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Interdisciplinary Thinking and the Bionic Leaf: Ecological Restoration’s Newest Superheroes

By Leah Churchward

New tools and interdisciplinary approaches are required for conservation in today’s climate, in particular for ecological restoration. In our rapidly changing world, it is important to be able to recognize these new tools and approaches and support them so that they can be funded, developed, and implemented on a large scale. In the case of ecological restoration, this might mean taking a step back from nature reserves and other traditional management methods and focusing on a tool from another discipline. Ecological restoration has the potential to be much more than returning plants and animals to where we found them. The development of the bionic leaf is one example of a newer technology that was created from an interdisciplinary background of biology and chemistry. It has the potential to serve a major role in modern ecological restoration and to reduce the need for ecological restoration as a whole.

(Source: Harvard University)

The bionic leaf was developed by Pamela Silver, a professor of biochemistry at Harvard Medical School, and Daniel Nocera, a professor of energy (also at Harvard University). It is able to split water molecules from natural solar energy and to produce liquid fuels from hydrogen eating bacteria (1). The bacterium Ralstonia eutropha, in combination with the catalysts of the artificial leaf, is used as a hybrid inorganic-biological system. (2) This combination is able to drive an artificial photosynthetic process for carbon fixation into biomass and liquid fuels (2). This artificial photosynthesis transpires through the solar electricity from the photovoltaic panel which is enough to power the chemical process that splits water into hydrogen and oxygen. (7) The pre-starved microbes then feed on the hydrogen and convert CO2 in the air into alcohol fuels. (7)

Initially, the bionic leaf was created to make renewable energy accessible at a local scale for developing communities that are without an electricity grid (3). This new technology also has the potential to intake carbon dioxide from the atmosphere (mentioned above), reduce CO2 emissions and pollution, and provide cleaner fertiliser. In the current era of the Anthropocene, human practices and behaviours have had an impact on the entire planet. One of the most significant consequences is the unprecedented influx of CO2 in the atmosphere over the last century. This is taking its toll on ecosystems around the world and the unique flora and fauna that inhabit them. The field of ecological restoration is a result of the efforts to restore ecosystems negatively affected by anthropogenic activities.

(Source: Schroders)

A majority of the world’s population live in cities that are near biodiversity hotspots. There are 24 megacities (cities with 10 million inhabitants or more) located in lesser developed regions, with an additional 10 cities in developing nations projected to become megacities sometime between 2016 and 2030. (4) With over half of the world’s population living in cities, a great deal of power and fuel is required, and currently a majority of the world’s energy consumption is from fossil fuels. These same fossil fuels are responsible for the increased CO2 in the atmosphere. The first opportunity the bionic leaf brings for ecological restoration is by removing CO2 while performing artificial photosynthesis to begin to restore the atmosphere’s composition to pre-industrial times. (2) The second is by bringing clean and accessible fuel to developing communities, eliminating the need to build facilities such as mining operations, and reducing the need for ecological restoration to begin with. (6) This will create a diminishing reliance on fossil fuels and the land, air, and sea pollution that comes with their use. Besides pollution, climate change has affected the timing of reproduction in animals and plants, the migration of animals, the length of the growing season, species distributions and population sizes, and the frequency of disease and pest outbreaks. (5) It is projected to affect all aspects of biodiversity and therefore should be considered in restoration tactics. (5)

(Source: Harvard University)

The bionic leaf also has been transformed into a system that is able to make nitrogen fertiliser. When added to soil, a different engineered microbe can make fertiliser on demand. (6) Unlike most fertilisers used today in the agricultural industry, this one would not be synthesized from polluting resources. (7) Agricultural frontiers, or the outer regions of modern human settlements, are concentrated in diverse tropical habitats that are home to the largest number of species that are exposed to hazardous land management practices like pesticide use. (8) Because of their high biodiversity, these areas contain more sensitive, vulnerable and endemic species, and are areas expected to undergo the highest rate of species losses. (8) A lack of resources and education on proper pesticide usage has led to sharp deviations from agronomical recommendations with the overutilization of hazardous compounds. (8) Bringing the bionic leaf to these regions would mean cleaner fertiliser and the resources and education for proper pesticide usage. This would help mitigate the damage from improper use of hazardous pesticides as well as protect the biodiversity that was harmed by ingesting them.

Ecological restoration in a changing world calls for new tools and interdisciplinary approaches. When the field of conservation biology was officially established in 1985, the problems of global climate change were just beginning to be understood, as well as the effects on animal and plant species. Ecological restoration is an important section of the conservation biology field but the research and management strategies used going into the future should focus on having a more interdisciplinary approach. The bionic leaf is just one tool from collaborative thinking that can help restore biodiversity and habitats as well as clean up our atmosphere to reduce the need for major restoration projects in the future.

 

 

References
1. Peter Reuell. 2016. Bionic Leaf Turns Sunlight into Liquid Fuel. The Harvard Gazette. Accessed April 2018. https://news.harvard.edu/gazette/story/2016/06/bionic-leaf-turns-sunlight-into-liquid-fuel/
2. C. Liu, B.C. Colón, M. Ziesack, P.A. Silver, D.G. Nocera. Water Splitting-Biosynthetic System with CO2 Reduction Efficiencies Exceeding Photosynthesis. Science. Vol. 352. Issue 6290. 1210-1213. (2016). DOI: 10.1126/science.aaf5039
3. W.J. Sutherland, P. Barnard, S. Broad, M. Clout, B. Connor, I. M. Côté, L. V. Dicks, H. Doran, A. C. Entwistle, E. Fleishman, M. Fox, K. J. Gaston, D. W. Gibbons, Z. Jiang, B. Keim, F. A. Lickorish, P. Markillie, K. A. Monk, J. W. Pearce-Higgins, L. S. Peck, J. Pretty, M. D. Spalding, F. H. Tonneijck, B. C. Wintle, N. Ockendon, A 2017 Horizon Scan of Emerging Issues for Global Conservation and Biological Diversity, Trends in Ecology & Evolution, Vol. 32, Issue 1, Pages 31-40. (2017). https://doi.org/10.1016/j.tree.2016.11.005.
4. United Nations. 2016. The World’s Cities in 2016. Available from http://www.un.org/en/development/desa/population/publications/pdf/urbanization/the_worlds_cities_in_2016_data_booklet.pdf. (Accessed April 27, 2018)
5. Intergovernmental Panel on Climate Change. Climate Change and Biodiversity. Technical Paper V. 2002. http://ipcc.ch/pdf/technical-papers/climate-changes-biodiversity-en.pdf. (Accessed April 27, 2018)
6. Veronika Meduna. 2017. Bionic Leaf Might Power Earth. Stuff, New Zealand. https://www.stuff.co.nz/science/96110864/bionic-leaf-might-power-earth. (Accessed April 18, 2018).
7. David Biello. Bionic Leaf Makes Fuel From Sunlight, Water and Air. Scientific American. https://www.scientificamerican.com/article/bionic-leaf-makes-fuel-from-sunlight-water-and-air1/ (Accessed April 26, 2018).
8. L. Schiesari, A. Waichman, T. Brock, C. Adams, B. Grillitsch. Pesticide Use and Biodiversity Conservation in the Amazonian Agricultural Frontier. Philosophical Transactions of the Royal Society B: Biological Sciences. Vol. 368. (2013). DOI: 10.1098/rstb.2012.0378.

