Journal of Wildlife and Biodiversity 4(2): 1-12 (2020) (http://jwb.araku.ac.ir/)

DOI: 10.22120/jwb.2019.109875.1074 Review Article Current knowledge of the Neozoa Nutria and Muskrat in Europe and their environmental impacts

development, low winter temperatures, and Friederike Gethöffer*, Ursula Siebert aquatic habitats are substantial factors. Research Institute for Terrestrial and Aquatic Wildlife on the reproductive outcome of both species in Research (ITAW) University of Veterinary Europe is rare, and mostly reaches back to Medicine Hannover, Foundation, Germany before the millennium. However, both species *email: [email protected] do have larger litter sizes and might reproduce

Received: 19 June 2019 / Revised: 21 August 2019 / Accepted: 4 all year round, which is not yet confirmed for all September 2019 / Published online: 5 September 2019. Ministry of habitats. The environmental impact of invasive Sciences, Research and Technology, Arak University, Iran. alien species (IAS) ranges from a mere nuisance Abstract in private gardens up to severe damage to In this study, we focus on literature dealing with protective dikes and a reduction in biodiversity differences in habitat use, environmental in several countries. The management of IAS is impact, reproductive output, and management cost-intensive and differs widely among states. strategies concerning nutria and muskrat in Europe in general and in Germany in particular. Keywords: Coypu, Environmental impact, What is the current knowledge about these habitat, management, muskrat, Myocastor species in European countries, and what coypus, nutria, Ondatra zibethicus, reproduction management strategies exist so far? We Introduction summarised more than 200 references on these Since the beginning of globalization a few topics using common scientific databases. In centuries ago, alien species have been their original distribution area, habitats suitable accidentally or deliberately taken to other for muskrats are characterized by low water continents. Some of these species have level fluctuations and sufficient small water established themselves in their new habitat over resources, large river banks, and adequate water time, which means that due to human activity (e. depths. In newly inhabited areas, different g., targeted release, escape from breeding habitat structures are exploited, although an facilities), these species have settled outside aquatic environment is required. In Europe, the their natural range and formed autonomous presence of muskrats can lead to habitat changes populations of so-called alien species. When and consequently, to biodiversity loss. Overall, populations of these species cause economic muskrats are regarded as generally being able to damage or pose a significant threat to native cope well with changing habitat conditions. biodiversity as they spread, they are called Feeding on crops merely seems to be a behavior invasive alien species (IAS) (Vitousek et al. restricted to new settlements in both nutrias and 1997, Nehring et al. 2015). muskrats. Nutrias, too, often achieve a reduction There are many reasons for the invasiveness of in plant diversity in the habitat through their species. It is often noticed that an invasive choice of food in the newly populated areas. species behaves differently in its area of origin Additionally, an urban occurrence along with than in its new distribution area. Climate change sightings of the animals during the day is almost can also contribute to the proliferation of a exclusively observed in new habitats. species, for example, through mild winters Concerning the modeling of nutria population (Nentwig 2010). It was only in 1958 that Charles

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Elton followed the assessment of science in the The nutria and muskrat species are currently direction of critical invasion biology (Elton listed on the Union List of this Regulation 2000). However, even today, there are different (Implementing Regulation (EU) 2016/1141 and approaches in the field of biological invasion Implementing Regulation (EU) 2017/1263), and management. The tendency to accept alien both are considered established in Germany. species as a "symptom and witness of Species listed were identified as invasive by an anthropogenic environmental changes" is quite evidence-based risk assessment, in accordance pragmatic (Kowarik 2010), in some cases, one with prescribed criteria. Listing of a species can even speak of new ecosystems that have means it is banned from import, trade, come into being as a result (Hobbs et al. 2006). possession, breeding, transport, use, and release Nonetheless, important protected goods can be into the