Implications – Novel Ecosystems

De-Extinction

Just as novel ecosystems challenge conservation thinking, so does the expansion of our ability to synthesize nature. Conservationists are facing new appeals to adopt bold approaches embracing advances in genetic technologies (Piaggio et al., 2016). These advances offer a vast array of putative technological applications for addressing conservation problems. But none have grabbed as many headlines as proposals to use cloning and gene-editing techniques (notably CRISPR-Cas9) to resurrect extinct species, in a new field known as de-extinction.

We do not yet share the planet with any creatures created through de-extinction. But, if current trends continue, one day soon we will (Folch et al., 2009). Lets assume that when that day comes our goal is to use de-extinction to help ecosystems and not just create zoo curiosities. How might de-extinction help? One driver of novelty in ecosystems the loss of ecosystem function due to extinction. If we could restore lost species to landscapes then we should also be able to restore the ecological functions they provided, right? The highly speculative nature of de-extinction makes it hard to draw meaningful conclusions about how well this would work. But one thing seems clear — de-extinction will have little ecological value to offer if we target the wrong species. Choosing de-extinction candidates wisely could make the difference between restoring a valuable ecosystem function and creating an “eco-zombie” (McCauley et al., In Press). Writing in the journal of Functional Ecology, McCauley and his co-authors give some guidelines for selecting de-extinction candidates most likely to restore ecosystem function. How does the list of current and proposed de-extinction projects line up? Lets hope eco-zombies don’t have an appetite for brains.

Proposed candidates for de-extinction exhibit obvious biases. They are mostly furry, feathered, terrestrial and include many long-lost but iconic species such as the mammoth, Tasmanian tiger, passenger pigeon and, more recently, the dodo (McCauley et al., In Press; Seddon et al., 2014). McCauley et al.’s guidelines do not identify “charismatic” as a criterion for species selection. Yet ecologically important but less beloved groups of species, including many marine and invertebrate species, are all but entirely ignored by de-extinction enthusiasts. Well then, according to the guidelines, how do we choose wisely? First, avoid species that went extinct a long time ago. The adage “absence makes the heart grow fonder” does not apply to ecosystems. When a species disappears, the ecosystem moves on and the remaining species settle into new relationships. And if a reintroduced species has been gone too long, there may no longer be a suitable niche for it to occupy.

Martha, the last passenger pigeon, skinned. Courtesy of R. W.Schufeldt/Wikimedia Commons

The guidelines also advise choosing species that provided unique ecosystem services — a characteristic common among marine species, for example. Finally, it is important to be mindful that some species only provide an ecological function when restored in very large numbers. The abundance-dependent nature of the passenger pigeon’s ecological impact, for example, would present a steep barrier to restoring ecosystem function. Unlike a top predator, such as wolves, which can provide an important ecological function with a relatively small number of individuals, the passenger pigeons would require millions or even billions of birds.

Even if one strictly adheres to these guidelines, there remains room to question whether releasing de-extinct creatures onto wild landscapes amounts to restoration. One might argue that de-extinction creates novel organisms not familiar to any landscape. Many argue, and I would tend to agree, that de-extinction would create a new and distinct class of beings rather than the biological and behavioral equivalents of extinct animals (Martinelli et al., 2014). In its draft report, Guiding Principles on De-extinction for Conservation Benefit, the IUCN (World Conservation Union) Species Survival Commission refers to species created through de-extinction as “proxy species,” rather than regarding them as faithful recreations of the extinct animals’ original forms (IUCN/SSC, 2016). Many authors have begun following IUCN’s lead in acknowledging the novel character that would distinguish these creatures from their extinct ancestors, referring to them as proxy species, or similarly “ecological proxies” or “analogues” (e.g. Adams, 2016; McCauley et al., In Press; Piaggio et al., 2016; Shapiro, 2016).

Why might the creatures we make through de-extinction be different? First, de-extinction requires another species to donate an “empty” egg cell and serve as a maternal host. Consequently, the resulting clone’s mitochondrial DNA, microbiome and epigenetics won’t match that of the extinct ancestor (Friese, 2013; Shapiro, 2015). And for long-extinct species (e.g. mammoth, passenger pigeon, Tasmanian tiger), departures from extinct ancestors will be much greater because we must piece them together using incomplete DNA fragments. Finally, who would teach these novel creatures how to find food, migrate, communicate and care for their young? But perhaps these differences are less ecologically consequential than we might be inclined to think.