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How to apply conservation in a multicultural world – education and collaboration to provide unique solutions

Author: Finlay Morrison, Victoria University of Wellington

 

In our human dominated world if we are to help protect nature in the state we desire conservation is essential. Unfortunately, due to the wide-ranging impacts of climate change (Rosenzweig et al 2008, Hoegh-Guldberg and Bruno 2010, Chen et al 2011) and the cost of conservation (Moore et al 2004, Bode et al 2008) protection of everything is not possible. Conservation must be targeted where it is needed most, but it is a value judgement whether we conserve a species for its own sake or for human benefit. There also needs to be public education of the limitations of conservation in the face of climate change. This is where values and culture play a large role in the outcomes of conservation, with various cultures having different approaches and successes. Therefore, with an approach that considers each culture’s conservation values, there is potential to provide unique solutions within a shared view for conservation in a multicultural world.

 

With the rise in technology the world has become more connected than ever before, some countries and cities have become a mix of many different cultures (Vertovec 2007). This has brought about difficulties when it comes to conservation in these areas, because a conservation objective is subject to the judgement of the global community as well as the locals. Therefore, conservation has become a globally critiqued act with many differing views, and as such is difficult to implement without some form of backlash (Manfredo et al 2017).

 

Conservation is implemented based on the values of a cultural group, be it protection of ecosystem services, a certain species, or a habitat. When you have a multicultural group of people values will vary throughout the population, and differing values should be considered as much as possible before anything is carried out. But what can be done when cultures clash and there is no room for compromise? For example, when there are species or habitats desired by a minority cultural group their values can often be ignored by the bigger more powerful group (Carter 2010). However, a way to control conservation in these situations would be the use of laws that gives rights to the minority culture and allows for compromise.

 

Minority cultural groups have had a history of being displaced and their beliefs ignored in the name of conservation (Mombeshora and Le Bel 2009, Carter 2010), especially when their customs are traditional and not driven by western science and technology. However, sometimes these cultural groups live a life closer to the nature they conserve and possess a great knowledge of their local ecosystem (Turvey et al 2014, Nash et al 2016). There are examples where local and traditional ecological knowledge proved useful for historic species counts and distribution identification (Rasalato et al 2010, Ainsworth 2011). Therefore, locals could be left in conservation areas and seen as keepers of the land, and through cooperation multicultural conservation could be possible.

 

Much like the species of the world, cultures are only going to continue to change and mix. It would be best if this change was guided towards a cooperative approach to conservation. For this to happen it will be necessary to educate the public that the world is changing, and some conservation values will need to be sacrificed. Each cultural group’s conservation practices aren’t perfect, but they possess unique knowledge on various methods of conservation (Berkes et al 2000). So, although complex, a cooperative approach considering each cultural group’s conservation values will help reach a shared value outcome (Berkes 2009, Raymond et al 2010, Meeussen et al 2018).

 

In conclusion, it is evident that each cultural group has their own unique beliefs for conservation. Some people are unable to accept the limitations of conservation and do not consider differing cultural dependencies on nature. Therefore, public education on conservation in the current state of our world and fostering collaboration between cultures will help to provide a shared vision for conservation in a multicultural world.

 

References:

  • Ainsworth, C.H. (2011). Quantifying species abundance trends in the northern gulf of California using local ecological knowledge. Marine and Coastal Fisheries 3(1), 190-218
  • Berkes, F. (2009). Indigenous ways of knowing and the study of environmental change. Journal of the Royal Society of New Zealand 39(4), 151-156
  • Berkes, F. Colding, J. Folke, C. (2000). Rediscovery of traditional ecological knowledge as adaptive management. Ecological Applications 10(5), 1251-1262
  • Bode, M. Watson, J. Iwamura, T. Possingham, H.P. (2008). The cost of conservation. Science 321(5887), 340-340
  • Carter, J. (2010). Displacing indigenous cultural landscapes: the naturalistic gaze at Fraser Island World Heritage Area. Geographical Research 48(4), 398-410
  • Chen, I.C. Hill, J.K. Ohlemuller, R. Roy, D.B. Thomas, C.D. (2011). Rapid range shifts of species associated with high levels of climate warming. Science 333(6045), 1024-1026
  • Hoegh-Guldberg, O. and Bruno, J.F. (2010). The impact of climate change on the world’s marine ecosystems. Science 328(5985), 1523-1528
  • Manfredo, M.J. Teel, T.L. Sullivan, L. Dietsch, A.M. (2017). Values, trust, and cultural backlash in conservation governance: the case of wildlife management in the United States. Biological Conservation 214, 303-311
  • Meeussen, L. Agneessens, F. Delvaux, E. Phalet, K. (2018). Ethnic diversity and value sharing: a longitudinal social network perspective on interactive group processes. British Journal of Social Psychology 57(2), 428-447
  • Mombeshora, S. and Le Bel, S. (2009). Parks-people conflicts: the case of Gonarezhou National Park and the Chitsa community in south-east Zimbabwe. Biodiversity and Conservation 18(10), 2601-2623
  • Moore, J. Balmford, A. Allnutt, T. Burgess, N. (2004). Integrating costs into conservation planning across Africa. Biological Conservation 117(3), 343-350
  • Nash, H.C. Wong, M.H.G. Turvey, S.T. (2016). Using local ecological knowledge to determine status and threats of the critically endangered Chinese Pangolin (Manis pentadactyla) in Hainan, China. Biological Conservation 196, 189-195
  • Rasalato, E. Maginnity, V. Brunnschweiler, J.M. (2010). Using local ecological knowledge to identify shark river habitats in Fiji (South Pacific). Environmental Conservation 37(1), 90-97
  • Raymond, C.M. Fazey, I. Reed, M.S. Stringer, L.C. Robinson, G.M. Evely, A.C. (2010). Integrating local and scientific knowledge for environmental management. Journal of Environmental Management 91(8), 1766-1777
  • Rosenzweig, C. Karoly, D. Vicarelli, M. Neofotis, P. Wu, Q.G. Casassa, G. Menzel, A. Root, T.L. Estrella, N. Seguin, B. Tryjanowski, P. Liu, C.Z. Rawlins, S. Imeson, A. (2008). Attributing physical and biological impacts to anthropogenic climate change. Nature 453(7193), 353-U20
  • Turvey, S.T. Fernandez-Secades, C. Nunez-Mino, J.M. Hart, T. Martinez, P. Brocca, J.L. Young, R.P. (2014). Is local ecological knowledge a useful conservation tool for small mammals in a Caribbean multicultural landscape?. Biological Conservation 169, 189-197
  • Vertovec, S. (2007). Super-diversity and its implications. Ethnic and Racial Studies 30(6), 1024-1054