environment (Genovesi et al. 2015). In endangered, and enormous ecological Germany, the nutria is subject to the hunting consequences and economic losses arise laws of some of the Federal States (NJagdG (Pimentel et al. 2005, Vilà et al. 2010). Alien 2018). In Lower Saxony, hunting of muskrats is species are known to be an important driver of currently the responsibility of specially trained recent extinctions (Bellard et al. 2016). The muskrat hunters who, as employees of the majority of alien species in Germany are plants Lower Saxony Chamber of Agriculture, carry and insects, which represent two-thirds of the out the contractually agreed monitoring and approximately 2000 non-native species here control of the populations (Fritz and Röver (Nentwig 2010), not all of which are invasive. In 2016). the category of terrestrial vertebrates, the This review reveals intensive examination of European database DAISIE (Delivering Alien both species either by science, administration or Invasive Species Inventories for Europe, inhabitants, concerning completely different www.europe-aliens.org) lists the nutria and foci depending on area and species. Throughout muskrat in the top 100 of the worst invasive the review, it is the main aim to summarise species, thus representing two of the IAS that differences in habitat use, find information on cause significant ecological and economic harm. reproduction figures and compile the impacts on Originating from North (muskrat) and South the environment of both species. Additionally, (nutria) America, nutrias inhabit all continents papers on current management strategies are except Australia, Antarctica and New Zealand compared since it is our hypothesis that no (Carter and Leonard 2002), while muskrats were common strategy exists for Europe so far. introduced into most of the Palearctic, including Material and methods Great Britain, Northern and Central Europe, Between October 2017 and April 2018, we Ukraine, Russia, parts of China and Mongolia, searched for articles on Myocastor coypus and and Honshu Island in Japan as well as in South Ondatra zibethicus using electronic databases, America (Genovesi 2006). Due to their including Web of Science, Medline, Google semiaquatic way of life and intensive burrowing Scholar, and electronic union catalogs of the in river banks and dikes, the invasive nutria and University of Veterinary Medicine Hannover, muskrat species have gained immense Germany. Search terms included “Myocastor importance in Germany, where risk assessment coypus”, “coypu”, “Nutria”, “Ondatra already should have been completed (Ikeda zibethicus”, “muskrat”, “Bisam”, “Bisamratte”. 2006), and biodiversity loss and the threat to After compiling a bibliography of more than 200 protected goods (Nehring et al. 2015) certainly articles traced through the database search, we pose an immense risk. acquired additional information using reference Within the framework of the EU biodiversity tracing, focusing on articles that discussed strategy, Regulation 1143/2014 was adopted, in Myocastor coypus and Ondatra zibethicus which measures to combat IAS are presented. distribution, reproduction, control, management

3 | Journal of Wildlife and Biodiversity 4(2): 1-12 (2020) or eradication. Besides, as far as possible, vegetation in swamp areas, the opposite was the contact was made with experts responsible for case with increased muskrat occurrence (Nyman the particular animal species in Germany in et al. 1993, Shaffer et al. 2015). In prediction particular or Europe in general to integrate any models, the temperature was considered as a relevant grey literature into the study, which significant factor for the spread and settlement consisted of very few institutional reports and of nutrias. The occurrence of frost days (<0°C final theses. Throughout the study, the main minimum, <5°C maximum (Gosling 1981)) was questions concerning both species comprised: assumed to impede the survival of the animals. Are there differences in habitat use in original Several scientists combined models to make habitats compared to newly adapted habitats? reliable predictions of nutria distribution What is the reproductive output of both species? (Doncaster and Micol 1989, Guichon et al. What is the impact on the environment in newly 2003b, Sheffels 2013, Jarnevich 2017). Based adapted habitats, and which kind of on current weather trends and hydrological management strategies are considered? processes, new settlements of nutrias could be Results detected early and invasions could be prevented Nutria habitat use (Sheffels 2013, Jarnevich 2017). For example, In the wet grasslands of the Argentine pampas, the northwest of Iran proved to be a suitable nutrias