Eurasian otter Lutra lutra in developing countries: a resurvey of 22 years after the fall of communism

A LESSANDRO B ALESTRIERI,SIMONE M ESSINA,FRANCESCA P ELLA C LAUDIO P RIGIONI,NICOLA S AINO and M AURO F ASOLA

Abstract In countries with emerging and developing econ- persistent organic pollutants, especially synthetic pesticides omies the need to promote development and the lack of in- (lindane, DDT) and chlorinated biphenyls (Ruiz-Olmo formation on the status of the Near Threatened Eurasian et al., ). otter Lutra lutra have given rise for concern about the con- Although most industrially developed countries have servation status of the species. In Albania information about made progress in controlling pollution and implementing the distribution of this otter dates from .In we re- conservation measures, in transitional or developing econ- surveyed  sites previously surveyed in , and a further omies biodiversity governance is hindered by ongoing insti-  sites throughout the country. At each site nine habitat tutional change and the need to promote economic variables of potential importance to otters were recorded development, which often result in overexploitation of natu- and analysed. Overall the distribution pattern in  did ral resources (CEC, ; Kluvánková-Oravská et al., ). not differ from that recorded in , although a reduction Approximately % of the countries within the Eurasian in marking intensity suggested a possible decline in otter otter’s range have been listed as emerging and developing numbers. Distribution of the otter has been influenced by economies by the International Monetary Fund (IMF, land use and human density, suggesting man-induced habi- ), and the species’ population trend in the eastern part tat changes since the fall of communism may have affected of its range was the basis for its categorization as Near the quality and fragmentation of otter habitats. Threatened on the IUCN Red List in  (Ruiz-Olmo et al., ). Keywords Albania, distribution, Eurasian otter, habitat Information about the current status of the species in change, Lutra lutra, monitoring, standard survey, tran- many developing countries is scarce. Although the otter sitional countries population is increasing in Poland (Romanowski, ) This paper contains supplementary material that can be and may not have declined in Hungary during the second found online at http://journals.cambridge.org half of the th century (Heltai et al., ), the species has reportedly declined in Turkey (Kayaöz, ; Özdemir, ), the South Caucasus region (Georgia, Armenia and Azerbaijan; Gorgadze, ), Belarus Introduction (Sidorovich, ), Nepal (Bhandari, ) and Morocco (Delibes et al., ). ollowing a dramatic decline in both range and popu- In Albania the communist era ended in . The tran- lation in the second half of the th century, the F sition from centralized management of land and natural Eurasian otter Lutra lutra is recovering in several resources to a market-oriented economy has caused wide- European countries, including the UK (Crawford, ), spread damage to the environment (Jansen et al., ), Sweden (Roos & Rigét, ), Denmark (Elmeros et al., especially to aquatic ecosystems of the western lowlands, ), France (Janssens et al., ), Spain (Ruiz-Olmo & as a result of increased urbanization, overexploitation of Delibes, ) and Italy (Prigioni et al., ). This recovery woodland and ineffective waste management (Cullaj et al., is probably largely attributable to efforts in the s to ban ; Keukelaar et al., ). Except for a few more recent surveys in the southern part ALESSANDRO BALESTRIERI (Corresponding author) and NICOLA SAINO Department of the country (rivers and ; Bego et al., ; of Biosciences, University of Milan, Via Celoria 26, 20133 Milan, Italy Hysaj et al., ), information about the distribution of E-mail [email protected] the otter in Albania dates back to , when during – SIMONE MESSINA Department of Biology and Biotechnology, Sapienza University,  Rome, Italy May Prigioni et al., surveyed sites, mostly in the western lowlands and in the upper catchment of the River FRANCESCA PELLA IUCN, Rruga Abdi Toptani, Torre , Tirana, Albania (Prigioni et al., ). The rationale for the survey method CLAUDIO PRIGIONI and MAURO FASOLA Department of Earth and Environmental ’ Sciences, University of Pavia, Pavia, Italy was based on Erlinge s recommendations; stretches of river up to  m long were surveyed for otter spraints Received  July . Revision requested  September . Accepted  October . First published online  February . and footprints on both banks (Chanin, ). A minimum

