Non-Invasive Genetic Mark-Recapture as a Means to Study Population Sizes and Marking Behaviour of the Elusive Eurasian Otter (Lutra lutra)

Quantifying population status is a key objective in many ecological studies, but is often difficult to achieve for cryptic or elusive species. Here, non-invasive genetic capture-mark-recapture (CMR) methods have become a very important tool to estimate population parameters, such as population size and sex ratio. The Eurasian otter (Lutra lutra) is such an elusive species of management concern and is increasingly studied using faecal-based genetic sampling. For unbiased sex ratios or population size estimates, the marking behaviour of otters has to be taken into account. Using 2132 otter faeces of a wild otter population in Upper Lusatia (Saxony, Germany) collected over six years (2006–2012), we studied the marking behaviour and applied closed population CMR models accounting for genetic misidentification to estimate population sizes and sex ratios. We detected a sex difference in the marking behaviour of otters with jelly samples being more often defecated by males and placed actively exposed on frequently used marking sites. Since jelly samples are of higher DNA quality, it is important to not only concentrate on this kind of samples or marking sites and to invest in sufficiently high numbers of repetitions of non-jelly samples to ensure an unbiased sex ratio. Furthermore, otters seemed to increase marking intensity due to the handling of their spraints, hence accounting for this behavioural response could be important. We provided the first precise population size estimate with confidence intervals for Upper Lusatia (for 2012: N^ = 20 ± 2.1, 95% CI = 16–25) and showed that spraint densities are not a reliable index for abundances. We further demonstrated that when minks live in sympatry with otters and have comparably high densities, a non-negligible number of supposed otter samples are actually of mink origin. This could severely bias results of otter monitoring if samples are not genetically identified.     

Body temperature and foraging behaviour of the Eurasian otter (Lutra lutra), in relation to water temperature

The effects of water temperature (T_w) on core body temperature (T_b) and foraging behaviour were studied in four free-ranging and one captive otter Lutra lutra in NE Scotland. The free-ranging animals were observed in and around two freshwater lochs, and measurements were made of T_w (2–16°C), T_b at the beginning and end of swimming bouts, lengths of swimming bouts, and dive times and intervals. T_b ranged from 35.9 to 40.4°C (mean 38.1°C). At the beginning of a period of activity and of a swimming bout. T_b rose significantly; during swimming it fell at a rate of 2.3°C/h, independent of T_w. Dive intervals were longer in colder waters, but this was probably due to other, seasonal environmental changes (perhaps water level). T_w had no significant effect on length of swimming bouts or on T_b. Although otters entered water with increased T_b, they exited when T_b was not significantly different from the mean resting T_b. The data suggest that otters maintain T_b irrespective of T_w, by increasing it before entering water, then either exiting at a given T_b, or at an earlier time determined by other environmental conditions.     

Genetic variability and size estimates of the Eurasian otter (Lutra lutra) population in the Bohemian Forest Ecosystem

Even though recent years have shown a slow recovery of the Eurasian otter (Lutra lutra) populations from their previous lows, the species is still highly endangered in most parts of its European distribution range. Surprisingly, only a few studies have so far assessed the species’ genetic variability and population density, and they have mostly been carried out only in small territories. In Germany, most otter populations live in protected areas whose management urgently needs data on population sizes and densities as well as on genetic variability of the species under their custody. Thus, we analyzed genetic variability and assessed size and density of the otter population in the Bohemian Forest Ecosystem, an area that had not been included in the few previous molecular studies. The study area comprised of 1500 km², divided into fifteen squares of 10 × 10 km², each of which was sampled in two collection periods. Overall we collected 261 fecal samples (spraints), of which 60 (23%) could be genotyped at least at eight microsatellite loci, yielding 38 distinct otter genotypes. The low genotyping success rate was the result of high ambient temperature at the time of sampling rather than that of high humidity. The population did not show signs of a past bottleneck, indicating a small yet stable population size. Population size was estimated to be 118 (CI_95% 64–163) individuals, with a mean density of 1 animal per 8.5 km² or 3.1 km river length. Our results imply that hunting, requested by local fishpond owners, should remain banned to avoid a decline in (effective) population size.     

