ref>.
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In a Guam case study, we mapped habitat suitability as a binary function of either “suitable” or “non-suitable” for each potential service provider. This was done essentially by using landcover maps and assessing the different types of resource and habitats potentially used by the studied species within a virtual homerange. For example, habitat suitability for starlings, a generalist species, was defined by landcover types and the amount of native forest (food resource) present around the evaluated area.
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 +
===Identifying the Optimal Areas for Rewilding to Maximize the Restoration of Ecological Functions===
 +
Steps described in Sections 4.2 and 4.3 produce two maps: one identifies the areas that could host the service provider and the other shows where the function is most needed in our landscape. Planners can then overlay both maps and use this to estimate where rewilding would bring maximal functional restorations. To do so, scores can be assigned to each area (Figure 4b), based on the how much areas in need of functional restoration would be potentially impacted by rewilding.
 +
 
 +
In the Guam example (Figure 4), a score was assigned to each spatial entity that could host starlings, by drawing their potential home range if they inhabited each cell, then assigning a score based on the proportion of their home range that contained areas needing the ecological function, as identified in Section 4.1.
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===Linking Ecology to Decision-Making to Efficiently Restore Ecological Function Across an Area===
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When it comes to resource management or conservation projects, many entities and stakeholders are involved at a wide variety of scales. Scientists and managers may be able to identify spatial areas where rewilding would optimally restore ecological function, but the ecological optimum may not be feasible for financial, logistical, social, or political reasons. This leads to the emergence of social-ecological systems that each follow their own specific set of rules<ref>Folke, C., Hahn, T., Olsson, P., and Norberg, J., 2005. Adaptive Governance of Social-Ecological Systems. Annual Review of Environment and Resources, 30, pp. 441–473. [https://doi.org/10.1146/annurev.energy.30.050504.144511 doi: 10.1146/annurev.energy.30.050504.144511] [//www.enviro.wiki/images/0/0f/Folke2005.pdf Article pdf]</ref><ref>Folke, C., 2006. Resilience: The emergence of a perspective for social–ecological systems analyses. Global Environmental Change, 16(3), pp. 253–267. [https://doi.org/10.1016/j.gloenvcha.2006.04.002 doi: 10.1016/j.gloenvcha.2006.04.002] [//www.enviro.wiki/images/e/e9/Folke2006.pdf Article pdf]</ref><ref>Walker, B., Holling, C.S., Carpenter, S.R., and Kinzig, A., 2004. Resilience, adaptability and transformability in social–ecological systems. Ecology and Society, 9(2):5. [https://doi.org/10.5751/ES-00650-090205 doi: 10.5751/ES-00650-090205] [[Special:FilePath/Walker.pdf| Article pdf]]</ref>. Having so many different actors and interactions can lead to many difficulties when identifying efficient management decisions<ref>Adger, W.N., Brown, K., and Tompkins, E.L., 2005. The political economy of cross-scale networks in resource co-management. Ecology and Society, 10(2): 9. [https://doi.org/10.5751/ES-01465-100209 doi:10.5751/ES-01465-100209] [//www.enviro.wiki/images/1/15/Adger2005.pdf Article pdf]</ref><ref>Anderies, J.M., Walker, B.H., and Kinzig, A.P., 2006. Fifteen weddings and a funeral: case studies and resilience-based management. Ecology and Society, 11(1): 21. [https://doi.org/10.5751/ES-01690-110121 doi:10.5751/ES-01690-110121] [[Anderies2006.pdf | Article pdf]]</ref><ref>Pahl-Wostl, C., Sendzimir, J., and Jeffrey, P., 2009. Resources Management in Transition. Ecology and Society, 14(1):46. [https://doi.org/10.5751/ES-02898-140146 doi: 10.5751/ES-02898-140146] [//www.enviro.wiki/images/0/0c/Pahl-Wostl2009.pdf Article pdf]</ref>.
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To encapsulate some of these difficulties, aggregating individual ecological spatial units into more social entities should be considered to facilitate decision-making. Thus, management units, or clusters of previously identified small areas of interest that share common characteristics, should be identified based on all of the parameters that could influence management decisions. Typical examples of factors of importance to consider that can influence a management strategy applied to that area:
 +
 