Oryx, 2016, 50(2), 368–373 © 2015 Fauna & Flora International doi:10.1017/S0030605314000921 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.219, on 30 Sep 2021 at 14:18:12, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605314000921 Eurasian otter in developing countries 369

coastal lagoons (Butrinti, Narta, Ceke, Merxhani, Patok, Viluni; Peja et al., ). Mean transect length was  m (range – m). The most thoroughly surveyed catch- ments were those of the rivers Shkumbin (n = ), Vjosa (n = ), (n = ) and Ishëm- (n = ); relative to their total length, few sites were located in the catchments of the rivers where otter occurrence had been confirmed recently. All sites were georeferenced using a global posi- tioning system. To avoid bias as a result of variation in ex- perience with sampling, all surveys were carried out by the same trained staff. Sprainting sites were identified as places with spraints se- parated by at least  m from other spraints (Kruuk et al., ). Following Prigioni et al. () an index of otter marking intensity was calculated as the number of spraint- ing sites or spraints per  m. We assumed marking intensity represented a broad index of relative abundance (Mason & Macdonald, ). The percentage of sites where otters were present in  was compared to that  found in  (χ test), with respect to both the total number of sites (n = ) and the number of sites surveyed in both years (n = ). For the latter sample the distribution of sites with presence and absence was compared using a  ×  summary table of coincidences and discrepancies. For each site on a watercourse five habitat variables of potential importance to otters (Prenda et al., ; Remonti et al., ) were recorded visually in the field (Supplementary Table S). Watercourse width and depth FIG. 1 Sites surveyed for the Eurasian otter Lutra lutra in were estimated at intervals of c.  m and the mean values Albania in . Filled and unfilled circles indicate otter presence for each site were assigned to one of four classes (# ., .– and absence, respectively. ., .–. or . . m, and # ., .–., .–. or . . m, respectively). Water speed was categorized as stag- nant, slow or moderate–high. The dominant land use within  distance of m was surveyed per site and the otter a  m wide belt on both river banks was estimated and ca- was presumed absent if no sign was detected along the tran- tegorized as bare soil, crops, pasture/shrubs or woods. sect. To update information on the distribution of the Water pollution was categorized as absent (transparent Eurasian otter in Albania and to assess the impact of water in $ % of watercourse depth, without any sign of ’ political and economic changes on the species conservation pollution), low (less transparent water, solid waste on the by comparing current and past range, we resurveyed the banks), medium–high (clear signs of pollution, such as major watercourses and coastal lagoons of Albania in bad smell, turbidity, foam). Mean altitude was recorded  summer . for each site (# , –, –, .  m). To assess the influence of human disturbance on otter occurrence,    Methods using GE-Path v. . . (Sgrillo, Ilhéus, Brazil), we assessed the overall percentage cover of agricultural and urban  Following the same protocol used by Prigioni et al. (), areas in a  km area centred on each site, by superimposing during  June– July  we resurveyed the  sites sur- a  ×  m grid on satellite images provided by Google veyed in , and an additional  sites, thus surveying all Earth (Google, Mountain View, USA). Results were categor- the major river catchments of Albania (Fig. ). We used a ized as # , .–, .– or . %.  : , road map to select sites, which were chosen for Otter presence/absence was then modelled against the ease of access, mainly at road bridges, to maximize the prob- predictor variables by backward stepwise logistic regression, ability of finding signs quickly (Chanin, ). Sites were using Wald’s test to examine the statistical significance of separated by at least  km. Twenty-nine sites were on each coefficient in the model. To avoid collinearity, which main rivers,  on tributaries, seven on canals, five on can inflate the standard errors of the estimates of model lakes (Shkodrës, Ohrit, Vaut të Dejës, Fierzes) and six on coefficients and produce unreliable results (Hosmer &