Habitat factors and the presence or absence of otters Lutra lutra in Denmark

The purpose of the present study was to examine the relative influence of different habitat factors on ottersLutra lutra (Linnaeus, 1758) and to develop a predictive model to better understand the distribution of the otter in Denmark. During the National Otter Survey in 1991 data were collected on 19 variables which reflected aspects of habitat structure, composition, organic pollution and human disturbance. Multiple logistic regression analysis was used to estimate probabilities of the presence of otters as a function of one or more explanatory variables. Six variables (county, pH, water depth, presence of trees, bottom substrate and Saprobien-Index) were identified. In Denmark, otter habitat typically consists of water courses with depths > 1 m over a varied bottom, with pH > 7.0, Saprobien-Index on II–III to III (indicating slight organic pollution) with no trees on the banks. Some of these variables reflect highly productive waters. The use of the otter as an indicator of good water quality and/or aquatic habitat should be used with care.     

Seasonal and area-related variations in the diet of otters Lutra lutra on Mull

The diet of otters Lurra lutrn living in a sea loch on the Isle of Mull was described by means of spraint analysis. Seasonal and spatial differences in the spraint composition were explored in the context of fluctuations in prey availability, as revealed by trapping. Butterfish Pholis gunnellus and the cottids Myoxocephalus scorpius and Taurulus bubalis were the most commonly occurring prey in spraints. In the winter, the proportion of rocklings ( Ciliata spp. and Gaidropsarus spp.) and non-rockling gadoids (Gadidae) in the diet increased. Their relatively large size makes these latter species an important constituent of the winter diet. Seasonal and spatial variation in fish consumption largely reflected fluctuations in availability. The mean size of principal prey fishes in spraints was similar to that observed in the traps. These observations suggest that otters were not strongly selective with regard to fish species and size. Shore crabs, in contrast, were not taken in proportion to availability. The findings are discussed in the light of other studies of the diet of coastal otters. It is suggested that the lack of selectivity demonstrated in this study, compared with previous studies, may be explained by area-related variations in prey availability.     

Assessing range re-expansion and recolonization of human-impacted landscapes by threatened species: a case study of the otter (Lutra lutra) in Italy

Detecting and understanding recoveries of threatened species from past and recent presence/absence data is essential to improving conservation efforts. However, false positive trends may be reported because of false absences in past data, therefore appropriate testing is needed. We tested an expansion/recolonization of the otter (Lutra lutra) populations in Italy from a fragmented distribution outlined in the 1984–1985 period by using Monte Carlo simulations. Land-use changes, human depopulation and decrease in influence of anthropogenic features were investigated as potential drivers of recolonization by using GIS modeling. A survey of the entire Italian range of the otter, conducted in 2002–2004, recorded a 2.2-fold increase in the proportion of occupied 10-km squares and 49 local colonizations. The range size and proportion of urban land-use in the 1984–1985 distribution were smaller (P < 0.05) than those derived from simulated surveys based on 49 random false absences versus colonization events. The distribution range expanded southward and nearly reached the southern margins of the peninsula. Recolonization of moderately urbanized landscapes was not accompanied by human depopulation. According to partial logistic regressions, the pure effect of urban land proportion and industry proximity on otter occurrence probability declined by about 48%, suggesting a decreased impact on the stream habitat. Conversely, natural factors, increased in importance by about 116%. The absence of a significant northward expansion in the 20 year period suggests that northward habitat restoration should be planned to encourage further recolonization. On the other hand, potential urban threats in the newly occupied landscapes should be controlled.     

