European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula

• 1 European rabbits are considered a keystone species in the Iberian Peninsula. Their populations have sharply declined over the past century, mainly due to habitat loss and the arrival of two viral diseases: myxomatosis in the 1950s and rabbit haemorrhagic disease (RHD) at the end of the 1980s. For the conservation of the Iberian Mediterranean ecosystem, it is important to determine whether rabbit populations are recovering two decades after the RHD outbreak, and to identify the factors associated with population recovery.
• 2 Here, we review the current knowledge on recent rabbit population trends in the Iberian Peninsula and the factors associated with these trends.
• 3 Although most rabbit populations are still declining in the Iberian Peninsula, a few seem to have recovered. In general, positive trends have been recorded in species‐friendly habitats characterized by non‐fragmented landscapes, interspersed patches of Mediterranean scrubland, good pastures and/or crops, soft soils that are suitable for warren construction and a Mediterranean climate with relatively high rainfall. Additionally, rabbits seem to be recovering better in areas where management practices (e.g. low hunting pressure, habitat management and predator control) are applied to increase their numbers.
• 4 From these findings, it is possible to identify five broad objectives for rabbit conservation in the Iberian Peninsula. First, it is clearly necessary to establish a long‐term programme for monitoring rabbit abundance and trends on a large scale. Second, the conservation and restoration of open Mediterranean scrubland should be a priority for stabilizing and maintaining existing healthy rabbit populations. Third, despite the lack of experimental evidence, management activities aimed at increasing the quantity and quality of both refuge and food should continue to be implemented. Fourth, legislation on the timing of the hunting season should be revisited following recommendations made by scientists. Finally, experimental approaches are required to investigate whether the control of generalist predators is a successful strategy to allow rabbit populations to recover.

     

Is the wild rabbit (<Emphasis Type="Italic">Oryctolagus cuniculus</Emphasis>) a threatened species in spain? Sociological constraints in the conservation of species

The Wild rabbit (Oryctolagus cuniculus) is an endemic species of the Iberian Peninsula and is essential for the conservation of endangered predators. Rabbits are also of high importance as a hunting species. From 1988, rabbits suffered the severe effects of rabbit hemorrhagic disease, which caused large declines in most populations. Despite this fact, the National Red Data Lists continued to classify rabbits as a “Least Concern” species. We used available hunting bag data from 1973 to 2002 to model national trends of rabbit abundance and to evaluate the conservation status according to the criteria of the National Red Data List and the World Conservation Union (IUCN). Generalized Additive Models were used as the statistical framework. The rabbit population of Spain suffered a large decline of about 71% between 1973 and 1993. This decline was 49% in the period 1980–1990. Based on both Spanish and World Conservation Union criteria, rabbits should be listed as ‘Vulnerable’, which demands a Conservation Plan Program. We suggest that the lack of concordance between the best available evidence and the conservation status of the species is a consequence of sociological constraints in conservation decisions. Rabbit conservation could face strong opposition from important socio-economic lobby groups (hunters and farmers). As such, governments and researchers may prefer to exclude rabbits from any status category requiring conservation action, despite the evidence of decline. We call for the urgent development of a nation-wide conservation program for rabbits which includes both socioeconomic constraints and the available biological data on population trends.     

Rabbit populations and game management: the situation after 15 years of rabbit haemorrhagic disease in central-southern Spain

Over recent decades wild rabbit populations have undergone a sharp decline in Spain with consequent negative impact both on a game-based economy, and on the conservation of threatened species that depend on rabbits. We investigated the relationships between rabbit population change and habitat and game management in central-southern Spain. To determine recent rabbit population changes we revisited 60 localities during summer 2002 to repeat surveys previously carried out in 1993. Each survey consisted of 4-km walked transects to record indices of rabbit abundance. The percentage of vegetation cover and of different soil types were also estimated during these transects. In the same areas, the type and intensity of game management practices were obtained by interviewing hunting managers, hunters or gamekeepers. Rabbit populations were stable or increasing only in 26.6% of the studied populations, more commonly in areas with soft soils where warren building is easier for rabbits and where rabbits were an important game species and managed to increase their numbers. Although we could not establish causality, habitat management and predator removal were the main management practices related to rabbit population change. Rabbit scarcity in Spain constitutes a serious problem for conservation, so hunters, researchers and policy makers need to reach a consensus to establish a long-term program to monitor rabbit population trends and share results obtained, especially when intense manage programs are being carried out to improve rabbit abundance.     