mostly stay close to the water and favour distribution area for nutrias, representing foraging on grazing areas, despite neighbouring approximately 35% of the country's area agricultural landscapes, which was confirmed (Farashi and Shariati Najafabadi 2015). by faecal analyses. Since these results are partly Nutrias are predominantly nocturnal in their contrary to observations in Europe, it is native range (Palomares et al. 1994), which was discussed whether possible causes are based on also documented for invasive nutrias by English the utilisation possibilities of resources or and American studies (Chabreck 1962, Gosling ecological interactions in the newly populated 1979, Gosling et al. 1980), and explained areas (D'Adamo et al. 2000). Aquatic and mainly with predator avoidance behaviour, semiaquatic food sources may be preferred over whereby deviations from the nocturnal activity terrestrial plants, which might be due to a cost- are known at food shortage and high population benefit principle and reduce the risk of density (Chabreck 1962). In Germany, however, predation. A further explanation for the it has been shown that nutrias tend to have conflicting experiences, especially in Europe, diurnal activity in urban areas, especially when where nutrias are sometimes regarded as a threat fed by humans (Meyer et al. 2005). High to crops, could be the different structure of activity during daytime has also been observed habitats since many European agricultural areas in various suburban areas of Oregon, USA are close to the waterways populated by nutrias (Sheffels 2013). and therefore easier to reach (Borgnia et al. Muskrat habitat use 2000, Guichon et al. 2003a). In addition, a Studies on habitat use usually refer to current reduced suitability of the new habitats is landscape changes or adaptation abilities of the assumed (Scheide 2012). animals. For example, authors from Illinois, The sparse occurrence of indigenous nutrias in USA, report that muskrat populations have to urban and semi-urban areas may be due to switch to habitats where unstable water levels increased hunting pressure on animals there can occur due to the running dry of wetlands and (Leggieri et al. 2011). The effect on vegetation stream control. Radio-telemetric studies on diversity and herbivore density in the swamps of these animals showed that they mainly fed on Louisiana, USA, differs between nutrias and riparian vegetation and stayed close to the muskrats. While nutria occurrence negatively riverbanks instead of visiting higher-lying affected biodiversity and species richness of the agricultural areas (Ahlers et al. 2010a).

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Subsequently, the authors investigated the and other predators of invertebrates are also effects of unstable water levels on the risk of considered problematic (Nummi et al. 2006). In local muskrats being predated during higher Sweden, muskrats seem to be the main food for water levels. Ultimately, the animals were more foxes, so that a predator-prey relationship is exposed to predators, especially along the upper assumed (Danell 1978, Danell 1985). reaches of the rivers. However, this did not In Poland, the long downward trend of the result in a higher mortality rate, as the main muskrat hunting bag is in contrast to the increase predator, the American mink, only hunted at in the hunting bag of the likewise occurring lower water levels. A positive correlation mink and also points to a predator-prey cycle between the survival rate of muskrats and bank (Brzezinski et al. 2010). width, especially in small rivers and agricultural In the Russian biosphere reserve, Prioksko- ditches, was discovered (Ahlers 2010, Ahlers et Terrasnyi, the influence of muskrats on the al. 2010b). Additionally, a positive correlation ecosystem is assumed to be insignificant due to between muskrat occurrence, precipitation and their limited occurrence (Bobrov et al. 2008). water depth was observed. Muskrats were Reproduction increasingly encountered on wide rivers with Indigenous nutria populations reproduce all year higher banks and in urban regions, where trap round, with the main reproduction period being hunting and higher levels of low tide were in the summer. In males and females, sexual presumably predominant (Cotner and Schooley maturity is reached at a body weight of 3 kg. The 2011). survival rates do not differ significantly between In Canadian swamps, locations with 10 cm the seasons here. In comparison, indigenous water depth minimum and deposits of reed nutria populations seem to mature more slowly (Typha spp., Scirpus spp.) are regarded as a and have a lower body weight than established preferred habitat and food