The Smell of New Competitors: The Response of American Mink, Mustela vison, to the Odours of Otter, Lutra lutra and Polecat, M. putorius

We tested the response of wild American mink (an established alien species in the UK), to the odours of unfamiliar mink, European polecat and Eurasian otter. Polecats are similar in size and habits to mink, otters are larger than mink and a dominant competitor; both are native to the UK and both were absent during the original colonization by mink but are now undergoing natural population recoveries. The response of mink to experimental odours was assessed by counting the numbers of tracks (footprints) on rafts treated with anal gland secretions, and compared with response to a control raft, on two rivers in the Upper Thames valley, UK. Remote video showed that the number of tracks was positively correlated with the time that mink spent investigating an odour. We found that mink were attracted to the odours of both unfamiliar mink and polecats. There was little evidence that mink avoided the odour of otters. We suggest that, during an encounter with a polecat, mink may behave much as they would to a conspecific. We infer from the response of mink to the odour of otters, that, if mink do avoid otters, the mechanism of avoidance is likely to be complex, situation-dependent and perhaps affected by prior experience.     

Genetic consequences of population decline in the European otter (Lutra lutra): an assessment of microsatellite DNA variation in Danish otters from 1883 to 1993

The European otter (Lutra lutra) was common in Denmark until the 1960s, but its present distribution encompasses only a minor part of the country. The aim of this study was to assess whether the recent population decline has resulted in loss of genetic variability and to gain further insight into the dynamics of the population decline. This was done by analysing microsatellite DNA variation in contemporary and historical samples, the latter encompassing DNA samples extracted from museum specimens covering a time-span from the 1880s to the 1960s. Tests for differences in expected heterozygosity and the numbers of alleles in contemporary versus historical samples and a test for detecting population bottlenecks provided few indications of a recent bottleneck and loss of variability. However, a procedure for detecting population expansions and declines, based on the genealogical history of microsatellite alleles, suggested that a drastic long-term population decline has taken place, which could have started more than 2000 years ago, possibly due to ancient anthropogenic pressure. Finally, assignment tests and pairwise F(ST) values suggested weak but statistically significant genetic differentiation between the extant population and historical samples of otters from other regions in Denmark, more likely reflecting differentiation among original populations rather than recent drift.     

Mitochondrial DNA variation in the European otter (Lutra lutra) and the use of spatial autocorrelation analysis in conservation

To add genetic information to the international conservation efforts on European otters Lutra lutra, we investigated the genetic population structure in and around a known "source" population of the otter, the Oberlausitz (OL) in eastern Germany. This was complemented by a first survey of genetic variation levels in the Central European otter population. Sequence analysis of 300bp of the mitochondrial control region in 76 specimens from the eastern German study region and 53 individuals from several other European populations revealed a low level of genetic variation, with only 5 haplotypes present and nucleotide diversities within populations ranging from 0.00% to 0.17%. Apart from eastern Germany, one haplotype was by far the most abundant one, from which other, only locally occurring types, could be derived by a single point mutation. This suggests a single Pleistocene refugium from which the analyzed European regions have been reinvaded after the glaciations. Within eastern Germany, two abundant haplotypes were found. Their occurrence differed significantly among subregions of eastern Germany. The uneven distribution of a locally restricted but abundant haplotype could be explained by isolation-by-distance and might reflect emigration from the OL source population to surrounding regions. This suggests that vital local populations can indeed serve as "sources" for the invasion of surrounding areas. Given a suitable genetic marker, we suggest a spatial autocorrelation analysis to monitor the genetic effect of such an emigration from a source population.     

Variation in cranial form and sexual dimorphism among five European populations of the otter Lutra lutra

Craniometric variation between otters Lutra lutra (L.) from Ireland, Scotland, Shetland, Norway, and Czechoslovakia was examined using multivariate statistical analyses. Significant sexual dimorphism in cranial size and shape occurred in all samples, although the degree of dimorphism varied between samples, with the Irish sample exhibiting the most. Morphological differences were also observed across samples. Three groups were observed; Irish, Scottish, (Mainland and Shetland), and Mainland European, though within the two composite groups the samples were still differentiable. There was a good agreement between the patterns of variation between male and female samples, but morphological differentiation was not significantly correlated with geographic separation. These results are discussed in the light of our current knowledge of the ecology of the species in Europe. It is argued that, while there is morphological evidence for subspecific status of the Irish otter (as L. l. roensis ), further investigations of morphological and genetic variation across Eurasia are clearly required.     