 +
*Land ownership
 +
*Accessibility
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*Land cover
 +
*Topography
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*Budget
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For example, land ownership might exclude any type of intervention on private land. Thus, all inaccessible areas should be excluded from the model. Topography might render specific management methods useless and thus reduce the amount of possibilities. This should be taken into account and management units should be separated into different categories based on topography. Each of these factors will be taken into account to identify management unit types, each requiring a unique management approach. Once the social and geographic factors are taken into consideration, and managers decide which management types are relevant for the area, then the individual ecological areas identified in Section 4.4 should be aggregated into management units. Scoring these spatial entities is also recommended, by using the scores of all the smaller areas of interests, in order to be able to rank the management units by order of priority.
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[[File: ThierryFig5.png|thumb|650px|right | Figure 5. Map of the management units identified throughout the island of Guam when considering (a) both management unit types together and (b) Forest and non-forest management units separately. Management units are then ranked by management score and put into the following categories: Best (Top 10% of total area assigned to management units), Great (10-25%), Good (25-50%), Average (50-75%), and Poor (75-100%).]]
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In Guam, management units have been identified based on the methods that will be used to control the brown tree snake (Figure 5). Several management methods are possible, ranging from traps to the aerial distribution of toxicant drops across large areas. These methods are detailed in Section 3. The main method considered for the control of brown tree snake throughout the island is the aerial distribution of toxicant drops. This method may be socially unacceptable to carry out in or near urban habitats, thus land cover (urban) is one of the main drivers that defines which management approach will be considered for rewilding. The current restoration projects are led by the Department of Defense and thus will be conducted on military-owned land. Finally, fencing can be used as a method of regulation of snake population, in combination with other methods, but can be extremely costly. Topography, and especially steep cliff lines can act as potential natural barriers, reduce fencing cost, and thus should be considered when designing management units.
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Another step to consider is the importance of listening to local actors and involving communities<ref>Bryan, T.A., 2004. Tragedy Averted: The Promise of Collaboration. Society & Natural Resources, 17(10), pp. 881–896. [https://doi.org/10.1080/08941920490505284 doi: 10.1080/08941920490505284]</ref><ref>Conley, A., and Moote, M.A., 2003. Evaluating Collaborative Natural Resource Management. Society &Natural Resources, 16(5), pp. 371–386. [https://doi.org/10.1080/08941920309181 doi: 10.1080/08941920309181] [//www.enviro.wiki/images/c/ca/Conley2003.pdf Article pdf]</ref><ref name=":8">
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Frame, T.M., Gunton, T., and Day, J.C., 2004. The Role of Collaboration in Environmental Management: An Evaluation of Land And Resource Planning In British Columbia. Journal of Environmental Planning and Management, 47(1), pp. 59–82. [https://doi.org/10.1080/0964056042000189808 doi: 10.1080/0964056042000189808] [//www.enviro.wiki/images/0/07/Frame2004.pdf Article pdf]</ref>. Local expertise is an invaluable resource, and their involvement increases the chance of success for any project. Frame et al. (2004)<ref name=":8" /> illustrates a detailed example of how collaborative planning of land-use in British Columbia has led to resolving environmental conflict and produced significant additional benefits such as improved stakeholder relations, skills, and knowledge. Many tools, ranging from surveys to participatory board games, are available to decision-makers and land managers to involve community members and obtain feedback<ref>Brandt, E., 2006. Designing Exploratory Design Games: a framework for participation in participatory design? In: Proceedings of the Ninth Conference on Participatory Design: Expanding Boundaries in Design- Volume 1, PDC 2006, Trento, Italy, pp. 57–66. [https://doi.org/10.1145/1147261.1147271 doi:10.1145/1147261.1147271] [//www.enviro.wiki/images/f/f7/Brandt2006.pdf Article pdf]</ref><ref>Mendoza, G.A., and Prabhu, R., 2006. Participatory modeling and analysis for sustainable forest management: Overview of soft system dynamics models and applications. Forest Policy and Economics, 9(2), pp. 179–196. [https://doi.org/10.1111/j.1468-2885.2003.tb00290.x doi: 10.1111/j.1468-2885.2003.tb00290.x]</ref><ref>Morris, N., 2003. A Comparative Analysis of The Diffusion and Participatory Models in Development Communication. Communication Theory, 13(2), pp. 225–248. [https://doi.org/10.1016/j.forpol.2005.06.006 doi: 10.1016/j.forpol.2005.06.006]</ref>.
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Results from recent small group discussions on Guam suggested that some Guam residents had doubts about the extent of the impact of brown treesnakes, confusion about the effectiveness of current management actions, and distrust of certain entities carrying out research and management<ref>Wald, D.M., Nelson, K.A., Gawel, A.M., and Rogers, H.S., 2019. The role of trust in public attitudes toward invasive species management on Guam: A case study. Journal of Environmental Management, 229, pp. 133–144. [https://doi.org/110.1016/j.jenvman.2018.06.047 doi: 10.1016/j.jenvman.2018.06.047]</ref>. Given this disconnect between conservation managers and members of the public, we decided to test a participatory approach with multiple stakeholders. Surveys were distributed that presented a wide range of charismatic species, asking people to identify they deemed important as a conservation priority. Participants could delve further into management scenarios with a board game that focused on sequentially developing conservation towards achieving participants’ vision of the Guam in ten years.
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==Long-term Monitoring==
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Finally, once areas have been chosen for rewilding, strategies have been applied, and species have been brought within the ecosystem, it is essential to keep monitoring long-term progress. Eradication and rewilding projects can appear to be successful at first but fail in the long term because of a lack of effective monitoring and adaptive management. Re-invasion can happen, with impacts on rewilded species and further degradation of the system. The consequences of failed eradications or rewilding projects can extend beyond just the species within an ecosystem – public support, future funding, and trust in managers and researchers can be adversely impacted as well.
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==Summary==
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Restoration of ecological function in terrestrial systems impacted by invasive species is a multi-step process. After identifying an invasive species that is affecting ecological function, the following steps include managing the invasive to prevent further degradation, identifying which ecological functions have been disrupted, identifying the role native and non-native species could play in restoring ecological function, and managing the invasive to the extent that species can be restored that provide the missing ecological function. Finally, long-term monitoring and adaptive management is necessary to prevent re-invasion and further degradation.  
  
 
==References==
 
==References==
 
<references />
 
<references />
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==See Also==
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[https://www.invasivespeciesinfo.gov/ United States Department of Agriculture (USDA), National Invasive Species Information Center (NISIC)]
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[http://www.iucngisd.org/gisd/ Global Invasive Species Database]

Latest revision as of 19:54, 2 August 2022

Invasive species are responsible for the decline or extirpation of many species around the world. When those lost species provide essential ecological functions, the system may further degrade over time. Restoration ecology aims to restore these systems and associated ecological functions. It is important to first understand the invaders and their direct and indirect impacts to the native ecosystems. This requires a thorough understanding of the system and functions pre-invasion. Once these links and mechanisms are understood, managers must decide on a course of action to control or halt the spread of the invasive species and prevent further ecological degradation. Managers must determine what types of control are most appropriate for their systems as well as to what levels an invader must be controlled before restoration actions lead to improved ecological function. Deciding on specific restoration actions will vary considerably from system to system, but must involve considerations such as topography, landcover, feasibility, scale, social impacts, and timing. Specific details about habitats and species natural history are important to incorporate into planning models. Finally, monitoring and adaptive management throughout the course of the restoration and beyond are crucial to long-term success.

