Prey Habitat Engineering for an Introduced, Threatened Carnivore Can Support Native Biodiversity

Short Communication A paradox of restoration: prey habitat engineering for an introduced, threatened carnivore can support native biodiversity

L IINA R EMM,ASKO L ÕHMUS and T IIT M ARAN

Abstract Conservation of charismatic vertebrates in mod- reconstruction of habitats be based on a suite of focal species ern landscapes often includes habitat engineering, which sensitive to each threat. Hobbs et al. () suggested is well supported by the public but lacks a consideration that traditional habitat restoration needs to be replaced of wider conservation consequences. We analysed a pond by an approach that maintains ecosystem services in management project for an introduced island population human-impacted environments by means of various inter- of captive-bred, Critically Endangered European mink ventions. Thus, if sustaining a threatened species is desirable Mustela lutreola. Ponds were excavated near watercourses either for its surrogate or public-perceived values, it may be in hydrologically impoverished forests to support the acceptable to engineer critical characteristics of its degraded main prey of the mink (brown frogs Rana temporaria and habitat beyond the natural range of variability. It is less clear, Rana arvalis). A comparison of these ponds with other, nat- however, to what extent such practices support the wider ural, water bodies revealed that the (re)constructed ponds aims of biodiversity conservation. could reduce food shortages for the mink. Moreover, the Here we explore a situation in which management for a ponds provided habitat for macroinvertebrates that were threatened flagship species has gone beyond conventional uncommon in the managed forests in the study area, includ- habitat restoration. The target species, the European mink ing some species of conservation concern. The cost- Mustela lutreola, is a Critically Endangered mustelid threat- effectiveness of the management of charismatic species ened by habitat loss and the impact of the alien American can be increased by explicitly including wider conservation mink Neovison vison (Maran et al., ). Balancing these targets at both the planning and assessment stages. threats, the Foundation Lutreola and Tallinn Zoo estab- lished a mink population in , using captive-bred indi- Keywords Amphibians, Estonia, focal species, habitat deg-  viduals, on the remote Estonian island of Hiiumaa ( km , radation, macroinvertebrates, Mustela lutreola, Odonata, % forest cover; Fig. ). The island has no historical records pond management of this species but the abundance of farm-escaped American This paper contains supplementary material that can be mink (now eradicated and the farm closed), combined with found online at http://journals.cambridge.org field assessments of riparian areas, suggested a potential car- rying capacity for – European mink (Macdonald et al., ; Maran & Põdra, ). The main limiting factor is the abitat management for charismatic threatened species sparse network of natural streams and a severe reduction of His a common conservation activity, and it is important lakes and pools as a result of artificial drainage and lowering to understand the contribution this makes to wider bio- of the water level for forestry and agriculture (Veering, diversity conservation at the scale of species and ecosystems. ). Riparian areas are the main habitat of the European In addition, the consequences of species-oriented habitat mink, which normally stays within  m of streams management can inform debates on the efficacy of surrogate (Danilov & Tumanov, ). Although larger ditches species (Caro, ) and realistic goal-setting in restoration could provide alternative habitat, drainage has presumably ecology. The concept of surrogate species was linked expli- reduced the mink’s prey base, notably the brown frogs Rana citly with habitat management for threatened species by temporaria and Rana arvalis (Suislepp et al., ; Põdra Lambeck (), who suggested that the conservation or et al., ). Improving the prey base via large-scale hydro- logical restoration would have been complicated, and artifi-

LIINA REMM (Corresponding author) and ASKO LÕHMUS Department of Zoology, cial ponds were therefore constructed. Here, we explore Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise Street whether these artificial ponds supported not only the 46, EE-51014 Tartu, Estonia. E-mail [email protected] mink’s prey but also other native macroinvertebrates.  TIIT MARAN Institute of Veterinary Medicine and Animal Sciences, Estonian Twenty-three small (–, m ) ponds were con- University of Life Sciences, Tartu, Estonia, and Species Conservation Lab, Tallinn Zoological Gardens, Estonia structed or reconstructed in forests and meadows.  Received  January . Revision requested  February . The ponds were c. m deep, to provide an environment Accepted  March . First published online  September . suitable for amphibian tadpoles up to the completion of

Oryx, 2015, 49(3), 559–562 © 2014 Fauna & Flora International doi:10.1017/S0030605314000271 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 30 Sep 2021 at 01:03:35, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605314000271 560 L. Remm et al.