Influence of herbaceous cover,shelter and land cover structure on wild rabbit abundance in NW Portugal

The European wild rabbitOryctolagus cuniculus (Linnaeus, 1758) populations in the Iberian Peninsula has suffered a serious decline. Therefore, the knowledge about the factors that influence rabbit distribution and abundance is of major interest for conservation and management programmes. Rabbit relative abundance was evaluated by pellet counting in relation to herbaceous ground cover, shelter availability (tall scrub cover and gaps in rocks) and land cover structure in the Peneda-Gerês National Park (PGNP), NW Portugal. Rabbit abundance was higher at intermediate levels of herbaceous cover, but no significant statistical differences were detected. A strong association between the abundance index and tall scrub cover was verified, and when this cover was rare, an association with gaps in rocks was observed. At the land cover level, rabbit abundance was associated with high interspersion sites of rocks with matorral and high interspersion sites of tall scrubland. Evidence from this study highlighted the importance of shelter and the interspersion of open/shelter habitats for rabbits. This pattern could be interpreted as an anti-predator strategy. Therefore, management actions should favour the growing and establishing of tall scrub patches and the selective cutting in highly continuous areas of tall scrub vegetation.     

Restocking a keystone species in a biodiversity hotspot: Recovering the European rabbit on a landscape scale

Rabbit populations in Iberia remain at low densities in several areas in which their endangered predators still coexist, and the recovery of these populations is therefore urgent if the integrity of Iberian Mediterranean ecosystems is to be maintained. The enhancement of wild rabbit populations has been attempted through the use of in situ extensive rabbit captive breeding enclosures (restocking plots), which reduce mortality caused by terrestrial predators and dispersal movements and permit the breeding of young individuals which can then naturally disperse to settle in the surrounding areas. However, their effectiveness, the role of its size, the optimal habitat management that should be promoted around them and the habitat features remains uncertain. Here, we show results from a four year study of an ambitious rabbit restocking plan on a landscape scale. We measured rabbit abundance in a vast area in which thirty-two restocking plots were built to create an initial rabbit population for further dispersion, in addition to an intensive habitat management program. We also compared rabbit abundance between managed and unmanaged UTM cells of 2.5 km × 2.5 km. Our results showed that rabbit abundance was three times higher in managed cells, but four years after restocking, rabbit abundances had only reached the threshold needed to support stable Iberian lynx presence (at least 10 latrines per km^?1) in 9 of the 23 managed cells. Rabbit abundance was strongly affected by habitat treatment and scrub coverage. The increase of shelter was useful in low cover areas but ineligible in places with high scrub cover, where the increase of refuge plus scrub clearing to create pastures improve rabbit abundance more effectively. In the light of our results, restocking plots should be built only in places with suitable habitat, whereas pastures should be created in dense scrublands and refuge in low cover areas.     

Evolutionary history and molecular epidemiology of rabbit haemorrhagic disease virus in the Iberian Peninsula and Western Europe

Background  

Rabbit haemorrhagic disease virus (RHDV) is a highly virulent calicivirus, first described in domestic rabbits in China in 1984. RHDV appears to be a mutant form of a benign virus that existed in Europe long before the first outbreak. In the Iberian Peninsula, the first epidemic in 1988 severely reduced the populations of autochthonous European wild rabbit. To examine the evolutionary history of RHDV in the Iberian Peninsula, we collected virus samples from wild rabbits and sequenced a fragment of the capsid protein gene VP60. These data together with available sequences from other Western European countries, were analyzed following Bayesian Markov chain Monte Carlo methods to infer their phylogenetic relationships, evolutionary rates and demographic history.     