Related Article(s):


Contributors: Dr. Hugo Thierry, McKayla M. Spencer, Ann Marie Gawel, and Dr. Haldre Rogers


Key Resources:

Introduction- Invasion Biology

Because of the increased ease and frequency of transportation of people and goods across the globe, almost all ecosystems have species introduced by humans that do not share an evolutionary history with the native members of the ecosystem. Only some of these species survive to reproduce, and even fewer cause harm[4]. Invasive species are recognized as having been transported to a novel geographic area, establishing in that area, and then causing ecological or economic harm to the systems in that geographic region[5][6][7]. Several attempts have been made by researchers in the field to distinguish “invasive” from “non-native,” “alien” and “exotic”[8][9]. Invasive species were defined in The President's Executive Order 13112 (1999) as, “an alien species whose introduction does or is likely to cause economic or environmental harm or harm to human health”. The Global Invasive Species Program of the International Union for the Conservation of Nature accepts a similar definition of “invasive alien species” as “This subset of alien species that become established in a new environment, then proliferate and spread in ways that are destructive to native ecosystems, human health, and ultimately human welfare…”[10]. Invasive species are one of the greatest threats to ecological and economic well-being of the planet. Developing common definitions was essential given the prevalence and urgency of the impacts.

Efforts focused on early detection and rapid response are preferable to trying to control a species once it has established[11]. However, in many cases, it can be difficult to identify potential invasive species until they have started causing obvious detrimental effects.

Once a species has been identified as invasive, there are some key questions that need to be asked and answered to attempt restoration of ecological function within an ecosystem. The return of ecosystems to their original state may not be financially feasible or even technically possible due to extinctions, invasive species, or climate change, but these ecosystems still have tremendous value[1], and managing them to maximize that value requires an understanding of how these systems function. In places where the cause of species loss and species endangerment are still present and the invasive species removal appears intractable, managers may need to utilize the strategy of “intervention ecology” (Figure 1)[1], restoring function within these novel systems without attempting to restore the original ecosystem[12].

Figure 1. When an invasive species cannot be eradicated, and disrupts important ecological processes, then, an intervention ecology approach is required to restore function and stability to the system.

A well-known example of an invasive species that caused detrimental effects to an entire ecosystem, where the intervention ecology approach is now being applied, is the brown treesnake (Boiga irregularis) on the island of Guam. The snake was introduced to the island at the end of WWII, likely a stowaway aboard U.S. military cargo ships. Within approximately 40 years the snake had spread throughout the entire island and eliminated 9 of the 11 species of native forest birds[13][14]. While the brown treesnake may be the most infamous, other introduced species also have detrimental effects on Guam’s ecosystems. Rats (Rattus sp.), feral pigs (Sus scrofa), and Philippine deer (Rusa mariannae) are well-established and numerous arthropod pests, including the little fire ant and coconut rhinoceros beetle are taking a noticeable toll on local species.

Identifying the Impacts of Non-native Species on the Ecosystem

When a species has been identified in an ecosystem, it is essential to determine how it has impacted the stability, composition, and diversity of the ecosystem. This may be done by comparing changes over time, if data exist from prior to the invasion, or comparing across space if comparable areas exist nearby. Experiments that compare areas where the invasive is excluded to areas where it is present (aka ‘exclosure experiments’) may also shed light on how the system would operate in the absence of the invader.  

Invasive species may cause the decline or extirpation of native species that provide essential ecological functions in the ecosystem. For example, the Hemlock Woolly Adelgid (Adelges tsugae), an invasive insect from Asia, has led to the destruction of up to 80% of the hemlock trees in the Eastern United States, which then impacted overall forest composition. In Florida, the burmese python (Python molurus) became a destructive invasive species in less than 20 years by causing severe declines in mammal populations through predation[15].

Invasive species also cause problems for human health and economies. They can be disease vectors, such as the Asian tiger mosquito (Aedes albopictus), which can transmit Dengue Fever and Chikungunya. Invasive species can impact local and even large economies[16][17]. Brown treesnakes on Guam climb onto powerlines or into transistor stations, and are linked to nearly 200 power outages per year costing approximately $4.5 million[18]. Species may also impact economically important animals and plants[17].

The nearby islands of Saipan, Rota, and Tinian, together with Guam, comprise the inhabited southern islands of the Mariana Island archipelago. Saipan, Tinian, and Rota have flora and fauna similar to Guam but do not have the invasive snake. Comparing Guam, Saipan, Rota, and Tinian offers a unique accidental experiment to test the effects of an invasive predator and its cascading effects on a forest system, particularly through the loss of native forest birds and their accompanying ecological roles. We use this as an example for designing restoration approaches to restore function to a system with an intractable invasive species problem.

It took several decades after the introduction of the brown treesnake to Guam for it to be identified as the culprit behind bird declines, and even longer to identify the cascading ecological effects of bird loss. Because the islands to the north of Guam have similar forests but still retain their bird populations, it was possible to set up comparative studies to determine impacts. Since 5 of the bird species were frugivores, the loss of seed dispersal stands out as a major impact on the forests of Guam[19]. With reduced seed dispersal, seeds fall underneath their parent tree unhandled by frugivores, which results in a lower chance of germination[2]. In addition, treefall gaps are filled almost exclusively by the trees adjacent to the gap, which has led to reduced species richness in treefall gap seedling communities[20]. In addition, spiders are more numerous in Guam compared to the other islands, presumably due to a lack of vertebrate predators[21]. The full impact of the snake is still being uncovered.

Preventing Further Degradation by Managing the Invasive Species

Once a species has been identified as being invasive in an ecosystem, it is essential to act as quickly as possible in order to prevent further impacts. In some systems, eradication may be impossible, in which case control methods should aim at containing the population. This step is challenging and calls for the cooperation of many actors such as scientists, policy holders and funding agencies to identify methods to control the invasive species across the landscape.

Many tools exist and are being developed to manage invasive species[22], but the specific tools to use depend on the species and habitat. Mechanical control methods, such as hunting and invasive plant removal, are manually intensive and can be costly if an invasive species has reached high densities. Chemical control methods such as application of herbicides and pesticides have proven effective but are often costly and may be socially unpalatable[17].