Sexual dimorphism in the skull of minks Mustela vison, badgers Meles meles and otters Lutra lutra

Multiple-group principal component analysis and discriminant analysis were used to investigate the morphological differences between adult skulls of male and female minks, badgers and otters from Norway. The first principal component axis, calculated from the variance-covariance matrix of log-transformed data, was interpreted as a growth-free size axis in all three species, while the other components were interpreted as representing shape. Having largely separated size and shape variation, these two aspects of sexual dimorphism could be studied. The standardized component scores were subjected to an analysis of variance and discriminant analyses were performed on size-in and size-out data. Sexual dimorphism was disclosed on eight of the 12 components in minks and on seven of the 12 components in badgers and otters. In mink the multivariate differences were more due to size than to shape, whereas in badgers and otters most of the multivariate differences were due to shape, but the differences in size were also significant. The shape dimorphism was shown to be functionally related to jaw and neck muscles. The results were discussed in relation to recent theories to explain the evolutionary significance of sexual dimorphism in body size of mustelids. It was concluded that these theories do not fully explain the dimorphism found in the skulls of the moderately dimorphic badger and otter.     

Craniometrical variability and developmental stability. Two useful tools for assessing the population viability of Eurasian otter (Lutra lutra) populations in Europe.

Morphometrical univariate analyses of otter skulls collected over the past hundred years in European countries from presumed healthy populations were compared with skulls from presumed endangered populations. The average degree of sexual dimorphism of die European populations was found to be directly correlated to die skull size of die male otters. Fluctuating asymmetry (FA) in metric skull traits was analysed as an estimator of developmental stability. There was evidence for increased FA in different traits over time in some of the presumed endangered populations, and for a reduction in size of skull traits. In contrast, the healthy populations did not show any significant changes in the same traits during the same period. The reduced sexual dimorphism of the endangered populations is suggested to be a product of relaxed sexual selection and deteriorated habitat conditions. Environmental and genetic forces that may have shaped these patterns are discussed.     

Body size changes among otters, Lutra lutra, in Norway: the possible effects of food availability and global warming

Using museum data of adult specimens whose sex, age, and locality are known, we studied temporal and geographical body size trends among the otter, Lutra lutra, in Norway. We found that body size of the otters increased during the last quarter of the twentieth century, and suggest that this trend is related to increased food availability from fish farming and possibly also to energy saving due to elevated sea temperatures. Birth year and death year explained 38.8 and 43.5%, respectively, of the variation in body size. Body size of otters was positively related to latitude, thus conforming to Bergmann’s rule.     

Individual identification and sex determination of Eurasian otters (Lutra lutra) in Daegu city based on genetic analysis of otter spraint

The Eurasian otter, Lutra lutra, is a well known endangered species in South Korea that experienced rapid population decreases through poaching and industrialization until the 1980’s. To evaluate the genetic diversity and the existing number of otters recently found in Daegu City, 81 fecal samples collected from the Gumho River and Shincheon stream were subjected to DNA extraction for sex determination and genetic analysis using nuclear genetic markers. Individual identification and relatedness between individuals were detemined by genotypic data using twelve microsatellite loci, and sex identification was also determined based on sequence variation of the zinc finger protein gene on sex chromosomes. Our results showed that at least seven otter individuals were identified and the kinship relationships of seven individual pairs were determined. It was concluded that otters distributed widely in Daegu City have moderate levels of genetic diversity, and close monitoring of the small-sized otter population is necessary to promote successful settlement of the otters in the area.     

Trophic flexibility of Eurasian otter (Lutra lutra) in Anzali Wetland,Iran, assessed by fecal and stable isotope analysis

Aquatic Ecology - Information on the feeding habits of species is essential to develop appropriate conservation actions. This study aimed to assess spatial and temporal variation in the diet of the...     