Should we pay to play? Charging for New Zealand’s landscape

Mt Taranaki – Harley Betts

By Daniel Papworth

New Zealand (NZ) has some of the most beautiful landscape in the entire world. However some areas are getting overrun by tourists. Over the past year 3.8 million people visited NZ’s shores[1]. Over half of them explored at least one national park or protected area[2].

NZ’s National parks system aims to preserve the country’s intrinsic worth for the enjoyment of the public. Park land contains “scenery of such distinctive quality, ecological systems, or natural features so beautiful, unique, or scientifically important that their preservation is in the national interest”[3]. The Department of Conservation (DOC) are charged with managing our parks, however they are seriously underfunded having around $20 a hectare of land they manage[4]. As a consequence from over use and lack of resources the beauty of these places may be at risk. Combined with climate change stress in these environments is mounting[5, 6]. Currently under the National Parks Act (1980) DOC is unable to charge for access. Regulation of the number of people visiting these area’s needs to be implemented to conserve them and their beauty.

Travelling abroad, you will almost always be charged to enter a national park. Chris Roberts, CEO of Tourism Aotearoa, says that only half a dozen sites in NZ are in serious need of number management[7]. Shouldn’t we then charge tourists to see these high use sites? Money spent on entry can be directed straight back into the maintenance of these tourist hotspots. The number of people visiting at one time can be monitored and regulated if needed. Another option is a ‘conservation tax’ or ‘nature levy’. When entering NZ international visitors could pay a small sum to be given to DOC for the upkeep of these high-use areas. If 3.8 million people visit a year and each is charged $20 that comes to seventy-six million dollars, nearly a quarter of DOC’s yearly budget. The total cost to visit NZ would then be $50, still cheaper than Australia’s $58-$85 border fee[8].

So why haven’t we used any of these methods yet? The problem is relatively new. Visitor numbers have increased from 2.6-3.8 million in the last five years[9]. In recent years DOC’s budget has reduced, making their job of maintaining these areas and conserving NZ’s endangered species all the more difficult. There is also likely hesitance to the investment for infrastructure. Buildings will need to be erected, people would have to be employed to process visitors. The difficulty of putting infrastructure in place could be avoided with the border tax option. However not every visitor is going to visit a national park, and some may visit multiple. Perhaps this information needs to be collected during the visa process. Or even just a free online booking system, purely for regulation purposes. Personally I feel that New Zealanders take great pride in their natural heritage. We have a certain expectation that these sort of things should free and easy to access. It feels less intrepid when you have to wait in a que to see it, less raw.

Over Easter weekend I had the pleasure of hiking the Northern Circuit in the central North Island. The locals say they cannot believe so many people still come to walk the Tongariro Alpine Crossing. Often commenting that so many come to do it they’re surprised everyone hasn’t already done it. That Easter Sunday over 3000 people walked the crossing. All those people winding their way up the mountain, using the toilets, wearing the track, stressing the fragile alpine environment[10]. Surely people will pay a small fee to experience these kind of areas. They didn’t pay to fly all the way around the globe to turn around at the gate because of a $10 entry fee. Visitors are great for the NZ economy, and these areas should be shared, but the need for number management is increasing.

So should we pay to play? Absolutely. More regulation is needed in these hot-spots for their longevity. Reducing the stress on these areas by having a charge is an opportunity we would be silly not to do. Let’s use tourism to help fund conservation. Let’s keep NZ beautiful.

 

References

  1. Statistics New Zealand (2018). Retrieved from https://www.stats.govt.nz/news/annual-visitor-arrivals-up-more-than-1-2-million-in-five-years
  2. Department of Conservation (2017). International Visitors Survey. Retrieved from http://www.doc.govt.nz/2017-annual-report-factsheets/?report=IVS_exp_by_NPk__2017_08_28_DOC_factsheet_template
  3. National Parks Act, No 66 (1980). Retrieved from http://www.legislation.govt.nz/act/public/1980/0066/latest/whole.html
  4. DOC is in desperate need of more funding (May 2017), Newshub. Retrieved from http://www.newshub.co.nz/home/new-zealand/2017/05/jesse-mulligan-doc-in-dire-need-of-more-funding.html
  5. Scott, D. (2003, April). Climate change and tourism in the mountain regions of North America. In 1st International Conference on Climate Change and Tourism (pp. 9-11).
  6. Moreno, A., & Becken, S. (2009). A climate change vulnerability assessment methodology for coastal tourism. Journal of Sustainable Tourism, 17(4), 473-488.
  7. Visitors will keep coming if national park fees introduced (February 2017), Newshub. Retrieved from http://www.newshub.co.nz/home/new-zealand/2017/02/visitors-will-keep-coming-if-national-parks-fees-introduced-industry.html
  8. New Zealand Green Party (2017). Tourism Levy Policy. Retrieved from https://www.greens.org.nz/policy/cleaner-environment/taonga-levy
  9. Statistics New Zealand (2018). Retrieved from https://www.stats.govt.nz/news/annual-visitor-arrivals-up-more-than-1-2-million-in-five-years
  10. Groot, R. (2003). The Tongariro National Park: Are We Loving it to Death? New Zealand Journal of Geography, 115(1), 1-13.

