March 11, 2015

The Grey Wolves of Europe

The grey wolf (Canis lupus) is one of the Northern Hemisphere’s most iconic carnivores. However, in a matter of centuries, the grey wolf has been exterminated from at least a third of its former range [1]. Until 2004, wolves remained listed as “Vulnerable” on the IUCN Red List for Endangered Species [1]. The grey wolf is now making an unexpected comeback in North America and Europe [2–4]. A proposal to strip the grey wolf of the protection from the US Fish and Wildlife Service (USFWS) recently sparked debate, leading to an independent review of the species’ situation in North America [5]. Despite the recovery wolves are making, retracting their protected status could reverse this situation once again [5]. What’s more, a mere rise in numbers may not suffice to ensure the future of the species, as extreme population reduction and fragmentation come with less apparent, genetic consequences as discussed below [6–8]. Additionally, as an apex predator, a great deal of controversy surrounds the conservation and return of the grey wolf [4]. With this short essay I intend to give a brief overview of some of the biological and cultural challenges facing the conservation and return of the grey wolf in Europe.

Though on a global scale the grey wolf’s numbers never plummeted to critical levels as many other carnivores have [1, 9, 10], on a local scale many geographic populations became extinct (see Figure 1 for European distribution). Remaining populations were reduced and fragmented. There have been increasing concerns regarding the consequences of small populations may have for species conservation [7, 8]. It may seem intuitive that small isolated populations are at greater risk of extermination by natural or anthropogenic catastrophes, such as disease or hunting; however, less evident effects may occur at the genetic level.
Figure 1 - Historical (orange, light) and present
(red, dark) grey wolf distribution in Western Europe.
Sources: WWF Germany, IUCN Red List,
and the European Commission.

As the size of a panmictic population is reduced, random genetic drift will increase, as will the occurrence of inbreeding [11]. Increasing effects of drift weaken the force of selection for the fittest individuals, as alleles are randomly fixed in the population [11]. Inbreeding can augment the chances of recessive deleterious alleles being uncovered [11]. Both processes ultimately reduce the genetic diversity of populations, reducing their adaptability and evolutionary potential, and causing a positive feedback effect of further population loss and greater risk of individual deaths [12]. The extent to which drift and inbreeding depression will affect populations depends on the genetic composition of the initial population [8] and environmental stress [13]. Therefore, to ensure the grey wolf’s future it may be important to assess whether there are any resounding genetic effects overshadowing the current populations, which could hinder the long-term survival of the species.

A pair of Eastern European wolves that established themselves in Scandinavia offered a unique opportunity for biologists to assess the genetic and fitness consequences of small populations from its founding [8, 14]. The current population suffers from a degree of inbreeding equivalent to full sibling matings, which correlates with developmental problems [15] and smaller litter sizes [14]. The introduction of new genetic material to the population seemed to counteract inbreeding depression by increasing heterozygosity and ultimately lead to population expansion (whether this is directly related to heterozygosity itself or other factors is less clear) [14]. This “rescue” was short-lived and did not prevent a subsequent decrease in heterozygosity and increase in inbreeding [8]. Bensch et al. [16] warned of the disparity  between heterozygosity and inbreeding coefficient in the Scandinavian population, and demonstrated what appears to be selection for heterozygosity in the grey wolf. Selection for heterozygosites favours the retention of genetic variation despite the counteracting effect of drift [16]. This selective pressure may make the best of a bad situation, but without gene flow between populations, the overall fitness of this Scandinavian wolves is likely to decrease [8].

The case of the Scandinavian grey wolves sheds hope on the possibility of recovering genetic diversity in severely inbred populations. Perhaps more importantly, the Scandinavian example highlights the importance of gene flow and connectivity between wolf populations. Anthropogenic landscape changes can be a barrier to gene flow. Pilot et al. [17] determined that vegetation was the most strongly correlated factor explaining the genetic structure of European grey wolf populations. This may be partly due to the enormous influence wolves are known to have on their surrounding habitat, due to their control of grazers [4, 18, 19]. However, it seems plausible that vegetation composition could have a causative effect on wolf dispersal and distribution, by determining that of its prey items. On an evolutionary scale, the preferred prey items of a given wolf population will be influenced by what is available in a given region; on an ecological scale, there may be a learned component influencing their preference. These mutually entwined mechanisms could lead to genetic divergence of populations based on their prey preference and/or hunting strategy. Altering habitat and availability of specific prey, therefore, limits wolf distribution and meta-population connectivity, despite the great dispersal capabilities of grey wolves [6, 17].