In a “TEDxDe-extinction” conference talk in 2013, conservation biologist Kent Redford challenges the significance we attribute to species purity.

As he points out, the bison repopulating plains in Western U.S. are ‘tainted’ with cattle genes. Yet they retain behaviors responding “to fire and grazing and predators like bison,” and defending “their calves from wolves like bison.” And the same goes for wolves, which are sometimes tainted with domestic dog genes but are still “taking down elk, [and] re-arranging energy flows” with top-down predatory behaviors.

Unsurprisingly, Redford does not suggest that we start referring to “proxy” bison or wolf “analogues.” Yet in a recent article, Redford and his coauthors describe de-extinction as “creating a proxy species that hopefully fills the same ecological role as the extinct species” (italics added) (Piaggio et al., 2016). Proxy probably won’t displace “de-extinction” anytime soon. But perhaps its growing use signals an increasing recognition for the need to ground the hyperbolic rhetoric that has emerged around this technology. And perhaps a recognition for the need to adopt vocabulary that will set proper expectations about its promise for addressing ecological and biodiversity problems.

~By Patrice Kohl~

Adams, W. M. (2016). Geographies of conservation I De-extinction and precision conservation. Progress in Human Geography, 0309132516646641.

Folch, J., Cocero, M. J., Chesné, P., Alabart, J. L., Domínguez, V., Cognié, Y., . . . Vignon, X. (2009). First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology, 71(6), 1026-1034. doi:http://dx.doi.org/10.1016/j.theriogenology.2008.11.005

Friese, C. (2013). Cloning wild life: zoos, captivity, and the future of endangered animals: NYU Press.

IUCN/SSC. (2016). Draft IUCN SSC Guiding Principles on Creating Proxies of Extinct Species for Conservation Benefit. Gland, Switzerland: IUCN Species Survival Commission.

Martinelli, L., Oksanen, M., & Siipi, H. (2014). De-extinction: a novel and remarkable case of bio-objectification. Croatian Medical Journal, 55(4), 423.

McCauley, D. J., Hardesty‐Moore, M., Halpern, B. S., & Young, H. S. (In Press). A mammoth undertaking: harnessing insight from functional ecology to shape de‐extinction priority setting. Functional Ecology.

Piaggio, A. J., Segelbacher, G., Seddon, P. J., Alphey, L., Bennett, E. L., Carlson, R. H., . . . Wheeler, K. (2016). Is It Time for Synthetic Biodiversity Conservation? Trends in Ecology & Evolution. doi:10.1016/j.tree.2016.10.016

Seddon, P. J., Moehrenschlager, A., & Ewen, J. (2014). Reintroducing resurrected species: selecting DeExtinction candidates. Trends in Ecology & Evolution, 29(3), 140-147.

Shapiro, B. (2015). How to clone a mammoth: the science of de-extinction: Princeton University Press.

Shapiro, B. (2016). Pathways to de‐extinction: how close can we get to resurrection of an extinct species? Functional Ecology.

Novelty and the Science of Ecology

Novel ecosystems present ecologists with a rare opportunity to expand the science of ecology. Ecological novelty is discussed in this seminar as a quantifiable gradient of change in one or several dimensions. This framework then allows for testing how classical theories (e.g.Island biogeography) hold up to various degrees of novelty, and more importantly to develop new questions that move the field of ecology forward. In this webpage, we will expand on the idea that novel ecosystems present an unforeseen and underutilized opportunity to develop the science of ecology across disciplines. We will use two research articles by Aronson et al. 2014 and McCullough Hennessy et al. 2016, to demonstrate systems where ecological novelty resulted in the exploration of (1) new ways to think of classical research questions and (2) novel ways to solve ecological problems respectively.