Ecological Disturbance – the intermediate hypothesis as a conservation tool in terrestrial ecosystems

By, Siosina Katoa

In the field of ecology, the concept of ecological disturbance has been debated whether it is acceptable to follow or just another theory that needs more evidence and more study. Paine (2012) defines this concept as an event, whether biological or non-biologically related, that help shapes the structure of an ecosystem or the population within (Paine, 2012). Few ecologists still argue that disturbance impacts ecosystem services and affects biodiversity especially in forests (Thom & Seid, 2015). Such includes the agricultural method of ‘slash-and-burn’ for shifting cultivation (Marks, et al., 2006). This eventually points out that disturbance then may hinder conservation management. However, others believe this is not true. Instead, they think disturbance enhances species diversity, habitat management and will allow species to adapt to change such as the fire-adapted systems. Indeed, ecological disturbance may then be a viable conservation tool.

The concept

The context of ecological disturbance, species diversity depends on the severity and intensity of disturbance. Connell describes this as a state of equilibrium at different succession stages of species abundance with regards to frequency of disturbance (Connell, 1978).

Figure 1 – the intermediate disturbance hypothesis (Hughes, 2010)

A range of hypotheses explains how ‘perturbation’ then affects species composition where it restores a disturbed community. In the popular intermediate disturbance hypothesis (Figure 1) also known as the non-equilibrium hypothesis explains species diversity is (a) low at low intensity of disturbance because of competition reducing diversity, (b) higher when disturbance is at an intermediate scale of frequency and (c) goes back to lower species diversity when the intensity of disturbance is high. This predicts then that in-between low and high disturbance; the intermediate intensity will maximize species diversity. This has been tested by various researchers in comparing the effects of disturbance to species diversity especially in terrestrial ecosystems (Hughes, 2010). Thus the said hypothesis proves that high diversity is sustained at a non-equilibrium state and that no or low disturbance will not

allow diversification of species.

Ecological Disturbance and conservation

The intermediate disturbance hypothesis allows regeneration of higher species diversity indicating ecological disturbance assist conservation.  A study on ecological effects of secondary roads on plant diversity concludes that further away from roadsides plant diversity decreases and alongside the road plants are abundant and growing in a fast rate (Fallahchai, et al., 2017). The establishment of a secondary road on the forest area promotes dispersal of seeds as well as other plant species by animals and stormwater runoff (Figure 2). It makes it easier by having the road diversify species rather than relying on pollinators and other occurrences. Herbivores find the road access easier to get to plants and disperse their seed. It helps increase speciation and diversity.

Figure 2 – Road establishment showing the effects on species distribution. Adapted from (Hughes, 2010)

Moreover, disturbance also assists in habitat management and maintaining the ecosystem’s holding capacity. An article on habitat management indicates disturbances interact in a complex manner with climate and soils to produce and maintain the diversity of species unique to that particular area (Marks, et al., 2006). It signifies that disturbances enhance resilience in the ecosystem through ecological succession. In a forest ecosystem, higher tree diversity provides forest resilience which allows the ecosystem to adapt to disturbance and change while still maintaining composition, the structure especially ecosystem functions and their niche (Miller, et al., 2018). Species can then co-evolve to increase diversity in a biological community such as forests and agricultural lands. This draws a result that a high diversity ecosystem is not maintained in a stable system but in a level of disturbances.

Way forward

Ecological disturbance is a viable conservation strategy but is still considered a hypothesis which is to be tested through further research and improved experiments. For example, examining the sizes and density of forest population may determine domination species as Connell (1978) suggested. Acknowledging the intermediate hypothesis along with better studies on how to manage disturbance is also critical to understand. Managers and conservationists should be aware of the state of the equilibrium of an ecosystem in order to maintain diversity. Diversity versus intensity of disturbances is the two considerable measures for effective management (Brawn, et al., 2001). Yet, it is still essential to appreciate the fact that ecological disturbance after all benefits conservation.

 

 

References

Brawn, J. D., Robinson, S. K. & Thompson III, F. R., 2001. The Role of Disturbances in the Ecology and Conservation of Birds. Annual Review of Ecology and Systematics, Volume 32, pp. 251-276.

Connell, J. H., 1978. Diversity in Tropical Rain Forests and Coral Reefs. Science, 199(4335), pp. 1302-1310.

Fallahchai, M. M., Haghverdi, K. & Mojaddamc, M. S., 2017. Ecological effects of forest roads on plant species diversity in Caspian forest of Iran. Acta Ecologica Sinica.

Hughes, R. A., 2010. Disturbance and Diversity: An Ecological Chicken and Egg Problem. Nature Education Knowledge, 3(10).

Marks, R. et al., 2006. Importance of Disturbance in Habitat Management. Washington DC: s.n.

Miller, K. M. et al., 2018. Eastern national parks protect greater tree species diversity than unprotected matrix forests. Forest Ecology and Management, pp. 74-84.

Paine, R. T., 2012. Ecological Disturbance – Ecology. [Online]
Available at: https://www.britannica.com/science/ecological-disturbance
[Accessed April 2018].

Thomas, C. D., 2017. Inheritors of the Earth: How Nature is Thriving in an Age of Extinction. New York: Public Affairs Hachette Book Group.

Thom, D. & Seid, R., 2015. Natural disturbance impacts on ecosystem services and biodiversity in temperate and boreal forests. Europe PMC Funders Group, pp. 760-781.


Teaching an Old Bird New Tricks: assisting the evolution of native species through selective breeding

Figure 1: A rat preying on a nesting bird 

By Rachel Selwyn

We’ve bred dogs to herd sheep, to point out hunting prey…can we breed NZ native species to fight back against introduced predators? Assisted evolution is a controversial conservation tactic but it’s not as far-fetched as you might think.

Native species on island ecosystems like in New Zealand have evolved for thousands of years without mammalian predators and without the appropriate predator avoidant behaviors1. The arrival of exotic predators like rats, stoats, and possums found the native species defenseless and had catastrophic effects on their populations2-4. In response, New Zealand has undertaken extensive eradication and predator control efforts which have helped species such as the North Island robin5-7.