source depending on populations in the USA and Northern Europe, muskrat density (Clark 1994). In these habitats, which the authors attribute mainly to the cold too, flooding has an indirect negative influence winters in Europe (Guichon et al. 2003b). on muskrat density, as it has reduced emerging In the 1970s, a study in England confirmed a vegetation (Clark and Kroeker 1993). relationship between the amount of body fat of In Germany and the Netherlands, it is assumed females in winter and the number of reproducing that muskrats leave their areas seasonally, for females in the following spring. There is a instance, during the main migration seasons in significant, inverse correlation of both body fat spring and autumn (Böhmer et al. 2001). and reproduction in spring that provides the Research on the biodiversity of swamp ponds in hypothesis that cold winters cause a critical the Netherlands has shown that, in addition to nutritional situation of the animals which results many habitat characteristics (such as turbidity, in a reduced number of litters in the population water depth, nutrients and sulphate T (Gosling 1981, Gosling et al. 1983). Brown concentration), the presence of muskrats also (1975) calculated an average litter size of 5.75 plays a role: Higher muskrat density seems to with a range of 3 to 12 foetuses for nutria reduce plant diversity (Sarneel et al. 2011). populations living in Florida, USA. Female and Foraging on shellfish can lead to a serious threat male animals reproduced all year round, of rare species in small areas (Stemmer 2017). according to histological ovarian and sperm A reduction in plant diversity and a change in examinations. With a gestation period of abiotic conditions and existence of native approximately 134 days, female animals could invertebrates in muskrat habitats also is reported produce up to 2.7 litters per year (Brown 1975). from North America and Argentina (De Szalay In a French study, no juveniles could be and Cassidy 2001, Silva and Saavedra 2008, observed during the wintertime. However, a Skinner and Skinner 2008). The effects on fish parturition peak was reached during the early

5 | Journal of Wildlife and Biodiversity 4(2): 1-12 (2020) summer (Doncaster and Micol 1989). A nutrias. A high percentage of the country is decrease in population density after severe located below sea level, which makes the winters is confirmed in Mediterranean areas preservation of dikes even more important. A (Reggiani et al. 1995). Food restriction could professional hunting system is implemented have a direct influence on the ovarian secretory with the help of 400 full-time professional activity of nutrias, so that fertility could also be trappers on behalf of the state, which includes directly influenced in the case of food shortages both a dense trapping network and active (Sirotkin et al. 2000). hunting. Nutrias are caught mainly with wire Puberty of muskrats generally starts at four to box traps that can also be installed on rafts six months of age, and gestation usually takes (Waterschappen 2017). 25-30 days (Beer 1950, Reeves and Williams Since muskrats have been caught all year round 1956, Donohoe 1966). Studies in East Germany for years, and evaluation of alternative strategies in the 1950s assume a gestation period of 28 should clarify whether, for example, a temporal days and the age of reaching sexual maturity to or a spatial adaptation of the hunting actions can be five months. The average litter size of free- be helpful. Using a population model, Bos and living populations in East Germany was 6.8, Ydenberg (2011) showed that there are reaching a maximum of ten. The author differences in the efficacy of strategies. postulates that up to five litters per year may be However, more information is needed on the accomplished and that young animals of the first costs of harvesting for each method. litter can already participate in reproduction up Great Britain eliminated the muskrat species as to twice a year (Hoffmann 1958). Muskrats in early as 1939 in the course of the first muskrat Northern Europe seem to have smaller litters and nutria eradication campaign using snap and might have adapted a shorter reproduction traps. However, the trapping method included time to weather conditions, resulting in lower high by-catch rates (Gosling and Baker 1989). overall reproduction rates (Danell 1978, Hjältén In accordance with the FACE (Federation of 1991). Associations for Hunting and Conservation of Environmental impact and management the EU) guidelines for catching muskrat, the strategies spring and autumn migration of animals must be In Germany, damage to agricultural land near used for intensified catching (FACE 