Sterilization and gene drive techniques are being developed for use in invasive species control. Sterilization involves sterilizing either males or females of a species and releasing those sterilized individuals into a population where they are mating but not physically able to produce offspring. Sterilization has been used successfully to suppress fruit fly populations[23] and has shown some success in pilot studies targeting mosquitoes[24]. Gene drive approaches manipulate a genome to increase the likelihood specific alleles will be inherited[25]. Gene drive control methods are being pursued for rats and some other invasive species[26][27], but remain controversial because of uncertainty of its safety and fears that effects may reach beyond target populations[28].  

In the case of invasive brown treesnakes on Guam, the snakes already occupied the majority of the island by the time management began, so management efforts were directed at control rather than eradication. The snake had spread throughout the entire island by the time it was linked to the loss of birds in the mid-1980’s. Dr. Julie Savidge ruled out other suspected agents such as disease and pathogens, and temporally and geographically aligned the spread of the snake with the disappearance of birds across the island[13], making a convincing case that the snake was the culprit. However, she still faced difficulties convincing others that a single species of introduced snake was responsible for the alarming disappearance of native birds, so control of the snake didn’t start occurring until 1993. The goal of control has largely been to keep the snakes from establishing on other islands, such as Hawaii. Initial control methods implemented included snake trapping, visual searching, and detector dogs to inspect cargo and planes leaving the island, and concrete barriers to quarantine cargo originating from Guam on snake-free islands[29]. Recently a chemical control method has been developed. This method consists of dropping dead mice with an attached acetaminophen tablet (a toxin for brown treesnakes) from helicopters to the forest canopy where snakes will encounter and consume them. These “mouse-drops” need to occur at regular intervals over a prolonged period to ensure all snakes in an area will be affected[30]. Areas may be enclosed with snake barriers in order to prevent incursion and reach eradication. The barriers erected for this purpose in Guam also serve as effective exclosures for invasive deer and pigs. Researchers are also trying to predict indirect effects of invasive control that may require further management, such as increases in invasive small mammals with the eradication of snakes or increases in weedy plant species with the eradication of ungulates.

Restoring Degraded Ecological Functions in the Ecosystem  

Figure 2. Conceptual framework for restoring ecological functions in an ecosystem. First, it is essential to identify the ecological services that need to be restored and the species that may be able to provide those services. The next step is to conduct a landscape-level evaluation of the potential spatial distribution of both the service and its provider. Then, both should be combined to identify optimal rewilding areas. Finally, societal constraints should be taken into account to develop effective management strategies and policies.

In an ideal situation, the invasive species would be eradicated, and then native species restored across the landscape, in turn restoring ecological function. However, complete eradication is often impossible. Instead, invasive population reduction or local eradication combined with restoration of native species or surrogate species within protected areas may be possible. In this section, we describe a proposed conceptual framework (Figure 2) to use when planning invasive control and rewilding scenarios for the purposes of restoring ecological functions.

Identifying the Key Ecosystem Function Providers

The degradation of an ecosystem is often caused by the extirpation of ecological functions provided by keystone or foundational species. If these functionally important species are not entirely extirpated from the system, the first step is to identify strategies for increasing the population, via conserving or enhancing essential habitats for these species and controlling the invasive species. In an ideal situation, one would be able to conduct an ecological function analysis to assess the abundance of the species required to provide sufficient ecological function[31]. On the other hand, if these species are already extinct from the ecosystem, then rewilding will be necessary to restore the extirpated ecological functions. Rewilding can be defined as introducing locally extinct or ecologically similar species to perform ecosystem functions analogous to those of extinct species[32][33][34] . In some cases, the species that has been extirpated can be found in ther systems. This is the most favorable case, with the possibility of translocating populations back into the ecosystem from these other sources. In other cases, if the species is globally extinct, rewilding can be done by selecting a species that can perform the same ecological function. This requires a great deal of caution, however, since predicting the extent of possible impacts on an ecosystem is very difficult. Many case studies have underlined the risks of such an approach[34].

Figure 3. Seed dispersal kernels of five avian seed dispersers and 15 tree species on Saipan. Each panel represents a modelled species-specific interaction. For each interaction, we show standard dispersal curves, median and 99th percentile dispersal distances (numbers in top right of panel), and probability of seed dispersal greater than 500 m (filled dots represent probabilities greater than 0 and hollow dots represent probability = 0). The final column represents potential seed dispersal in two dimensions for bird species dispersing that given plant species (Rehm et al.,2019).

The first step towards restoring a functional ecosystem in Guam was to identify frugivorous species that were effective seed dispersers[35] . Nearby islands to Guam were unaffected by the brown treesnake and host avian communities similar to those historically present in Guam. This allowed us to prioritize reintroducing native species over introducing non-native species to Guam, and to assess which native frugivores were the most effective dispersers. We conducted studies to evaluate the effect of gut passage on germination of native forest tree species, and to study the movement of the candidate avian frugivore species (Figure 3)[36]. The Micronesian Starling was identified as an ideal candidate for rewilding because of its extensive diet, probability of dispersing seeds a long distance, and propensity for crossing from native to degraded forest, and thus assisting with forest regeneration[35]. Other strong candidates for rewilding are the Mariana Fruit Dove (Ptilinopus roseicapilla) and the Mariana Fruit Bat (Pteropus mariannus), because they also disperse many tree species. Furthermore, Micronesian Starlings and Mariana Fruit Bats are still present in small populations on the island of Guam, even in the presence of the brown treesnake. Restoration of seed dispersal can be accomplished through a combination of increasing the population and extending the range of the two extant species and rewilding the extirpated species[2][20][37].