Despite locally adapted preferences for vegetation and prey types, the grey wolf has proven itself to be a highly adaptable species: their spread throughout Europe has restored populations in the mountains and plains of Northern and Central Spain [3]; they have returned to places like Germany and Scandinavia, where they had been actively exterminated [4, 8, 14]; and while the glacial cycles of the Pleistocene deeply affected most European flora and fauna, climate change seems to have had relatively little impact on the distribution and population genetics of the grey wolf [20]. However, the environmental resilience of the grey wolf cannot confer it the means to pass some man-made and natural obstacles [1]. The United Kingdom (UK) and Ireland perhaps represent the clearest examples of this. Separated from the rest of Europe by the English Channel and the Irish Sea, the only way for wolves to once again become established is to be reintroduced by humans.

“Rewilding" is a sensitive contemporary issue, whether it involves allowing “weeds” to re-establish or reintroducing locally extinct species. While reintroducing any species sparks concerns over the effect it will have on the modified environment or, indeed, whether the species will be able to establish itself successfully, the notion of reintroducing large carnivores is particularly controversial [4, 21]. These are animals which have generally been driven from their former range either by competition with humans or active persecution. Brown bears (Ursus arctos), Eurasian lynx (Lynx lynx), and grey wolves once topped the food chain of the British Isles, but there is a great deal of opposition to reintroducing these species, particularly bears and wolves [22]. Other than for moral or aesthetic appeal of rewilding the countryside, could reintroducing wolves benefit humanity or the ecosystems the canids once reigned?

Carnivores play a key role in controlling populations of grazers. Overgrazing can substantially reduce biodiversity by preventing slow-growing species to mature (e.g. trees), reduce soil fertility, and alter riparian communities [19, 23, 24]. Such consequences of predator suppression have been clearly demonstrated in various National Parks (NP) in the United States. Reductions in puma occurrence (Puma concolor) in Zion NP lead to a substantial increase in mule deer (Odocoileus hemionus) populations, followed by a decrease in plant biodiversity and altered river topologies [19]. Likewise, the loss of large carnivores (including wolves) in Olympic NP had impacts on sapling survival and tree diversity, river topology, and even fish stocks [19]. Such conclusions were drawn based on comparisons between areas with and without predators. The direct effects of grey wolf reintroduction can be appreciated from studies in Yellowstone NP. Wolves were reintroduced to Yellowstone NP from Canada in the mid-90’s. Although both elk (Cervus elephas) and bison (Bison bison) have readjusted their behaviour since the presence of wolves, elk abundance has decreased to a more manageable level [18, 25]; consequently, cottonwood (Populus spp) and aspen (Populus tremuloides) populations have rebounded [19, 26, 27].

Despite the benefits of reintroducing locally extinct carnivores, fears of personal and livestock safety fuel opposition in most of rural Europe [21]. Livestock compensation schemes where wolves are already present improve local acceptance but do not necessarily change attitudes or prevent killing [3, 4]. Before active rewilding of former wolf ranges is possible, a change in attitudes is necessary to ensure the species’ long-term survival [2]. Given the declining and diverging genetic variability of the grey wolf in Europe, prioritising the protection and allowing the natural return of wolves may be more useful to conservation. Proper management of the remaining wolf populations — including monitoring the budding and migration of new populations — may suffice to salvage and ensure the grey wolf’s persisting genetic diversity. Conserving their adaptive potential will be crucial to allowing their continued spread and facilitate their successful reintroduction into less accessible territories.

Cited literature

1 - Mech, L. D. and Boitani, L. (2010). Canis lupus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. <>. Downloaded on 09 February 2014.

2 - Wydeven, A. P., Van Deelen, T. R., and Heske, E. J. (2000). Recovery of grey wolves in the Great Lakes region of the United States: an endangered species success story. Springer Science+Business Media, New York, USA.

3 - Blanco, J. C., Reig, S., and de la Cuesta, L. (1992). Distribution, status and conservation problems of the wolf Canis lupus in Spain. Biological Conservation, 60(2): 73-80.

4 - Gross, M. (2008). Return of the wolf: ecological restoration and the deliberate inclusion of the unexpected, Environmental Politics, 17(1): 115-120.

5 - National Center for Ecological Analysis and Synthesis (2014). Report: Review of Proposed Rule Regarding Status of the Wolf Under the Endangered Species Act. University of California, Santa Barbara.

6 - Vilà, C., Amorim, I. R., Leonard, J. A., Posada, D., Castroviejo, J., Petrucci-Fonseca, F., Crandall, K. A., Hellgren, H., and Wayne, R. K. (1999): Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Molecular Ecology, 8: 2089-2103.