FIG. 1 Locations of (re)constructed ponds and other water bodies and of water bodies suitable for the European mink Mustela lutreola on Hiiumaa island (Põdra & Maran, ). The landscape units were differentiated based on types of relief, dominant soils, vegetation, Pond in forest movement of water and land use  Pond in meadow (Arold, ). On the inset the location of Hiiumaa island is Mink habitat indicated by the black circle, the areas shaded dark grey depict where Transects, with locations wild European mink may still of water bodies sampled survive and the areas shaded light 10 km grey where the species possibly went extinct in recent times in Borders of landscape units Europe (modified from Maran et al., ).

metamorphosis, with a shallow northern bank to provide samples per km; this resulted in a total sample of  water sun-warmed water. The ponds were ,  km (usually bodies along five transects. As for the (re)constructed much closer) from the streams suitable for the mink ponds there was a total of  seconds of sampling in each. (Fig. ), to aggregate its prey and facilitate movement of We used a rapid assessment strategy for identification of R. temporaria to winter habitat in stream bottoms. We macroinvertebrates. We determined all species of Clitellata, focus on  forest ponds, excavated during –.In Gastropoda, Araneae, Amphipoda and Odonata of later late spring  we determined the presence of amphibian developmental stages; remaining individuals were identified larvae (with  sweeps of a triangular net of  cm side to family. We tested for difference in family-level compos- and . mm mesh), sampled macroinvertebrates ( ×  sec- ition between the (re)constructed ponds and other water onds in different parts of the pond, using a  ×  cm, . bodies using multi-response permutation procedures mm mesh D-frame net) and determined the characteristics (Sørensen dissimilarity), and distinguished the taxon groups of the ponds. In addition, – of these ponds were surveyed contributing to that difference using indicator species ana- for amphibian spawn in April of –. We measured lysis (Dufrêne & Legendre, )inPC-ORD v. . water depth in the middle (mean of three measurements), (McCune & Mefford, ). To establish differences in habi- pH (using a Lutron PH- meter), and proportions of sur- tat characteristics we used Mann–Whitney U tests with the face in shade and of different bottom substrates (estimated Bonferroni correction. visually by the same person). All  (re)constructed ponds surveyed in April were used Similar procedures were used for other, natural, water by brown frogs for breeding at least once during –. bodies, some of which were artificial but not created specif- Mean average occupancy was % for R. temporaria and ically as wildlife habitat, sampled in May  along  km of % for R. arvalis. In nine of the ponds we found tadpoles transects (eight transects, stratified by landscape units, with during late spring searches in . Other breeding amphib- random starting points and in cardinal directions; Fig. ). We ians included common newt Lissotriton vulgaris (in six  mapped all water bodies that were .  m on a -m wide ponds; adults additionally in five ponds) and common toad  transect strip or .  m on a -m wide transect, and dip- Bufo bufo (in one pond). We found brown frogs breed- netted in each of them for amphibians. In water bodies $  ing in only two of the other water bodies (a ditch and a  cm deep or $  m in size we also dip-netted for macro- wheel-rut pool). invertebrates. To avoid pseudoreplication we treated similar The (re)constructed ponds contained more sand/clay on adjacent water bodies as one and collected no more than five the bottom and were deeper, less acidic and less shaded than

TABLE 1 Characteristics of the  (re)constructed ponds and  other water bodies (Fig. ), and Mann–Whitney U tests for differences.