Identifying Key Areas in Need of Restoration

Restoration projects, and thus rewilding scenarios, are often limited in terms of financial resources. Future funding often relies on successful rewilding efforts, so projects should attempt to maximize success. To do so, rewilding should be spatially optimized to aim at restoring functions at key locations within the landscape. Misplacing rewilded species within the landscape can not only potentially lead to insufficient ecological function benefits but could also lead to negative ecological effects.  For example, pollinators and seed dispersers may pollinate or disperse non-native plants, exacerbating the ecological problems.  Thus, it is essential to understand the spatial pattern of lost ecological function, along with the habitat and desired and undesired effects of the rewilded species.

Figure 4. Visual representation of scores assigned to different areas (here cells) of a landscape with (a) a service score representing areas that should be prioritized for functional restoration and (b) a reintroduction score for areas where rewilding would maximize functional restoration. Colors represent landcover types.

In the case of Guam, an important goal is to reintroduce seed dispersal of native plant species across the island. Therefore, our first decision was that native forest should be prioritized since it provides the source of native seeds. We first focused on the dispersal behavior and the seed gut passage time of the one remaining native avian frugivore species– Micronesian starlings (Aplonis opaca). Some of the important criteria that were taken into account were:

  • Landcover type: represents different levels of forest degradation. Some landcover types were considered too degraded to benefit from seed dispersal.
  • Distance to native forest and density of surrounding native forest: represents the probability of starlings efficiently dispersing native seeds into the focal area.

Using this information, we identified areas across the island where the restoration of seed dispersal should be prioritized (Figure 4a)[3].

Identifying Potential Habitats for The Function Providers

In combination to the previously identified areas of interest for restoring ecological function, it is necessary to identify all potential areas that could successfully host the reintroduction of the desired service providers[38]. Thus, habitat suitability should be mapped across the studied ecosystem. Habitat models allow evaluating the quality of habitat for a species within the studied landscape. These models can take into account a wide variety of parameters such as landcover, elevation, water availability, tolerance to disturbed habitats, and climate. Published methodologies are available as guidance to conceptualize a habitat suitability index that fits the biology of a wide range of function providers[39][40][41].

In a Guam case study, we mapped habitat suitability as a binary function of either “suitable” or “non-suitable” for each potential service provider. This was done essentially by using landcover maps and assessing the different types of resource and habitats potentially used by the studied species within a virtual homerange. For example, habitat suitability for starlings, a generalist species, was defined by landcover types and the amount of native forest (food resource) present around the evaluated area.

Identifying the Optimal Areas for Rewilding to Maximize the Restoration of Ecological Functions

Steps described in Sections 4.2 and 4.3 produce two maps: one identifies the areas that could host the service provider and the other shows where the function is most needed in our landscape. Planners can then overlay both maps and use this to estimate where rewilding would bring maximal functional restorations. To do so, scores can be assigned to each area (Figure 4b), based on the how much areas in need of functional restoration would be potentially impacted by rewilding.

In the Guam example (Figure 4), a score was assigned to each spatial entity that could host starlings, by drawing their potential home range if they inhabited each cell, then assigning a score based on the proportion of their home range that contained areas needing the ecological function, as identified in Section 4.1.

Linking Ecology to Decision-Making to Efficiently Restore Ecological Function Across an Area

When it comes to resource management or conservation projects, many entities and stakeholders are involved at a wide variety of scales. Scientists and managers may be able to identify spatial areas where rewilding would optimally restore ecological function, but the ecological optimum may not be feasible for financial, logistical, social, or political reasons. This leads to the emergence of social-ecological systems that each follow their own specific set of rules[42][43][44]. Having so many different actors and interactions can lead to many difficulties when identifying efficient management decisions[45][46][47].

To encapsulate some of these difficulties, aggregating individual ecological spatial units into more social entities should be considered to facilitate decision-making. Thus, management units, or clusters of previously identified small areas of interest that share common characteristics, should be identified based on all of the parameters that could influence management decisions. Typical examples of factors of importance to consider that can influence a management strategy applied to that area:

  • Land ownership
  • Accessibility
  • Land cover
  • Topography
  • Budget

For example, land ownership might exclude any type of intervention on private land. Thus, all inaccessible areas should be excluded from the model. Topography might render specific management methods useless and thus reduce the amount of possibilities. This should be taken into account and management units should be separated into different categories based on topography. Each of these factors will be taken into account to identify management unit types, each requiring a unique management approach. Once the social and geographic factors are taken into consideration, and managers decide which management types are relevant for the area, then the individual ecological areas identified in Section 4.4 should be aggregated into management units. Scoring these spatial entities is also recommended, by using the scores of all the smaller areas of interests, in order to be able to rank the management units by order of priority.

Figure 5. Map of the management units identified throughout the island of Guam when considering (a) both management unit types together and (b) Forest and non-forest management units separately. Management units are then ranked by management score and put into the following categories: Best (Top 10% of total area assigned to management units), Great (10-25%), Good (25-50%), Average (50-75%), and Poor (75-100%).

In Guam, management units have been identified based on the methods that will be used to control the brown tree snake (Figure 5). Several management methods are possible, ranging from traps to the aerial distribution of toxicant drops across large areas. These methods are detailed in Section 3. The main method considered for the control of brown tree snake throughout the island is the aerial distribution of toxicant drops. This method may be socially unacceptable to carry out in or near urban habitats, thus land cover (urban) is one of the main drivers that defines which management approach will be considered for rewilding. The current restoration projects are led by the Department of Defense and thus will be conducted on military-owned land. Finally, fencing can be used as a method of regulation of snake population, in combination with other methods, but can be extremely costly. Topography, and especially steep cliff lines can act as potential natural barriers, reduce fencing cost, and thus should be considered when designing management units.

Another step to consider is the importance of listening to local actors and involving communities[48][49][50]. Local expertise is an invaluable resource, and their involvement increases the chance of success for any project. Frame et al. (2004)[50] illustrates a detailed example of how collaborative planning of land-use in British Columbia has led to resolving environmental conflict and produced significant additional benefits such as improved stakeholder relations, skills, and knowledge. Many tools, ranging from surveys to participatory board games, are available to decision-makers and land managers to involve community members and obtain feedback[51][52][53].