2013). watercourses is observed due to nutrias foraging The successfully implemented eradication on roots or tubers, digging and partial collapse program in the UK may serve as a model for of dams and dikes, damage to softwood, and European management plans. After an initial foraging in allotments. Increased feeding of failed experiment in the 1960s (Norris 1967), a nutrias can lead to water pollution in urban areas population of about 3000 adult female nutrias (Biela 2008, Scheide 2012, Nehring et al. was reduced to 20 animals between 1981 and 2015). Reed beds (Typha spp.), which serve as 1986. The extinction was facilitated by breeding habitats for black terns (Chlidonias coincidental severe winters. The operation, niger), can be severely damaged by nutrias originally planned over a ten-year period, cost at (Vossmeyer et al. 2016), as well as freshwater least £ 2.5 million (Gosling and Baker 1987). A mussel populations (Anodonta cygnea, Stemmer cost evaluation of the harmful effects of nutrias 2017). The digging of both nutrias and muskrats in Italy distinguishes between agricultural poses a serious risk to the stability of dams and damage, damage to river banks, prevention and dikes (Burghause 1996, Böhmer et al. 2001, management measures, with nutria occurring in Reinhardt et al. 2003, Nehring et al. 2015). 75% of Italy's regions. While the cost of damage In the Netherlands, the purpose of management amounts to tens of millions of dollars, the is to significantly minimize the number of national campaign cost several millions of euros muskrats and simultaneously eradicate invading without the actions that have taken place in a

6 | Journal of Wildlife and Biodiversity 4(2): 1-12 (2020) concerted manner. The authors propose vegetation may be protected by plastic tubes researchers and managers to approach (LeBlanc 1994, Sheffels 2013). management strategies via cost-benefit analyses As a general conclusion of many studies, the within the context of different ecological and lack of concerted management in experiments economic settings (Panzacchi et al. 2007). In on nutria reduction is obvious (Kuhn and addition, better coordination between Peloquin 1974, Sheffels and Sytsma 2007, Hong neighbouring countries and import bans for et al. 2015). areas not yet populated are recommended Research on nutrias and muskrats reveals (Bertolino and Genovesi 2007). fundamental differences in the use of habitat in The coastal wetlands of Louisiana, southern US native and newly adapted ranges, respectively. state on the Gulf of Mexico, serve as essential This is in line with the behaviour and ecology of habitat for nutrias in North America. Since alien species, forming one of the main problems 2001, damage caused by this species has led to when the species is considered invasive (Wright a continuous loss of marshland. The Coastwide et al. 2010, Kumschick et al. 2015, Bellard et Nutria Control Program (CNCP) was developed al. 2016). Knowledge of reproductive ecology as a result of this. Implemented methods include is an important part of scientific evaluation of trapping and shooting animals with shotguns or population growth and essential for developing rifles (Normand and Manuel 2016). management plans. Especially for IAS, Maryland, a US state on the Atlantic coast, also reproductive ecology might differ from what is hosts important nutria populations near the established or known about native species (Koen Chesapeake Bay. The Chesapeake Bay Nutria et al. 2018, Ramírez‐García et al. 2018). The Eradication Project, which was launched in impact of IAS on the environment ranges from 2002, pursues a systematic hunting concept, economical to ecological threats of different developing novel methods for collecting and degrees. Whereas in Germany, the risk eliminating nutrias. Conibear traps, leghold assessment was carried out by the Federal traps and snares are used alongside box traps and Agency for Nature Conservation (Nentwig positioned on paths frequented by the animals. 2010) without the concern of management By-catches were minimized by specific implications, international approaches of manipulation of the traps (Kendrot 2011). In the scientists include data-based risk analyses to northwest of the USA, damage to agriculture, include and improve further management tools dikes, banks and dams dominates, depending on (Early et al. 2016, Booy et al. 2017, Carboneras different habitat types in the south of the United et al. 2018, Roy et al. 2018). States (Meyer 2005, Sheffels and Sytsma 2007, According to several studies, different Sheffels 2013). prerequisites are necessary for the complete In some studies, habitat adaptation is proposed eradication of an already widespread