Water body characteristics Mean, (re)constructed ponds Mean, other water bodies1 U P Peat & mud (% of bottom) 21 32 75 0.215 Sand & clay (% of bottom) 44 6 34.5 0.001* pH 6.9 5.9 42 0.006* % surface in shade 33 60 49 0.015* Depth (cm) 98 17 8 ,0.001*

 Weighted by macroinvertebrate sampling duration. *Statistically significant after Bonferroni correction.

the other water bodies (Table ). Macroinvertebrate assem- addition to monitoring, this should include a critical assess- blages differed significantly between the (re)constructed ment of the management techniques used and of the alter- ponds and other water bodies (multi-response permutation natives (see also Koper & Schmiegelow, ). For example, procedure: A = .,P, .). Twenty-three families re- a habitat-based alternative to increase the amphibian popu- corded in the (re)constructed ponds were not found in the lations in Hiiumaa would have been large-scale blocking of other water bodies, and eleven families were significantly artificial drainage (H. Drews, pers. comm.), with possibly more common in the (re)constructed ponds (indicator spe- even wider benefits for other aquatic biota, including the cies analysis; Supplementary Table S). Dragonflies and European mink (Fournier et al., ). damselflies were found only in the (re)constructed ponds, including two species of European conservation concern: Aeshna viridis (Sahlén, ) and Nehalennia speciosa Acknowledgements (Bernard & Wildermuth, ). (Re)constructed ponds appeared generally more suitable for the taxa requiring semi- Permissions for the population and habitat management permanent or permanent water, such as the water spider were provided by the National Environmental Board and Argyroneta aquatica, hemipterans, and several species of the management was performed in accordance with the pulmonate water snails. The assemblages in the other national action plan for the European mink. Financial sup- water bodies contained more hydrophilous terrestrial taxa, port was provided by the Environmental Investment Centre, such as land snails (some of which were possibly captured the Estonian Science Foundation (grant ), the Estonian from emergent vegetation) and mosquito larvae (Culicidae). Ministry of Education and Science (project SFs) These observations suggest that habitat engineering for and the European Union through the European Regional a threatened charismatic carnivore also created habitat for Development Fund (Centre of Excellence FIBIR). We less conspicuous species. The taxon groups that appeared thank T. Torp, M. Vaikre, H. Timm, T. Timm, M. Martin to benefit from the creation of ponds were uncommon in and M. Meriste for help with macroinvertebrate identifica- the surrounding forest landscape, which had been impover- tion, R. Rannap for fieldwork guidance, and two anonym- ished by long-term drainage, and some of these species are ous reviewers for comments. of wider conservation significance. Although the (re)constructed ponds served their primary aim (concentrating amphibians near mink habitat and thus probably improving References critical winter food for mink) there were probably too few  of them to significantly increase amphibian numbers at AROLD,I.( ) Estonian Landscapes: Factors of Landscape Formation and Landscape Investigation in Estonia. Landscape Regions. the scale of the island. However, the functioning of the University of Tartu, Tartu, Estonia. ponds as novel habitat for macroinvertebrates of semi- CARO,T.() Conservation by Proxy: Indicator, Umbrella, Keystone, permanent water bodies provides additional motivation Flagship, and Other Surrogate Species. Island Press, Washington, for such conservation activity. The few other studies of DC, USA.  this issue suggest that a range of other techniques can BERNARD,R.&WILDERMUTH,H.( ) Nehalennia speciosa.InThe IUCN Red List of Threatened Species v. .. Http://www. support biodiversity in anthropogenic landscapes: supple-    iucnredlist.org [accessed July ]. mentary feeding (Martín-Vega & Baz, ), nest-site provi- DANILOV, P.I. & TUMANOV, I.L. () The ecology of the European sioning (Heneberg, ) and, possibly, the control of exotic and American mink in the northwest of the USSR. In Ecology of predators (O’Donnell & Hoare, ) and diseases. Birds and Mammals in the Northwest of the USSR (ed. E.V. Ivanter), – The cost-effectiveness of the management of charismatic pp. . Karelian branch of Academy of Sciences of USSR, species can be increased by explicitly and routinely consid- Institute of Biology, Petrozavosk, USSR. [in Russian] DUFRÊNE,M.&LEGENDRE,P.() Species assemblages and ering positive and negative impacts on wider conservation indicator species: the need for a flexible asymmetrical approach. targets at both the planning and assessment stages. In Ecological Monographs, , –.

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