Results from recent small group discussions on Guam suggested that some Guam residents had doubts about the extent of the impact of brown treesnakes, confusion about the effectiveness of current management actions, and distrust of certain entities carrying out research and management[54]. Given this disconnect between conservation managers and members of the public, we decided to test a participatory approach with multiple stakeholders. Surveys were distributed that presented a wide range of charismatic species, asking people to identify they deemed important as a conservation priority. Participants could delve further into management scenarios with a board game that focused on sequentially developing conservation towards achieving participants’ vision of the Guam in ten years.

Long-term Monitoring

Finally, once areas have been chosen for rewilding, strategies have been applied, and species have been brought within the ecosystem, it is essential to keep monitoring long-term progress. Eradication and rewilding projects can appear to be successful at first but fail in the long term because of a lack of effective monitoring and adaptive management. Re-invasion can happen, with impacts on rewilded species and further degradation of the system. The consequences of failed eradications or rewilding projects can extend beyond just the species within an ecosystem – public support, future funding, and trust in managers and researchers can be adversely impacted as well.

Summary

Restoration of ecological function in terrestrial systems impacted by invasive species is a multi-step process. After identifying an invasive species that is affecting ecological function, the following steps include managing the invasive to prevent further degradation, identifying which ecological functions have been disrupted, identifying the role native and non-native species could play in restoring ecological function, and managing the invasive to the extent that species can be restored that provide the missing ecological function. Finally, long-term monitoring and adaptive management is necessary to prevent re-invasion and further degradation.