7 - Leonard, J. A., Vilà, C. and Wayne, R. K. (2005) Fast track: Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus). Molecular Ecology, 14(1): 9-17.

8 - Liberg, O., Andren, H., Pedersen, H.-C., Sand, H., Sejberg, D., Wabakken, P., Ãkesson, M., and Bensch, S. (2005). Severe inbreeding depression in a wild wolf Canis lupus population. Biology Letters, 1: 17-20.

9 - Simón, M. A., Gil-Sánchez, J. M., Ruiz, G., Garrote, G., McCain, E. B., Fernández, L., López-Parra, M., Rojas, E. V. A., Arenas-Rojas, R., Rey, T. D., García-Tardío, M., and López, G. (2012). Reverse of the Decline of the Endangered Iberian Lynx. Conservation Biology, 26(4): 731-736

10 - Jackson, R., Mallon, D., McCarthy, T., Chundaway, R.A. & Habib, B. (2008). Panthera uncia. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. <>. Downloaded on 11 February 2014.

11 - Futuyma, D.J. (2005). Evolution. Sinauer Associates Inc, Sunderland, USA.

12 - Hedrick, P. W. and Kalinowski, S. T. (2000). Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics, 31:139-162.

13 - Armbruster, P. and Reed, D. H. (2005). Inbreeding depression in benign and stressful environments. Heredity, 95(3): 235-242.

14 - Vilà, C., Sundqvist A.-K., Flagstad, Ø., Seddon, J., Björnerfeldt, S., Kojola I., Casulli, A., Sand, H., Wabakken, P., and Ellegren, H. (2003). Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceeding of the Royal Society of London B, 270: 91–97

15 - Räikkönen, J., Bignert, A., Mortensen, P., and Fernholm, B. (2006). Congenital defects in a highly inbred wild wolf population (Canis lupus). Mammalian Biology, 71: 65–73.

16 - Bensch, S., Andrén, H., Hansson, B., Pedersen, H. C., Sand, H., Sejberg, D., Wabakken, P., Åkesson, W., Liberg, O. (2006). Selection for Heterozygosity Gives Hope to a Wild Population of Inbred Wolves. PLoS ONE, 1(1): e72. doi:10.1371/journal.pone.0000072. 

17 - Pilot, M., Jedrzejewski, W., Branicki, W., Sidorovich, V. E., Jedrzejewska, B., Stachura, K., and Funk, S. M. (2006). Ecological factors influence population genetic structure of European grey wolves. Molecular Ecology, 15: 4533–4553.

18 - Laundré, J. W., Hernández, L., and Altendorf, K. B. (2001). Wolves, elk, and bison: reestablishing the "landscape of fear" in Yellowstone National Park, U.S.A. Canadian Journal of Zoology, 79(8): 1401-1409.

19 - Beschta, R. L. and Ripple, W. J. (2012). The role of large predators in maintaining riparian plant communities and river morphology, Geomorphology, 157–158: 88-98.

20 - Sommer, R. and Benecke, N. (2005). Late-Pleistocene and early Holocene history of the canid fauna of Europe (Canidae). Mammalian Biology, 70(4): 227-241.

21 - Wilson, C. J. (2004). Could we live with reintroduced large carnivores in the UK? Mammal Review, 34(3): 211–232.

22 - Stuart, A. J. (1974). Pleistocene history of the British vertebrate fauna. Biological Review, 49: 225-266

23 - Fleischner, Thomas L.Ecological Costs of Livestock Grazing in Western North America (1994). Conservation Biology, 8(3): 629–644.

24 - Fjeldså, J. (2007). The relationship between biodiversity and population centres: the high Andes region as an example. Biodiversity Conservation, 16: 2739–2751

25 - Mao, J. S., Boyce, M. S., Smith, D.W, Singer, F. J., Vales, D. J., Vore, J. M., Merrill, E. H. (2005). Habitat selection by elk before and after wolf reintroduction in yellowstone national park. Journal of Wildlife Management, 69(4):1 691-1707.

26 - Ripple, W. J., and Beschta, R. L. (2003) Wolf reintroduction, predation risk, and cottonwood recovery in Yellowstone National Park. Forest Ecology and Management, 184(1-3): 299-313.

27 - Ripple, W. J., and Beschta, R. L. (2012). Trophic cascades in Yellowstone: The first 15 years after wolf reintroduction. Biological Conservation, 145(1): 205-213.

No comments :

Post a Comment