species. to prevent nutria colonization. In addition to Thus, a very early stage of invasion or a spatial well-drained field areas, a bank slope of less limitation (insularity) can favour eradication than 45° is regarded as an obstacle; in areas with (Robertson et al. 2017). Particularly successful adjustable water levels, a lowering of the level was the eradication of domestic and migratory in summer (supporting emigration) and an rats (Rattus rattus, Rattus norvegicus) on increase in winter (deterrence by exposure to Mediterranean and US islands, as a result of cold water) are helpful (Peloquin 1968, LeBlanc which the vulnerability of some breeding birds 1994). Wire mesh fences and electric fences have declined significantly (Genovesi 2005, prevent the settlement and entry of garden areas. Witmer et al. 2011). To successfully eliminate Metal wrapping of the trunk is suitable for established species, sufficient financial protecting individual trees. Seedlings in woody resources, clear responsibility of authorities with sufficient support of the general public, as well

7 | Journal of Wildlife and Biodiversity 4(2): 1-12 (2020) as successful trapping or hunting techniques Acknowledgments must be made available. Besides, reinvasion This study was funded by the Ministry for must be ruled out and, if necessary, the Nutrition, Agriculture, and Consumerism of ecosystem must be restored (Myers et al. 2000). Lower Saxony through the financial resources of A feasibility study on the eradication of the hunters of Lower Saxony and the Hunters Australian "pest animals" stipulates clear Association of Lower Saxony, Germany. conditions: 1) the rate of removed animals must exceed the reproduction rate, 2) the immigration References rate must be zero, 3) all reproducing animals Ahlers A. A. 2010. Survival and space use of must be targeted. Furthermore, eradication is riparian muskrats (Ondatra zibethicus) only considered a preferred option if 1) the within an agroecosystem. The University of animals can be found at low densities, 2) a cost- Illinois at Urbana-Champaign, Illinois. benefit analysis has shown that eradication is Ahlers A. A., Heske E.J., Schooley R.L., indeed preferred over a control measure, and 3) Mitchell M.A. 2010a. Home ranges and an appropriate, supportive socio-political space use of muskrats Ondatra zibethicus in environment prevails. Since these criteria are restricted linear habitats. Wildlife Biology rarely met in existing widespread species, 16:400-408. regional eradication would rarely be considered Ahlers A. A., Heske E.J., Schooley R.L., (Bomford and O’Brien 1995a;b), and complete Mitchell M.A. 2010b. Effects of flooding extinction of IAS in new habitats is hardly and riparian buffers on survival of muskrats possible (Koike et al. 2006). A thorough (Ondatra zibethicus) across a flashiness evaluation of cost-benefit-ratios for the different gradient. Canadian Journal of Zoology- management options in each country is essential to evolve a professional, scientifically supported Revue Canadienne De Zoologie 88:1011- management for the further handling of IAS in 1020. Germany and the rest of Europe. Beer J. R. 1950. The reproductive cycle of the muskrat in Wisconsin. The Journal of Wildlife Management 14:151-156. Bellard C., Cassey P., Blackburn T. M. 2016. Conclusion Alien species as a driver of recent When dealing with management implications, extinctions. Biology letters 12.2:20150623. knowledge of current IAS reproduction rates is Bertolino S., Genovesi P. 2007. Semiaquatic essential. Information on sexual maturity and mammals introduced into Italy: case studies th litter sizes relies on studies of the 20 century, in biological invasion. 175-191 in Gherardi so that especially in newly inhabited areas, F. Biological invaders in inland waters: current research would be appropriate. The Profiles, distribution, and threats. Springer management strategies of countries are closely Netherlands, Dordrecht. connected with the damage caused by nutrias Biela C. 2008. Die Nutria (Myocastor coypus and muskrats and therefore range from local Molina 1782) in Deutschland – prevention measures, e.g., in private gardens, up to habitat adaption, e.g., by water level Ökologische Ursachen und Folgen der adjustment and intensive hunting. Since Ausbreitung einer invasiven Art. Lehrstuhl eradication can only be achieved in countries für Landschaftsökologie der Technischen without re-immigration (Robertson et al. 2017), Universität München, appropriate management plans have to prioritize Wissenschaftszentrum Weihenstephan, actions, including a cost-benefit analysis (Booy München. et al. 2017, Roy et al. 2018).

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