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Lemeshow, ), the correlation between the predictors TABLE 1 Otter Lutra lutra mean marking intensity along seven was measured by Spearman’s coefficient. Model variables major rivers in Albania (Fig. ), and at all sites surveyed for otters    were then selected, omitting those that represented redun- in (Prigioni et al., ) and (blank cells indicate unsur- dant information; when two variables were correlated veyed sites). (P , .), the one to be rejected was chosen according to 1985 2013 the strength of its correlation with the dependent variable. Sites per Spraints per Sites per Spraints per Analyses were performed only for sites on watercourses, River 200 m 200 m 200 m 200 m as most habitat variables could not be assessed precisely Drin/Buna 0.8 0.8 0.4 0.4 for lakes and lagoons. Mat 3.6 5.8 1.0 1.4 Finally, from the last human population census Shkumbini 0.7 2.6 0.8 1.1 (INSTAT, ) we obtained the population density (inhabi- / 0.7 2.6  tants per km ) of the counties (qarku;n=) and municipa- Dunacecit lities where sampling sites were located. For sites in the same Vjosa 0.7 2.6 administrative area the results were pooled to avoid pseu- Shushice 0.9 1.1 Bistrice 3.3 7.3 doreplication (Hurlbert, ), and mean values for positive – All surveyed 1.7 3.6 0.78 1.1 and negative sites were compared using the Mann Whitney sites test. The relationship between marking intensity and either altitude or population density was examined using ’ Spearman s correlation test. municipalities was significantly lower for sites where otters were present than sites where they were absent (. vs .  inhabitants per km ;U=,P=.). Results

Otter signs were detected at  (.%) of the  survey sites. From north to south, the species was widespread in the Discussion catchments of the rivers Drin, Mat, Shkumbin and Seman (where the otter occurred in the plain of Coriza) and absent The distribution of the otter in Albania in  was similar on the rivers Gjanica and Vjosa. Otter signs were not found to that recorded by Prigioni et al. ()in. Otters were in the downstream stretches of the rivers Shkumbin, Seman absent on the coastal stretches of the rivers Gjanica, Seman and Vjosa, which cross the intensively populated plain fa- and Vjosa, where oil extraction and refinement remain the cing the . No otter sign was found in the catch- primary source of water pollution (Cullaj et al., ), ments of the rivers Ishëm (which runs through the counties whereas urban and industrial waste, together with increased of Durazzo) or Tirana and Bistrice, in the south, whereas urbanization, probably prevent colonization of the catch- otter presence was detected at one of four sites in the catch- ments of the rivers Ishëm and Erzen. The largest difference ment of the River Erzen (Fig. ). Otters were present in five was recorded in the River Bistrice, the river with the highest of six lagoons and in the Lake of Ocrida (Ohrit), and absent marking intensity in , where otters are now absent from from the Lake of Scutari (Shkodrës) and two of three arti- two of three sites where they were present in . In a report ficial lakes (Liqueni Fierzes and Liqeni i Vaut të Dejës). by the Government of Albania, direct killing has been indi- The percentage of surveyed sites where otters were cated as the main threat to otters in the Southern Coastal present did not differ from that recorded in the  survey Plain, but the River Bistrice has been canalized for much  (. vs .%; χ = .,P=.), even considering only the of its length and the whole watershed area has been  sites surveyed in both years (. vs .%; χ = ., degraded by uncontrolled urbanization (PAP/RAC- P=.). The distribution of presence and absence was SOGREAH, ), suggesting that habitat alteration may also similar: otter status in  was the same as in  have been a significant factor in the decline of the otter.  for % of sites (χ = .,P=.). In contrast, marking Although no habitat variable seemed to affect distri- intensity was lower in  than in  (Table ). bution at a local scale, confirming that otters are tolerant Logistic regression identified percentage cover as the of a wide range of habitat conditions (Chanin, ), at main variable affecting the occurrence of the otter the landscape scale the effect of land use and human popu- (Table ). Pecentage cover was negatively correlated with lation density may be regarded as an index of the impact of mean altitude (ρ = −.,P=.,n=) and positively human activities on otter occurrence. Similarly, on the correlated with water pollution (ρ = .,P=., Iberian Peninsula otter distribution was reported to be affec- n=). ted by human variables such as distance to major urban cen- Marking intensity was not correlated with any of the tres and to highways, which were related to water pollution variables tested. Mean human population density of downstream (Barbosa et al., ).