Unfortunately, predator control has several flaws including the difficulty and high cost of achieving 100% eradication across the whole country8-9, the risk of unintended ecological effects10, questionable ethics11, and the never-ending battle against reintroductions12-13. Eradicating several species across an entire landmass is a massive undertaking especially given the difficulty monitoring international borders sufficiently to prevent reintroduction events. An alternative approach is to help native species adapt to the presence of new predators, through selective breeding, to create a sustainable coexistence of predator and prey.

The underlying issue in New Zealand is the prey naïveté, or lack of antipredator behavior, of native fauna that have not had the opportunity to adapt to the presence of these new predators14. Encouraging evolutionary adaptations to arise in the native fauna through selective breeding provides an alternative solution that does not involve large-scale extermination of an entire class of species.

Figure 2: A graphic depicting the process of selectively breeding a plant species for desired increased plant height.

Humans have used selective breeding for thousands of years, choosing desirable traits in agricultural plant species and domestic animals15. Selective breeding does not just apply to physical characteristics. Domesticated dogs are an example of using this technique to promote desirable behaviors such as pointing in hunting breeds and herding in sheepdogs16. Some conservationists are advocating for selective breeding to be similarly used for wild species to choose adaptive behaviors like predator avoidance to counteract prey naïveté17. Identifying individuals from a population that demonstrate the desired behavior or characteristic and selectively breeding them together increases the prominence of this trait in the population, as seen in Figure 2. Beneficial predator avoidant traits would ordinarily develop over time through natural selection, however, it can take a long time and high levels of predation often wipe out native populations before they have a chance to adapt18.  As humans are responsible for the dramatic scale of invasions around the world, it is our responsibility to help native species adapt to the changes we have provoked.

Some anti-predator traits have begun to arise in some New Zealand species although the frequency of these traits remains too low to effectively protect them. The New Zealand bellbird (Anthornis melanura) has begun decrease parental activity during nesting periods when predators are present in their habitat19. This behavior is believed to be adaptive as high parental activity at a nest can attract predators and lead to higher predation rates. Identifying adaptive behaviors like this would allow conservationists to deliberately breed the individual bellbirds showing this behavior and effectively speed up the process of natural selection.

Selective breeding to modify wild populations has been conducted in the past including with the plains zebra20 and with largemouth bass21. Selective breeding is currently being considered in marine conservation with species of corals and their symbionts. Researchers working to determine the genetic link within heat-tolerant corals hope to promote this trait in coral populations making them more resistant to climate change22-23.

How could we apply this to New Zealand? Kiwis couldn’t realistically be bred to fly away from predators without significantly altering them from a well-loved species. Species like the kiwi could be bred to encourage protective strategies that improve their ability to survive alongside novel predators. Captive breeding programs that are already in place, like those with the kakapo and takahe24, could be supplemented with selective breeding trials. Selective breeding would have to take place amongst all naïve prey simultaneously to avoid predators simply switching to easier less adapted prey25. Assisting evolution in New Zealand species would involve a widespread and costly effort over many years, however, this option provides a definite solution compared to the never-ending fight of eradication efforts. Critics are concerned that selective breeding for a single trait could lead to loss of genetic diversity within the population and magnification of harmful alleles26. While loss of genetic diversity is a risk with captive breeding, continually supplementing breeding efforts with individuals from the larger wild population will minimize this issue. Selective breeding may not succeed equally amongst all species so it is vital that trials are conducted in isolation with predator control maintained in wild populations.

Assisting evolution through selective breeding is a controversial and radical solution to prey naïveté that has the potential to replace predator eradication efforts. This should be conducted alongside predator control initially to provide time for adaptations to persist. There are several risks associated with this approach that merit further investigation, however, the benefit has more weight as successfully assisting native species to coexist alongside introduced predators would be a monumental conservation success. Current predator control efforts will need to continue forever to protect New Zealand’s native species, however, by selectively breeding naïve species to hold their own we can one day achieve ecosystems that can sustain themselves without human intervention.

 

Works cited:

  1. Bull, P.C., Whitaker, A.H. (1975). The amphibians, reptiles, birds and mammals. Biogeography and Ecology in New Zealand 231-276. Springer, Dordrecht.
  2. Remes, V., Matysiokova, B., Cockburn, A. (2012). Nest predation in New Zealand’s songbirds: Exotic predators, introduced prey and long-term changes in predation risk. Biological Conservation148(1):54-60.
  3. O’Donnell, C.F.J., Clapperton, B.K., Monks, J.M.(2015). Impacts of introduced mammalian predators on indigenous birds of freshwater wetlands in New Zealand. New Zealand Journal of Ecology 39(1):19-33
  4. O’Donnell, C.F.J., Weston, K.A., Monks, J.M. (2017). Impacts of introduced mammalian predators on New Zealand’s Alpine Flora. New Zealand Journal of Ecology 41(1):1-22
  5. Armstrong, D.P.(2016). Population responses of a native bird species to rat control. The Journal of Wildlife Management 81(2):342-346.
  6. Starling-Windhof, A., Massaro, M., Briskie, J. (2011). Differential effects of exotic predator-control on nest success of native and introduced birds in New Zealand. Biological Invasions 13(4):1021-1028
  7. Whitehead, A.L., Edge, K.A., Smart, A.F., Hill, G.S., Willans, M.J. (2008). Large scale predator control improves productivity of rare New Zealand riverine duck. Biological Conservation 141(11):2784-2794.
  8. Anderson, D.P., Gormley, A.M., Ramsey, D.S.L., Nugent, G., Martin, P.A.J., Bosson, M., Livingston, P., Byrom, A.E. (2017). Bio-economic optimisation of surveillance to confirm broadscale eradications of invasive pests and diseases. Biological Invasions 19(10):2869-2884.
  9. Harding, E.K., Doak, D.F., Albertson, J.D. (2002). Evaluating the effectiveness of predator control : the non-native red fox as a case study. Conservation Biology 15(4):1114-1122.
  10. Keller Kopf, R., Nimmo, D.G., Humphries, P., Baumgartner, L.J., Bode, M., Bond, N.R., Byrom, A.E., Cucherousset, J., Keller, R.P., King, A.J., McGinness, H.M., Moyle, P.B., Olden, J.D. (2017). Confronting the risks of large-scale invasive species control. Nature Ecology & Evolution 1
  11. Souther, C.E.(2016). The Cruel Culture of Conservation Country: Non-Native Animals and the Consequences of Predator-Free New Zealand. Transnational Law & Contemporary Problems 26(1):63-119.
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  13. King, C.M., McDonald, R.M., Martin, R.D., Dennis, T.(2009). Why is eradication of invasive mustelids so difficult? Biological Conservation 142(4):806-816.
  14. Sih, A., Bolnick, D.I., Luttbeg, B., Orrock, J.L., Peacor, S.D., Pintor, L.M., Preisser, E., Rehage, J.S., Vonesh, J.R. (2010). Predator-prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610-621.
  15. Akey, J.M., Ruhe, A.L., Akey, D.T., Wong, A.K., Connelly, C.F., Madeoy, J., Nicholas, T.J., Neff, M.W. (2010). Tracking footprints of artificial selection in the dog genome. PNAS 107(3):1160-1165.
  16. Akaad, D.A., Gerding, W.M., Gasser, R.B., Epplen, J.T. (2015). Homozygosity mapping and sequencing identify two genes that might contribute to pointing behavior in hunting dogs. Canine Genetics and Epidemiology 2:5.
  17. Moseby, K.E., Blumstein, D.T., Letnic, M. (2015). Harnessing natural selection to tackle the problem of prey naïveté. Evolutionary Applications 9(2):334-343.
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Images:

Image 1: https://thespinoff.co.nz/science/06-05-2017/what-if-the-predator-free-2050-plan-is-actually-a-terrible-idea/

Image 2: https://www.yourgenome.org/facts/what-is-selective-breeding

 

 


Testing the Waters. How coral reef restoration can address drivers of marine biodiversity loss.

By: Gliselle Marin

Introduction

The natural and anthropogenic drivers of habitat degradation have resulted in global biodiversity loss that continues at an accelerated rate. In addition to conservation and ecological mitigation strategies, a new scientific discipline has resulted from human efforts to reverse the deterioration of habitats and preserve biodiversity. Ecological restoration is the process of assisting the recovery of an ecosystem that has been degraded, damaged of destroyed (SER, 2004). Habitat restoration was originally developed for terrestrial ecosystems, and has since succeeded in creating new habitats for biodiversity (Hobbs and Norton, 1996; Dobson et al., 1997). Such success in marine ecosystems has not yet been seen, particularly in coral reefs where restoration efforts through artificial reefs and coral transplantation have had debatable effectiveness (Edwards and Clark, 1998).

The broader, more flexible concept of intervention ecology has been proposed for application on coral reefs, by managing for future change with historical guidelines to maintain the goods and services provided by the ecosystem (Hobbs et al., 2011). Where a historical ecosystem state is not attainable, a hybrid or novel ecosystem may be used for new restoration goals (Hobbs et al., 2009). This is the case for many coral reef ecosystems where anthropogenic disturbances have changed species compositions through the loss of biodiversity, and have resulted in an alternative state ecosystem dominated by new organisms (Graham et al., 2003). Coral reef restoration methods like artificial reefs and transplantation are now being used to provide increased connectivity and resilience by enhancing rates of recovery and adaptation of corals (van Oppen et al., 2015).

Coral Transplantation

Figure 1. Coral Transplantation in the Phillipines

Coral reefs and seagrass are among the most expensive ecosystems to restore (Bayraktarov, 2016). This may be due to high levels of mortality experienced in restoration strategies such as coral transplantation. Coral transplantation involves harvesting coral fragments (either from damaged coral with pieces broken off by disturbance, or selective harvesting), and cultivating these in coral nurseries (Abelson, 2006). The corals are later attached to a substrate and transplanted to a new, degraded site and left to grow naturally. Potential drawbacks associated with coral transplantation include: loss of colonies from donor areas; high mortality rates of transplanted corals; reduced growth rates of transplanted corals; failure of attachment of transplants, loss due to wave action; and reduced fecundity of transplants due to stress (Abelson, 2006). With all these factors limiting its success, the most notable appeal of transplantation seems to be its fast and prominent achievement in switching a bare reef into a live, “recovered” reef (Abelson. 2006). However, critical examination of transplantation as a restoration approach has concluded that where a degraded area receives enough recruits naturally, coral transplantation should be the last resort (Edwards and Clark, 1998). With the slow recruitment, high mortality rates, and often damaging harvesting strategies in coral transplantation, new methods for improvement are now being researched. Some of this has come from the idea of applying silviculture restorations strategies to coral restoration methods. Because of the biological structural and functional similarities between trees and corals, coral mariculture and gardening have been proposed as a potential sustainable practice for coral reef restoration (Epstein et al., 2003). This involves the establishment of coral nurseries containing local species and genets that are managed sustainably, eventually to eliminate the need for extraction of corals at natural sites (Epstein et al., 2001).

 

Artificial Reefs

Another widely used coral restoration tool is the use of artificial reefs. The efficiency of artificial reefs is seen mostly in fisheries management and in mitigation of marine ecosystems (Bohnsack and Sutherland, 1985; Seaman and Sprague, 1991; Collins and Jensen, 1999; Jensen et al., 2000). In addition to providing refuge for invertebrates, and adults and juvenile fish, they also divert human activities from natural reefs, which aids in the conservation of natural systems that are under pressure (Collins and Jensen, 1999). One of the pros when using artificial reefs, is the ease of their removal in cases where they fail to achieve their goals, as opposed to more complex restoration methods like coral transplantation (Abelson, 2006). They also provide extra surfaces that can assist in recruitment of natural reefs, provide connectivity between reefs and restore areas damaged by human activity (Abelson, 2006; Viral Forest, 2015). Not only do these reefs provide ecological benefits, but some countries have collaborated with local artists to create sculptured sunken reefs that serve as tourist diving attractions. The wide diversity of artificial reef designs range from Christian statues, to abstract structures, to placement of larger objects such as sunken aircrafts and New York subway cars (Milon, 1983; Raineault et al., 2004). Some of these objects take as little as 6-7 years to equilibrate with their environments and have been shown to increase diversity and numbers of fish and invertebrates (Raineault et al., 2004; Speiler, 2001). However, studies on the impact of large seafloor objects on sedimentation and currents have shown an increased rate of flow around those objects, creating scour moats (Raineault et al., 2014). This has serious implications for the stability for certain benthic communities and organisms trying to establish on these reefs. Where coral reefs are a major tourist attraction, individuals also still prefer the aesthetic value of more “natural looking” reefs as opposed to unnatural or artistic structures (Speiler et al., 2001).