Over half of the human population now lives in cities and this is a trend that is expected to be maintained. The authors in Aronson et al. 2014, aim to look at the potential biotic homogenization of 147 cities worldwide. They find that the regional nature of most cities is responsible for reducing global biotic homogenization. They also find that most cities maintain higher diversity of native birds and plants than exotic species. Nevertheless, the density of native species is lower than in peri-urban and rural areas. This example was chosen to demonstrate cities as novel ecosystems and how biotic homogenization can be tested in these systems. While the author recognizes cities as novel ecosystems, there is no way to assess the degrees of novelty of different cities. European cities are in average hundreds if not thousands of years older than western cities, which could be perceived as less novel than cities that have been settled for a few hundred years. This is a challenge that needs to be addressed for the novel ecosystem framework to develop the science of ecology. Are older cities more similar to each other in terms of biotic diversity, or do modern cities have better plans for maintaining biotic diversity or other ecosystem properties? These questions could be expanded upon by a quantitative metric of novelty that considers the characteristics of cities. For example, light pollution levels, the total area of homogeneous yard space, degree of the heat-island effect are several characteristics of cities that can be incorporated into a novelty metric. This metric in turn can be used to assess the effect of novelty on ecosystem properties of interest.

Novel ecosystems can also be used to test experimental approaches that can be applied for conservation or restoration ecology. The authors in McCullough et al. 2016 consider an invaded tallgrass ecosystem as a novel ecosystem, where they aim to reintroduce the ground squirrel (Otospermophilus beecheyi), to improve the habitat opportunity of the western burrowing owl (Athene cunicularia hypugaea). The authors use this novel ecosystem as an opportunity to restore the availability of burrows in the invaded grassland by reintroducing the ground squirrel, mowing and augering the soil without a removal or extermination of the invasive tall grass. They find that the number of burrows was much higher in the auger and mowing plots. They also find that locally, squirrels could maintain tall grasses at low height. This is important for the habitat quality of the burrowing owl and the squirrel. They hypothesize that if squirrels were at higher abundance the effect would be sufficient to maintain the tall grass at low height. The authors argue that this system would resemble a hybrid system, maintaining aspects of novel ecosystems and the native or historical ecosystem. We agree with the authors in this aspect, yet we suggest that this ambivalence of hybrid or novel ecosystem would be resolved with a metric of novelty that can be assessed in a gradient. This approach can facilitate thinking and managing novel ecosystems. If novelty is not a desirable characteristic of a system,management approaches could aim to lower the novelty of a system, instead of eliminating it.

We found that the literature of novel ecosystems is embedded deeply in the conservation and restoration ecology disciplines. We found that in these disciplines rarely novel ecosystems used as an opportunity to explore classic ecological questions or develop new concepts and ideas in ecology. We are interested in why this occurs. We ask, do we know everything we need to know in the field of ecology? Are more people interested in conservation science and not in theoretical ecology? We would like to continue to explore what are the big questions that remain in the field of ecology and to what extent novel ecosystems can be used to address some of these questions. We hope that these ideas will continue to be explored beyond conservation and restoration ecology. This is a continuing conversation that needs to expand beyond our group, and through this medium we look forward to maintain this conversation.

References

Aronson, Myla F. J., Frank A. La Sorte, Charles H. Nilon, Madhusudan Katti, Mark A. Goddard,Christopher A. Lepczyk, Paige S. Warren, et al. 2014. “A Global Analysis of the Impacts ofUrbanization on Bird and Plant Diversity Reveals Key Anthropogenic Drivers.” Proc. R. Soc.

B 281 (1780): 20133330. doi:10.1098/rspb.2013.3330.

McCullough Hennessy, S., D. H. Deutschman, D. M. Shier, L. A. Nordstrom, C. Lenihan, J.-P.Montagne, C. L. Wisinski, and R. R. Swaisgood. 2016. “Experimental Habitat Restorationfor Conserved Species Using Ecosystem Engineers and Vegetation Management.” Animal

Conservation 19 (6): 506–14. doi:10.1111/acv.12266.