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TABLE 2 Results of backward stepwise logistic regression with otter presence/absence as the dependent variable and five habitat variables of potential importance to otters as independent variables.

Variables B2 Wald statistic df P Exp(B)3 % cover1 0.021 ± SE 0.008 7.207 1 0.007 1.022 Constant −1.487 ± SE 0.508 8.564 1 0.003 0.226

  % cover of agricultural and urban areas in a  km area centred on each survey site  Logistic coefficient  Odd ratios

Although there is no direct relationship between numbers of The otter is still widespread in Albania, and effective pol- spraints and numbers of otters, sprainting activity reflects lution management policies may favour the reinforcement changes in the distribution of otters (Chanin, )andin- of otter populations in the future, as has occurred in several creases with otter numbers (Lanszki et al., )andhabitat European countries (Ruiz-Olmo et al., ). As shown by use (Clavero et al., ). In general, – m surveys are the systematic monitoring of otter populations in the UK effective for ascertaining otter presence (Chanin, ); to assess (e.g. Strachan, ), annual otter surveys, complemented marking intensity, however, constant-length surveys are recom- by effective statistical analysis of pollution data collected mended (Balestrieri et al., ). Nonetheless, the numbers of by environment protection agencies, can identify habitat spraints and sprainting sites did not differ from those recorded changes and guide conservation programmes. in surveying a  km stretch of the River Drinos (Hysaj et al., ), and corresponded to those reported for peripheral areas of the otter’s range in Italy (Prigioni et al., ; Balestrieri et al., Acknowledgements ). Although two surveys are insufficient to assess any This study was conducted within the framework of the In- trendintheotterpopulationinAlbania,variationinmarking stitutional Support to the Albanian Ministry of Environ- intensity suggests that changes in socio-economic policies dur- ment, Forest and Water Administration (MoEFWA) for ing – may have had a greater impact on otter numbers Sustainable Biodiversity Conservation and Use in Protected than on the large-scale distribution of the species. Areas project by IUCN, funded by the Italian Ministry of During the early transitional period from communism to Foreign Affairs, General Directorate for Cooperation Devel- democracy, lack of control and effective management poli- opment, in collaboration with MoEFWA. We thank the cies exacerbated the environmental problems inherited project manager, Andrea Ghiurghi, for supporting and facil- from the previous centralized planning political model. itating the research, and the trainees of the Animal Ecology Privatization of land has led to the urbanization of plains Units of IUCN’s project, specifically Tonin Macaj, Eduard and the conversion of land-use from broadleaved forests Gajtani, Zeqir Ujka, Festim Broja and Elvin (APA to herbaceous crops in hilly areas, with detrimental effects Shkoder) of the Buna River Protected Landscape, and on the environment (Jansen et al., ). Uncontrolled fish- Lavdim Qoshi, Enver Koçi, Mitat Bicaku (Librazhd Forest ing, deforestation, river-bed excavation and pollution of riv- Office), Eriola Katjai, Luljeta Koçi and Bledar Pepa ers by wastewater from tanneries and petroleum refineries (Elbasan University), and Bledi Oxha (PPNEA NGO) of are still considered major threats to the otter (Cullaj et al., Shebenik–Jabllanice National Park. We thank Etleva Hysaj ; Hysaj et al., ). The burning of urban waste in and Ferdinand Bego for help with fish identification and the open air is the main contributor of PCDD/PCDF (poly- promoting research on otters in Albania. Lesley C. Wright chlorinated dibenzo-p-dioxin and dibenzofuran) emissions (IUCN Species Survival Commission Otter Specialist into freshwater (Kleger et al., ). Group) and Prof. Christopher F. Mason kindly revised the Nonetheless, since the beginning of the st century there English. has been increased awareness of environmental problems, and some progress has been made in policy and legislation. A National Strategy and Action Plan for Biodiversity was References approved in , and in  the otter was included in