References

  1. ^ 1.0 1.1 1.2 Hobbs, R.J., Hallett, L.M., Ehrlich, P.R., and Mooney, H.A., 2011. Intervention Ecology: Applying Ecological Science in The Twenty-first Century. BioScience, 61(6), pp. 442–450. doi: 10.1525/bio.2011.61.6.6 Article pdf
  2. ^ 2.0 2.1 2.2 Rogers, H.S., Buhle, E.R., HilleRisLambers, J., Fricke, E.C., Miller, R.H., and Tewksbury, J.J., 2017. Effects of an invasive predator cascade to plants via mutualism disruption. Nature Communications, 8:14557. doi: 10.1038/ncomms14557 Article pdf
  3. ^ 3.0 3.1 Thierry, H., and Rogers, H., 2020. Where to rewild? A conceptual framework to spatially optimize ecological function. Proceedings of the Royal Society B: Biological Sciences, 287:20193017. doi: 10.1098/rspb.2019.3017 [[Media:Thierry2020.pdf | Article pdf]]
  4. ^ Williamson, M., and Fitter, A.,1996. The varying success of invaders. Ecology, 77(6), pp. 1661–1666.| doi:10.2307/2265769
  5. ^ Blackburn, T.M., Pyšek, P., Bacher, S., Carlton, J.T., Duncan, R.P., Jarošík, V., Wilson, J.R., and Richardson, D.M., 2011. A proposed unified framework for biological invasions. Trends in Ecology & Evolution, 26(7), pp. 333–339. doi: 10.1016/j.tree.2011.03.023
  6. ^ Kraus, F., 2008. Alien Reptiles and Amphibians: A Scientific Compendium and Analysis. Springer, Dordrecht, Netherlands. ISBN: 978-1-4020-8945-9/eISBN: 978-1-4020-8946-6 doi:10.1007/978-1-4020-8946-6
  7. ^ Kraus, F., 2015. Impacts from Invasive Reptiles and Amphibians. Annual Review of Ecology, Evolution, and Systematics, 46(1), pp. 75–97. doi:10.1146/annurev-ecolsys-112414-054450
  8. ^ Colautti, R.I., and MacIsaac, H.J., 2004. A neutral terminology to define ‘invasive’species. Diversity and Distributions, 10(2), pp. 135–141. doi:10.1111/j.1366-9516.2004.00061.x Article pdf
  9. ^ Richardson, D.M., Pyšek, P., Rejmánek, M., Barbour, M.G., Panetta, F.D., and West, C.J., 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions, 6(2), pp. 93–107. doi: 10.1046/j.1472-4642.2000.00083.x Article pdf
  10. ^ McNeely, J.A., 2000. The future of alien invasive species: changing social views. In: H.A. Mooney and R.J. Hobbs (eds), Invasive Species in a Changing World. Island Press, Washington, DC, pp. 171–190. ISBN: 978-1559637824.
  11. ^ Simberloff, D., Martin, J.-L., Genovesi, P., Maris, V., Wardle, D.A., Aronson, J., Courchamp, F., Galil, B., García-Berthou, E., Pascal, M., Pyšek, P., Sousa, R., Tabacchi, E., and Vilà, M., 2013. Impacts of biological invasions: what’s what and the way forward. Trends in Ecology & Evolution, 28(1), pp. 58–66. doi: 10.1016/j.tree.2012.07.013
  12. ^ Marris, E. (2011). Rambunctious Garden: Saving Nature in a Post-wild World. Bloomsbury, New York. ISBN: 978-1-6081-9454-4/eISBN: 978-1-6081-9455-1
  13. ^ 13.0 13.1 Savidge, J.A., 1987. Extinction of an Island Forest Avifauna by an Introduced Snake. Ecology 68(3), pp. 660–668. doi: 10.2307/1938471
  14. ^ Wiles, G.J., Bart, J., Beck, R.E., and Aguon, C.F., 2003. Impacts of the Brown Tree Snake: Patterns of Decline and Species Persistence in Guam’s Avifauna. Conservation Biology, 17(5), pp. 1350–1360. doi: 10.1046/j.1523-1739.2003.01526.x
  15. ^ Hoyer, I.J., Blosser, E.M., Acevedo, C., Thompson, A.C., Reeves, L.E., and Burkett-Cadena, N.D., 2017. Mammal decline, linked to invasive Burmese python, shifts host use of vector mosquito towards reservoir hosts of a zoonotic disease. Biology Letters, 13(10):20170353.doi: 10.1098/rsbl.2017.0353 Article pdf
  16. ^ Crowl, T.A., Crist, T.O., Parmenter, R.R., Belovsky, G., and Lugo, A.E., 2008. The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment, 6(5), pp. 238–246. doi: 10.1890/070151 Article pdf
  17. ^ 17.0 17.1 17.2 Pimentel, D., Zuniga, R., and Morrison, D., 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52(3), pp. 273–288. doi: 10.1016/j.ecolecon.2004.10.002
  18. ^ Fritts, T.H. (2002). Economic costs of electrical system instability and power outages caused by snakes on the island of Guam. International Biodeterioration & Biodegradation, 49(2-3), pp. 93–100. doi: 10.1016/S0964-8305(01)00108-1
  19. ^ Caves, E.M., Jennings, S.B., HilleRisLambers, J., Tewksbury, J.J., and Rogers, H.S., 2013. Natural Experiment Demonstrates That Bird Loss Leads to Cessation of Dispersal of Native Seeds from Intact to Degraded Forests. PLoS One, 8(5), e65618. doi: 10.1371/journal.pone.0065618 Article pdf
  20. ^ 20.0 20.1 Wandrag, E.M., Dunham, A.E., Duncan, R.P., and Rogers, H.S., 2017. Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings. Proceedings of the National Academy of Sciences 114(40), pp. 10689–10694. doi: 10.1073/pnas.1709584114 Article pdf
  21. ^ Rogers, H., Lambers, J.H.R., Miller, R., and Tewksbury, J.J., 2012. ‘Natural Experiment’ Demonstrates Top-Down Control of Spiders by Birds on a Landscape Level. PLoS One, 7(9):e43446. doi: 10.1371/journal.pone.0043446 Article pdf
  22. ^ Wittenberg, R., and Cock, M.J., 2001. Invasive alien species: a toolkit of best prevention and management practices. CAB International, Wallingford, Oxon, UK. ISBN: 0 85199 569 1 doi: 10.1079/9780851995694.0000
  23. ^ Zacharopoulou, A., Augustinos, A.A., Drosopoulou, E., Tsoumani, K.T., Gariou‐Papalexiou, A., Franz, G., Mathiopoulos, K.D., Bourtzis, K., and Mavragani‐Tsipidou, P.,2017. A review of more than 30 years of cytogenetic studies of T ephritidae in support of sterile insect technique and global trade. Entomologia Experimentalis et Applicata, 164(3), pp. 204–225. doi: 10.1111/eea.12616 Article pdf
  24. ^ Lees, R.S., Gilles, J.R., Hendrichs, J., Vreysen, M.J., and Bourtzis, K., 2015. Back to the future: the sterile insect technique against mosquito disease vectors. Current Opinion in Insect Science, 10, pp.156–162. doi: 10.1016/j.cois.2015.05.011 Article pdf
  25. ^ Champer, J., Buchman, A., and Akbari, O.S., 2016. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nature Reviews Genetics, 17, pp. 146-159. doi: 10.1038/nrg.2015.34 Article pdf
  26. ^ Harvey-Samuel, T., Ant, T., and Alphey, L., 2017. Towards the genetic control of invasive species. Biological Invasions, 19, pp. 1683–1703. doi: 10.1007/s10530-017-1384-6 [[Media:Harvey2017.pdf | Article pdf]
  27. ^ Leitschuh, C.M., Kanavy, D., Backus, G.A., Valdez, R.X., Serr, M., Pitts, E.A., Threadgill, D., and Godwin, J., 2018. Developing gene drive technologies to eradicate invasive rodents from islands. Journal of Responsible Innovation, 5(S1), pp. S121–S138. doi: 10.1080/23299460.2017.1365232 Article pdf