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Biotic Homogenization

Biotic homogenization is an emerging, yet pervasive, threat in the ongoing biodiversity crisis. Originally, ecologists defined biotic homogenization as the replacement of native species by exotics (McKinney and Lockwood 1999), but this phenomenon is now more broadly recognized as the process by which ecosystems lose their biological uniqueness (Olden and Rooney 2006). Specifically, ecologists now differentiate between taxonomic, functional, and genetic homogenization. Taxonomic homogenization, or the increased similarity of species over space and time, has occurred across numerous taxa, including plants (Rooney et al. 2004), insects (Dormann et al. 2007), fish (Rahel 2000), birds (Devictor et al. 2007), and mammals (Isaac et al. 2014). Rising community similarity can occur via multiple pathways. For example, communities may become more similar following species invasions due to increased species richness (i.e. changes in α diversity), or, conversely, communities may become homogenized following the loss or replacement of native species (i.e. changes in β diversity). While such taxonomic homogenization has received the lion’s share of the attention, functional homogenization, or the convergence of ecological niches and functional roles among community members, may be more consequential due to the constraints imposed on both biodiversity and ecosystem processes (Olden et al. 2004; Clavel et al. 2011). Indeed, functional homogenization is a near ubiquitous consequence of human agency and is driven by the loss of specialized species or functional groups and their subsequent replacement by generalist taxa (Fig. 1). The loss of rare or endangered species, though, is not a new phenomenon, and conservationists have been combating such processes through reintroductions for generations. However, such translocations and human-assisted dispersal events can lead to a third, genetic, form of homogenization, whereby native populations lose local adaptations or evolutionary potential through reductions in allelic diversity (Olden et al. 2004). This process, commonly referred to as outbreeding depression, has long been a concern among reintroduction biologists, but the increase in genetic homogenization due to invasive species, hybridization events, and increasing human-assisted dispersal (McDonald et al. 2008) is an emerging concern in conservation and evolutionary biology.

Figure 1. Regional species pools consist of generalists and specialists with specific functional traits. Anthropogenic gradients of disturbance filter species traits and ultimately determine the functionality of the community. Low disturbance ecosystems tend to result in communities of specialists with high complementarity and high ecosystem function, while highly disturbed systems favor generalist species and lead to communities homogenized both taxonomically and functionally. Adapted from Clavel et al. (2011).

What are the drivers of biotic homogenization?

All forms of biotic homogenization have broadly been tied to human activities, but the mechanisms driving these patterns are diverse. For example, landscape simplification can lead to resource declines while agricultural intensification precipitates the heavy use of pesticides, and both processes have generated taxonomic and functional homogenization in managed landscapes (Dormann et al. 2007; Gámez-Virués et al. 2015). Similarly, the loss of habitat and resources following urbanization can induce all three forms of biotic homogenization (Clavero and Brotons 2010; Luck and Smallbone 2011; Morelli et al. 2016), as can competition and hybridization with invasive species (Devictor et al. 2007; McDonald et al. 2008; Isaac et al. 2014). Even seemingly mundane practices like supplemental food via backyard bird feeders can favor exotic species and homogenize local communities (Galbraith et al. 2015), and the intentional management of overabundant herbivore populations can promote exotic, generalist flora through reductions in native species (Rooney et al. 2004). The mechanisms can also be cryptic. For example, introduced species regularly hybridize with endemics and can homogenize local gene pools (Dowling and Childs 1992; McDonald et al. 2008), and the construction of human infrastructure such as dams often unknowingly facilitates such processes. Moreover, looming ecological threats, like climate change, promote the expansion of generalist species and homogenize regional bird communities (Davey et al. 2012), while oceanic acidification has promoted similar changes in coral reef communities (Hughes et al. 2003; Burman et al. 2012). Ultimately, biotic homogenization at all levels appears to be an inescapable consequence of human agency.

Is biotic homogenization novel?

Clearly, the causes of biotic homogenization are numerous and the consequences great, but is this homogenization novel? As global species assemblages converge toward communities of generalists, it can be argued that homogenized ecosystems are the antithesis of novelty, with nearly identical communities replicated across the globe. Yet, relative to Pleistocene or even pre-Columbian baselines, simplified local communities composed of non-native species are almost certainly novel. Such mixing of biota, however, is not a new phenomenon, and novel communities have clearly arisen throughout earth’s history (Vermeij 1991; Williams and Jackson 2007). Nevertheless, the pace and trajectory of the current biotic homogenization crisis is unparalleled (Ricciardi 2007), and human agency has undoubtedly facilitated such changes. Moreover, drivers like rapid climatic warming, agricultural intensification, booming urban centers, uncontrollable invasive species, intensive overharvest of wildlife, and immeasurable human-derived food subsidies likely have few analogs in earth’s history. Consequently, it appears that the most novel components of biotic homogenization are the mechanisms driving this phenomenon rather than the process itself. In the end, the novel pressures exacted upon our ecosystems by human activities will likely continue to blend the planet’s biota (Fig. 2), with unknown consequences for future ecosystem stability and function.