Individual identification and distribution assessment of otters (Lutra lutra) through non-invasive genetic sampling: Recovery of an endangered species in the Basque Country (Northern Spain)

Non-invasive genetic techniques have proven to be cost-effective for monitoring and studying otter populations, largely due to the linearity of otter territories and the marking behavior of the species. After a severe decline, in the 60, the Eurasian otter is recovering in the Iberian Peninsula. However, the recovery pattern is not homogeneous and the species is still considered “Threatened” in many regions. During 2007–2010 a systematic non-invasive genetic sampling effort was carried out to determine the spatial distribution and to estimate the population size of an endangered otter population in northern Iberian Peninsula (Basque Country). Samples were identified to species level by sequencing a 226 bp mtDNA fragment prior to genotyping. Among the 132 obtained samples, 127 (98.4%) belonged to the study species, one sample was genetically identified as European mink (Mustela lutreola) and one as American mink (Neovison vison) while genetic species confirmation was not possible in the three remaining samples. These results provided novel and accurate data on species distribution, highlighting an overall increase of 25% in 10 × 10 UTM grids occupied by otter and a clear pattern of re-colonization upstream of the main rivers. All samples corresponding to otter were subsequently individually genotyped using a novel multiplex panel of 11 microsatellite markers and sexed by typing the sex-chromosome-related gene ZFX/ZFY. We obtained a complete individual genetic profile for 55 samples (genotyping success 43%), corresponding to 20 different individuals (11 females, 6 males, and 3 individuals of unknown gender). The mean otter density in occupied areas estimated to be 0.09 (0.06–0.12) individuals per river kilometer. The present study enabled us to obtain updated and relevant information about this elusive species’ distribution and population size, essential to define population status and to design successful and effective management and conservation programs.     

Social learning and the development of individual and group behaviour in mammal societies

As in human societies, social learning may play an important role in shaping individual and group characteristics in other mammals. Here, we review research on non-primate mammals, concentrating on work at our long-term meerkat study site, where longitudinal data and field experiments have generated important insights into the role of social learning under natural conditions. Meerkats live under high predation pressure and occupy a difficult foraging niche. Accordingly, pups make extensive use of social information in learning to avoid predation and obtain food. Where individual learning is costly or opportunities are lacking, as in the acquisition of prey-handling skills, adults play an active role in promoting learning through teaching. Social learning can also cause information to spread through groups, but our data suggest that this does not necessarily result in homogeneous, group-wide traditions. Moreover, traditions are commonly eroded by individual learning. We suggest that traditions will only persist where there are high costs of deviating from the group norm or where skill development requires extensive time and effort. Persistent traditions could, theoretically, modify selection pressures and influence genetic evolution. Further empirical studies of social learning in natural populations are now urgently needed to substantiate theoretical claims.     

A genetic analysis of group movement in an isolated population of tree-roosting bats

Group fission is an important dispersal mechanism for philopatric adults. In Cypress Hills Interprovincial Park, Saskatchewan, tree-roosting big brown bats (Eptesicus fuscus) exhibit fission-fusion roosting behaviour. During 2004-2007, the majority of females previously resident to roosting area 1 (RA1) moved to a new roosting area (RA4). We examined how genetic relationships, inferred from data for microsatellite loci and mitochondrial DNA, influenced new roost area (RA) selection during 2006 when colony members were split between the RAs. We found that females who moved to RA4 had higher average relatedness than those that remained in RA1. We found that nearly all females belonging to matrilines with high average relatedness moved to RA4 while females from matrilines with low average relatedness were split between the two RAs. These results suggest that closely related maternal kin preferentially move to new RAs. However, daily roosting preferences within a RA are not based on genetic relationships probably because daily roosting associations between kin and non-kin are used to ensure adequate roost group size. Studying the effects of kinship on the fission and movements of groups not only enhances our understanding of social behaviour and population genetics but also informs conservation decisions.