  28. ^ Esvelt, K.M., and Gemmell, N.J., 2017. Conservation demands safe gene drive. PLoS Biology, 15(11), e2003850. doi: 10.1371/journal.pbio.2003850 Article pdf
  29. ^ Clark, C., Clark, L., and Siers, S., 2018. Brown Tree Snakes: Methods and Approaches for Control. In: W.C. Pitt, J.C. Beasley, and G.W Witmer (eds), Ecology and Management of terrestrial vertebrate invasive species in the United States. CRC Press, Boca Raton, FL. pp. 107–134. eISBN: 978-1-3151-5707-8 doi: 10.1201/9781315157078 Chapter pdf
  30. ^ Siers, S.R., Barnhart, P.D., Shiels, A.B., Rabon, J.A., Volsteadt, R.M., Chlarson, F.M., Larimer, J.R., Dixon, J.C., and Gosnell, R.J., 2018. Monitoring Brown Treesnake Activity Before and After an Automated Aerial Toxicant Treatment. Final Report QA-2621. USDA, APHIS, WS, NWRC. Hilo, HI. Report pdf
  31. ^ Brodie, J.F., Redford K. H., and Doak, D.F., 2018. Ecological Function Analysis: Incorporating Species Roles into Conservation. Trends in Ecology and Evolution, 33(11), pp.840–850. doi: 10.1016/j.tree.2018.08.013 [[Media:Brodie2018.pdf | Article pdf]}
  32. ^ Seddon, P.J., Griffiths, C.J., Soorae, P.S., and Armstrong, D.P., 2014. Reversing defaunation: Restoring species in a changing world. Science, 345(6195), pp. 406–412. doi: 10.1126/science.1251818
  33. ^ Sobral-Souza, T., Lautenschlager, L., Morcatty, T.Q., Bello, C., Hansen, D., and Galetti, M., 2017. Rewilding defaunated Atlantic Forests with tortoises to restore lost seed dispersal functions. Perspectives in Ecology and Conservation, 15(4), pp. 300–307. doi: 10.1016/j.pecon.2017.08.005 Article pdf
  34. ^ 34.0 34.1 Svenning, J.-C., Pedersen, P.B., Donlan, C.J., Ejrnæs, R., Faurby, S., Galetti, M., Hansen, D.M., Sandel, B., Sandom, C.J., and Terborgh, J.W., 2016. Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research. Proceedings of the National Academy of Sciences, 113(4), pp. 898–906. doi: 10.1073/pnas.1502556112 Article pdf
  35. ^ 35.0 35.1 Rehm, E.M., Chojnacki, J., Rogers, H.S., and Savidge, J.A., 2018. Differences among avian frugivores in seed dispersal to degraded habitats. Restoration Ecology, 26(4), pp. 760–766. doi: 10.1111/rec.12623
  36. ^ Rehm, E., Fricke, E., Bender, J., Savidge, J., and Rogers, H., 2019. Animal movement drives variation in seed dispersal distance in a plant–animal network. Proceedings of the Royal Society B, 286(1894):20182007. doi: 10.1098/rspb.2018.2007 Article pdf
  37. ^ Wandrag, E.M., Dunham, A.E., Miller, R.H., and Rogers, H.S., 2015. Vertebrate seed dispersers maintain the composition of tropical forest seedbanks. AoB Plants, 7. doi: 10.1093/aobpla/plv130 Article pdf
  38. ^ Hirzel, A.H., and Le Lay, G., 2008. Habitat suitability modelling and niche theory. Journal of Applied Ecology, 45(5), pp. 1372–1381. doi: 10.1111/j.1365-2664.2008.01524.x [[Media:Hirzel2008.pdf | Article pdf]
  39. ^ Donovan, M.L., Rabe, D.L., and Olson, C.E., 1987. Use of Geographic Information Systems to Develop Habitat Suitability Models. Wildlife Society Bulletin, 15(4), pp. 574–579.
  40. ^ Rondinini, C., Di Marco, M., Chiozza, F., Santulli, G., Baisero, D., Visconti, P., Hoffmann, M., Schipper, J., Stuart, S.N., and Tognelli, M.F. (2011). Global habitat suitability models of terrestrial mammals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 366(1578), pp. 2633–2641. doi: 10.1098/rstb.2011.0113 Article pdf
  41. ^ Van Horne, B., and Wiens, J.A., 1991. Forest bird habitat suitability models and the development of general habitat models. Fish and Wildlife Research, 8. ADA322800 Report pdf
  42. ^ Folke, C., Hahn, T., Olsson, P., and Norberg, J., 2005. Adaptive Governance of Social-Ecological Systems. Annual Review of Environment and Resources, 30, pp. 441–473. doi: 10.1146/annurev.energy.30.050504.144511 Article pdf
  43. ^ Folke, C., 2006. Resilience: The emergence of a perspective for social–ecological systems analyses. Global Environmental Change, 16(3), pp. 253–267. doi: 10.1016/j.gloenvcha.2006.04.002 Article pdf
  44. ^ Walker, B., Holling, C.S., Carpenter, S.R., and Kinzig, A., 2004. Resilience, adaptability and transformability in social–ecological systems. Ecology and Society, 9(2):5. doi: 10.5751/ES-00650-090205 Article pdf
  45. ^ Adger, W.N., Brown, K., and Tompkins, E.L., 2005. The political economy of cross-scale networks in resource co-management. Ecology and Society, 10(2): 9. doi:10.5751/ES-01465-100209 Article pdf
  46. ^ Anderies, J.M., Walker, B.H., and Kinzig, A.P., 2006. Fifteen weddings and a funeral: case studies and resilience-based management. Ecology and Society, 11(1): 21. doi:10.5751/ES-01690-110121 Article pdf
  47. ^ Pahl-Wostl, C., Sendzimir, J., and Jeffrey, P., 2009. Resources Management in Transition. Ecology and Society, 14(1):46. doi: 10.5751/ES-02898-140146 Article pdf
  48. ^ Bryan, T.A., 2004. Tragedy Averted: The Promise of Collaboration. Society & Natural Resources, 17(10), pp. 881–896. doi: 10.1080/08941920490505284
  49. ^ Conley, A., and Moote, M.A., 2003. Evaluating Collaborative Natural Resource Management. Society &Natural Resources, 16(5), pp. 371–386. doi: 10.1080/08941920309181 Article pdf
  50. ^ 50.0 50.1 Frame, T.M., Gunton, T., and Day, J.C., 2004. The Role of Collaboration in Environmental Management: An Evaluation of Land And Resource Planning In British Columbia. Journal of Environmental Planning and Management, 47(1), pp. 59–82. doi: 10.1080/0964056042000189808 Article pdf
  51. ^ Brandt, E., 2006. Designing Exploratory Design Games: a framework for participation in participatory design? In: Proceedings of the Ninth Conference on Participatory Design: Expanding Boundaries in Design- Volume 1, PDC 2006, Trento, Italy, pp. 57–66. doi:10.1145/1147261.1147271 Article pdf
  52. ^ Mendoza, G.A., and Prabhu, R., 2006. Participatory modeling and analysis for sustainable forest management: Overview of soft system dynamics models and applications. Forest Policy and Economics, 9(2), pp. 179–196. doi: 10.1111/j.1468-2885.2003.tb00290.x
  53. ^ Morris, N., 2003. A Comparative Analysis of The Diffusion and Participatory Models in Development Communication. Communication Theory, 13(2), pp. 225–248. doi: 10.1016/j.forpol.2005.06.006
  54. ^ Wald, D.M., Nelson, K.A., Gawel, A.M., and Rogers, H.S., 2019. The role of trust in public attitudes toward invasive species management on Guam: A case study. Journal of Environmental Management, 229, pp. 133–144. doi: 10.1016/j.jenvman.2018.06.047

See Also

United States Department of Agriculture (USDA), National Invasive Species Information Center (NISIC)

Global Invasive Species Database