the Red Data Book of Albanian fauna, categorized as BALESTRIERI, A., REMONTI,L.&PRIGIONI,C.() Detectability of Vulnerable (Cullaj et al., ; Hysaj et al., ), although the Eurasian otter by standard surveys: an approach using marking it can still be hunted under permit, to prevent damage to intensity to estimate false negative rates. Naturwissenschaften, , – fisheries. The Stockholm Convention was signed in  . BALESTRIERI, A., REMONTI, L., SMIROLDO, G., PRIGIONI,C.& and a National Implementation Plan for the reduction REGGIANI,G.() Surveying otter Lutra lutra distribution at the and disposal of persistent organic pollutants was approved southern limit of its Italian range. Hystrix, The Italian Journal of in . Mammalogy, , –.

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A. Balestrieri & L. Remonti). Hystrix, The Italian Journal of STRACHAN,R.() National Survey of Otter Lutra lutra Distribution Mammalogy, Supp (), . in Scotland –. Scottish Natural Heritage Commissioned RUIZ-OLMO,J.&DELIBES,M.() La nutria en España ante el Report No.  (ROAME No. FAC). SNH, Inverness, Scotland. horizonte del año . SECEM, Málaga, Spain. RUIZ-OLMO,J.,LAFONTAINE,L.,PRIGIONI,C.,LÓPEZ-MARTÍN,J.M.& SANTOS-REIS,M.() Pollution and its effects on otter Biographical sketches populations in south-western Europe. In Proceedings of the First Otter Toxicology Conference (eds J.W.H. Conroy, P. Yoxon & A.C. ALESSANDRO BALESTRIERI and CLAUDIO PRIGIONI’s research Gutleb), pp. –. International Otter Survival Fund, Isle of Skye, activities focus mainly on the behavioural ecology and conservation Scotland. of meso-carnivores. They are also involved in the management of in- RUIZ-OLMO, J., LOY, A., CIANFRANI, C., YOXON, P., YOXON, G., vasive coypus in northern Italy. SIMONE MESSINA participated in this DE SILVA, P.K. et al. () Lutra lutra.InIUCN Red List of research for his undergraduate thesis. FRANCESCA PELLA is involved Threatened Species. Http://www.iucnredlist.org [accessed  April in conservation research, wildlife management, and capacity building ]. in developing countries. NICOLA SAINO’s main research interests are SIDOROVICH,V.() Recent strong decline in otters Lutra lutra in sexual selection, the evolution and consequences of maternal effects, Belarus: the data gained and hypothesis established. In XIth parent–offspring communication and sex allocation, and the impacts International Otter Colloquium (eds C. Prigioni, A. Loy, of climate change on migration phenology and population dynamics. A. Balestrieri & L. Remonti). Hystrix, The Italian Journal of MAURO FASOLA’s research interests range from demography and for- Mammalogy, Supp (), . aging ecology of birds, to behaviour of reptiles, environmental con- tamination, and phylogeography.

Oryx, 2016, 50(2), 368–373 © 2015 Fauna & Flora International doi:10.1017/S0030605314000921 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.219, on 30 Sep 2021 at 14:18:12, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605314000921