Figure 2. NYC Subway after 10 years of being sunken

Some of these artificial reefs have been proposed to solve other environmental issues such as garbage and recycling accumulation in developed nations. Project Oyster-Tecture is an artificial reef composed of thousands of recycled glass “jacks” (as in the game) sunken into the seabed. The plan is to seed oysters in the reef off the coast of Brooklyn to act as a natural filtration system for industrial pesticides and heavy metals (Glasiusz, 2010). In addition to creating habitat for marine life, it would also be a partial solution to the nearly 3,000 tonnes of glass per week that is discarded in New York (Glasiusz, 2010).

Not all artificial reef proposals present extensive, scientifically evaluated waste solutions. In 1987, a Philadelphia based company, Waste Central Inc. proposed a 70 mile-long artificial reef off the coast of Saba, in the Netherlands Antilles. The reef would be made of rubbish and landfill encased in layers of concrete and steel. The project proposal was rejected due to the risk of environmental harm to the marine environment by leached waste materials (Morrissey 1998).

Future Research

Until extensive research is encouraged for all artificial reef endeavors, these options cannot be considered the ultimate solution to coral reef degradation. Hein et al., 2017 proposes evaluating coral restoration across 10 socio-ecological indicators including: (1) coral diversity; (2) herbivore biomass and diversity; (3) benthic cover; (4) recruitment; (5) coral health; (6) reef structural complexity; (7) reef user satisfaction; (8) stewardship; (9) capacity building; and (10) economic value. Integrating ecological, socio-cultural, economic and governance consideration is vital in the sustainability of coral reef restoration (Hein et al., 2010). Until extensive and long term monitoring is employed at these reef sites, we cannot determine whether these projects were successful, or whether these methods can be applied in other areas of the world. In addition, any new restoration plans must be developed with specific restoration objectives in mind. In this way, multi-treatment, hypothesis-based restoration plans can be monitored and evaluated to test for the success of their outcomes (Speiler et al., 2001). In conclusion, coral reef restoration has produced some positive results in mitigating anthropogenic impacts of biodiversity decline; however, without continued research and long term monitoring, we may not be utilizing these methods to their full potential in creating resilience in our marine ecosystems.

Bibliography

Abelson, A. 2006. Artificial Reefs vs. Coral Transplantation as Restoration Tools for Mitigating Coral Reef Deterioration: Benefits, Concerns and Proposed Guidelines. Bulletin of Marin Science. 78(1): 151-159

Bayraktarov, E., Saunders, M. I., Abdullah, S., Mills, M., Beher, J., Possingham, H. P., . . . Lovelock, C. E. (2015). The cost and feasibility of marine coastal restoration. Ecological Applications. doi:10.1890/15-1077.1

Bohnsack, J. A. and D. L. Sutherland. 1985. Artificial reef research: a review with recommendations for future priorities. Bull. Mar. Sci. 37: 11–39.

Collins, K. J. and A. Jensen. C. 1999. Artificial reefs. Pages 259–272 in C.P. Summerhayes and S.A. Thorpe, eds. Oceanography: an illustrated guide. John Wiley & Sons, New York.

Dobson AP, Bradshaw AD, Baker AJM. 1997. Hopes for the future: restoration ecology and conservation biology. Science 227: 515–521.

Edwards AJ, Clark S. 1998. Coral transplantation: a useful management tool or misguided meddling? Marine Pollution Bulletin 37: 8–12.

Epstein N, Bak RPM, Rinkevich B. 2001. Strategies for gardening denuded coral reef areas: the applicability of using different types of coral material for reef restoration. Restoration Ecology 9: 432–442.

Epstein, N., Bak, R., & Rinkevich, B. (2003). Applying forest restoration principles to coral reef rehabilitation. Aquatic Conservation: Marine and Freshwater Ecosystems,13(5), 387-395. doi:10.1002/aqc.558

Glausiusz, J. 2010. Artificial Reefs to Buffer New York. Nature. 464: 982-983.

Graham NAJ, Bellwood DR, Cinner JE, Hughes TP, Norstrom AV, Nystrom M (2013) Managing resilience to reverse phase shifts in coral reefs. Frontiers in Ecology and the Environment, 11, 541–548.

Hein, M. Y., Willis, B. L., Beeden, R., & Birtles, A. (2017). The need for broader ecological and socioeconomic tools to evaluate the effectiveness of coral restoration programs. Restoration Ecology,25(6), 873-883. doi:10.1111/rec.12580

Hobbs RJ, Hallett LM, Ehrlich PR, Mooney HA (2011) Intervention ecology: applying ecological science in the twenty-first century. BioScience, 61, 442–450.

Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends in Ecology & Evolution, 24, 599–605.

Hobbs RJ, Norton DA. 1996. Towards a conceptual framework for restoration ecology. Restoration Ecology 4: 93–110.

Jensen, A. C., K. J. Collins, and A. P. M. Lockwood. 2000. Artificial reefs in European seas. Kluwer Academic Publishing, Dordrecht.

Milon, J. W. 1983. Economic benefits of artificial reefs: An analysis of the Dade County, Florida reef system. Florida Sea Grant Prog. Rpt. 93 p.

Morrissey, S. 1988. Sanctuaries or Garbage Dumps? Oceans. 21(4) pp. 57

Raineault, N. A., Trembanis, A. C., Miller, D. C., & Capone, V. (2013). Interannual changes in seafloor surficial geology at an artificial reef site on the inner continental shelf. Continental Shelf Research,58, 67-78. doi:10.1016/j.csr.2013.03.008

Rinkevich B. 1995. Restoration strategies for coral reefs damaged by recreational activities: the use of sexual and asexual recruits. Restoration Ecology 3: 241–251.

Seaman, W. and L. M. Sprague. 1991. Artificial habitats for marine and freshwater fisheries. Academic Press, San Diego. 285 p.

SER (2004) The SER Primer on Ecological Restoration. Version 2. Society for Ecological Restoration Science and Policy Working Group. Available at: http://www.ser.org

Speiler, R.E., Gilliam, D.S., Sherman, R.L. 2001. Artificial substrate and coral reef restoration: what do we need to know and know what we need. Bulletin of Marine Science. 69 (2), 1013-1030.