Figure 2. The “Anthropogenic blender” homogenizing earth’s ecosystems, sensu (Olden 2006). Reproduced from http://depts.washington.edu/oldenlab/biotic-homogenization/.

~By Phil Manlick~

References:

Burman SG, Aronson RB, and Woesik R Van. 2012. Biotic homogenization of coral assemblages along the Florida reef tract. Mar Ecol Prog Ser 467: 89–96.

Clavel J, Julliard R, and Devictor V. 2011. Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9: 222–8.

Clavero M and Brotons L. 2010. Functional homogenization of bird communities along habitat gradients: Accounting for niche multidimensionality. Glob Ecol Biogeogr 19: 684–96.

Davey CM, Chamberlain DE, Newson SE, et al. 2012. Rise of the generalists: Evidence for climate driven homogenization in avian communities. Glob Ecol Biogeogr 21: 568–78.

Devictor V, Julliard R, Couvet D, et al. 2007. Functional homogenization effect of urbanization on bird communities. Conserv Biol 21: 741–51.

Dormann CF, Schweiger O, Augenstein I, et al. 2007. Effects of landscape structure and land-use intensity on similarity of plant and animal communities. Glob Ecol Biogeogr 16: 774–87.

Dowling T and Childs M. 1992. Impact of hybridization on a threatened trout of the southwestern United States. Conserv Biol.

Galbraith JA, Beggs JR, Jones DN, and Stanley MC. 2015. Supplementary feeding restructures urban bird communities. Proc Natl Acad Sci U S A: E2648–57.

Gámez-Virués S, Perović DJ, Gossner MM, et al. 2015. Landscape simplification filters species traits and drives biotic homogenization. Nat Commun 6: 8568.

Hughes TP, Baird AH, Bellwood DR, et al. 2003. Climate change, human impacts and resilience of coral reefs. Science (80- ) 301: 929–33.

Isaac B, White J, Ierodiaconou D, and Cooke R. 2014. Simplification of arboreal marsupial assemblages in response to increasing urbanization. PLoS One 9.

Luck GW and Smallbone LT. 2011. The impact of urbanization on taxonomic and functional similarity among bird communities. J Biogeogr 38: 894–906.

McDonald DB, Parchman TL, Bower MR, et al. 2008. An introduced and a native vertebrate hybridize to form a genetic bridge to a second native species. Proc Natl Acad Sci U S A 105: 10837–42.

McKinney M and Lockwood J. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14: 450–3.

Morelli F, Benedetti Y, Ibáñez-Álamo JD, et al. 2016. Evidence of evolutionary homogenization of bird communities in urban environments across Europe. Glob Ecol Biogeogr: 1–10.

Olden JD. 2006. Biotic homogenization: A new research agenda for conservation biogeography. J Biogeogr 33: 2027–39.

Olden JD, Leroy Poff N, Douglas MR, et al. 2004. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19: 18–24.

Olden JD and Rooney TP. 2006. On defining and quantifying biotic homogenization. Glob Ecol Biogeogr 15: 113–20.

Rahel FJ. 2000. Homogenization of fish faunas across the United States. Science (80- ) 288: 854–6.

Ricciardi A. 2007. Are modern biological invasions an unprecedented form of global change? Conserv Biol 21: 329–36.

Rooney TP, Wiegmann SM, Rogers D a., and Waller DM. 2004. Biotic impoverishment and homogenization in unfragmented forest understory communities. Conserv Biol 18: 787–98.

Vermeij GJ. 1991. When biotas meet: understanding biotic interchange. Science (80- ) 253: 1099–104.

Williams JW and Jackson ST. 2007. Novel climates, no-analog communities, and ecological surprises. Front Ecol Environ 5: 475–82.