 

Van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences of the United States of America, 112, 2307–2313.

Viral Forest (2015, January 22). Stunning Photos Showing NYC Subway Cars Being Dumped Into the Ocean. Retrieved from http://www.viralforest.com/subway-cars-dumped-coral-reef/

 


Climate Change: Shifting Wildlife Disease Dynamics

By Linzy Jauch

Emerging infectious disease threatens biodiversity as it causes significant ecologic shifts in response to a changing climate. Climate change provides opportunities for infectious disease to emerge through elevated mean temperatures, extreme temperature variation, and altered global patterns of precipitation 4,8. Environmental change has the potential to alter physiological and ecological traits of disease such as host-pathogen interactions, pathogen resistance and range distribution. Recent discoveries in wildlife diseases such as Batrachochytrium dendrobatidis (Bd) in amphibians 2 or blue tongue virus (BTV)4 in ruminants is allowing us to understand to the extent in which climate change is altering disease.

Bd infection of the skin causing death through cardiac arrest. Photo: SOLVIN ZANKL/ VISUALS UNLIMITED/ CORBISFI

Today, one-third (32.5%) of the Earth’s amphibians are threatened with extinction6. The pathogenic fungus Batrachochytrium dendrobatidis has been tied to the extinction of 50-80 species worldwide 2 and continues to threaten global amphibian biodiversity. The fungus attacks the moist skin of amphibians and causes degeneration15. Amphibians use their skin in respiration and in balancing essential ions13 within the body. The fungus creates an imbalance in essential ions within the body that result in death through cardiac arrest13. Though rates of infection have been increasing, Bd is not new to species rich environments7, amphibian immune systems were just previously able to fend off infections.

Climate change has altered the disease dynamics of Bd, specifically host-pathogen interactions and pathogen resistance4. Amphibians are ectothermic, relying on external sources to regulate their body temperature and regulate bodily processes such as metabolism and immune responses. Increased climate variability results in temperature fluctuations that subject amphibians to thermal stress. Documented outbreaks of Bd coincide with dramatic changes in temperatures over a short period of time, characteristic of climate change10.   Ectothermic species are more susceptible to thermal stress at temperatures in which they are unaccustomed2 due to an inability to quickly acclimate and match their body temperature with the envrionment4. When temperature changes rapidly, there is an acclimation lag in which the amphibian is adjusting bodily functions to coincide with the temperature shift. However, microbes and pathogens have a broader range of temperature tolerances2 and acclimate quickly8. This thermal mismatch creates a window of opportunity for infection that was less frequent before human-caused climate change caused increased regional temperature variation. Monthly and diurnal fluctuations in temperature decreases amphibian resistance to Bd by suppressing immune defenses that are relient on the amphibian’s ectothermic physiology. Together, through a slow acclimating immune response and a suppressed immune system, Bd is becoming an epidemic.

While Bd’s emergence is in response to changes in host-pathogen interactions, other infectious diseases such as blue-tongue virus in ruminants has undergone a different type of shift in response to climate change. The disease is transferred though the bites of cold-sensitive midges and has been responsible for mass mortalities of sheep and cattle in the Mediterranean region14. Higher average temperatures have led to the northward expansion of midges, and thus an expansion of the BTV range4. The expansion provides new opportunities for the infection of new hosts and threatens domestic and wild ruminant biodiversity.

Regions in blue demonstrate areas now suitable for BTV based on current climate data and increased average temperatures allowing range expansion. Original ranges in North Africa and in the Middle East (4). Chart by Samy and Peterson 2016.

Disease dynamics are altering in response to human-caused climate change7 and are contributing to more extinctions than we originally suspected. The link between human-mediated climate change and infectious disease is complicated due to many intertwining factors5 and must be teased apart to understand what can be done to prevent future emerging infectious diseases. Infectious disease is significantly impacting complex ecologic processes. Biodiversity loss, abandoned niches, and new host infections have already resulted as a response to climate change and infectious disease emergence. Future research focused on understanding the extent to which biodiversity loss has been magnified through infectious disease emergence is necessary for developing mitigation methods that may save small and endangered wildlife populations from extinction.

References

[1] Altizer S, Ostfeld RS, Johnson PT, Kutz S, Harvell CD. 2013. Climate Change and Infectious Diseases: From Evidence to a Predictive Framework. Science 341: 514 – 519.

[2] Cohen J. 2016. Climate Change Drives Outbreaks of Emerging Infectious Disease and Phenological Shifts. Unpublished PhD thesis, University of South Florida, Tampa, USA.

[3] Daszak P, Cunningham AA, Hyatt AD. 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78: 103-116.

[4] Gallana M, Ryser-Degiorgis MP, Wahli T, Segner H. 2013. Climate change and infectious diseases of wildlife: Altered interactions between pathogens, vectors and hosts. Current Zoology 59(3): 427-437.

[5] Lafferty KD. 2009. The ecology of climate change and infectious diseases. Ecology 90(4): 888-900.

[6] Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins JP. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. PNAS 103(9): 3165-3170.

[7] Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, Marca EL, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sánchez-Azofeifa, Still CJ, Young BE. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439: 161-167.

[8] Raffel TR, Halstead NT, McMahon TA, Davis AK, Rohr JR. 2015. Temperature variability and moisture synergistically interact to exacerbate an epizootic disease. Proceedings of the Royal Society B 282(1801).

[9] Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR. 2013. Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change 3: 146-151.

[10] Rohr JR and Raffel TR. 2010. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. PNAS  107(18): 8269-8274.

[11] Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ. 2008. Evaluating the links between climate, disease spread, and amphibian declines. PNAS 105(45):17436-17441.

[12] Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR. 2008. Agrochemicals increase trematode infections in a declining amphibian species. Nature 445(30): 1235 -1239.

[13] Rollins-Smith LA. 2017. Amphibian immunity – stress, disease, and climate change. Developmental and Comparative Immunology 66:111-119.

[14] Samy AM and Peterson AT. 2016. Climate Change Influences on the Global Potential Distribution of Bluetongue Virus. PLoS ONE 11(3).

[15] Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ. 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 10(21): 9689-9694.

[16] Yang Xie G, Olson DH, Blaustein AR. 2016. Projecting the Global Distribution of the Emerging Amphibian Fungal Pathogen, Batrachochytrium dendrobatidis, Based on IPCC Climate Futures. PLoS ONE 11(8).