Hunting for answers: rabbit (<Emphasis Type="Italic">Oryctolagus cuniculus</Emphasis>) population trends in northeastern Spain

Some populations of European wild rabbit (Oryctolagus cuniculus) in Spain have recovered after rabbit hemorrhagic disease, but others (the majority) have not recovered. The European wild rabbit is a keystone species in Spain’s Mediterranean ecosystems, and several factors have been studied to determine what will stabilize populations and possibly propagate recovery. Many of the previous efforts to determine these pivotal factors have been short-term studies focused on few localities. Most management efforts and studies focused on the well-preserved habitats of southwestern Spain. Our objective was to examine spotlight counts from 60 localities over the past 13 years following the arrival of rabbit hemorrhagic disease in Aragón, northeastern Spain, to estimate rabbit population trends using linear regressions. The number of rabbits seen was transformed into a rough kilometric abundance index. With this data, we calculated a population trend index only for those localities with 6 or more years of data (n=42). No clear population trends were observed for the study period at a regional scale [±SE, range]; (0.065±0.081 from −0.860 to 0.915). We also examined factors that potentially influence regional rabbit population trends, including vegetation, topography, soil softness, climate, predator population trends, and hunting pressure. Our results indicate that rabbit trends have their strongest positive correlation with low hunting pressure and are negatively affected in areas of hard soils. In Aragón, the best populations of endangered raptors are concentrated in the Central Valley, which is the same area where rabbit populations are currently increasing.     

Seroepidemiology of rabbit haemorrhagic disease (RHD) in wild rabbits (Oryctolagus cuniculus) in the United Kingdom

An extensive collection of blood samples from adult wild rabbits, from areas where Rabbit Haemorrhagic Disease (RHD) had not been recorded, was obtained from sites across the U.K. and parts of Eire over the winter of 1994/95. Sera from 946 animals were examined for antibodies to RHD. Antibody was found in all populations, varying between 20 and 100% depending on locality, and overall 64% of rabbits were seropositive in midwinter, supporting the view that non-pathogenic RHD or RHD-like caliciviruses, which are not producing clinical disease, circulate within rabbit populations. The serological response to these agents appears to confer significant immunity on rabbits subsequently exposed to the virulent RHD virus, so the disease will not be as devastating as myxomatosis was in the early 1950s (99% mortality) but at least one-third of the c. 40 million rabbits in the U.K. are susceptible.     

Effectiveness of habitat management in the recovery of low-density populations of wild rabbit

Understanding the relationship between spatial patterns of landscape attributes and population presence and abundance is essential for understanding population processes as well as supporting management and conservation strategies. This study evaluates the influence of three factors: environment, habitat management, and season on the presence and abundance of the wild rabbit (Oryctolagus cuniculus), an important prey species for Mediterranean endangered predator species. To address this issue, we estimated wild rabbit presence and abundance by latrine counting in transects located in 45 plots within a 250?×?250 m grid from June 2007 until June 2009 in a 1,200 ha hunting area in southern Portugal. We then analyzed how wild rabbit presence and abundance correlate with the aforementioned factors. Our results showed that the main variable influencing wild rabbit presence and abundance was the distance to the artificial warrens. North and northeast slope directions were negatively related to wild rabbit presence. Conversely, rabbit presence was positively correlated with short distances to ecotone, artificial warrens, and spring. Regarding rabbit abundance, in addition to artificial warrens, soft soils, bushes, and season also had a positive effect. We found that environmental variables, management practices, and season each affect wild rabbit presence and abundance differently at a home range scale in low-density population. Thus, our major recommendations are reducing the distance to artificial warrens and ecotone, ideally to less than 100 m, and promoting habitat quality improvement on slopes with plenty of sun exposure.     

European rabbit research in the Iberian Peninsula: state of the art and future perspectives

The European rabbit (Oryctolagus cuniculus) is a high-profile prey, native from the Iberian Peninsula, the only region in the world where the two rabbit subspecies (O. cuniculus algirus and O. cuniculus cuniculus) currently co-exist in natural conditions. In this area, this important prey represents a keystone species and ecosystem engineer of Mediterranean landscapes, being also the most harvested and one of the most managed small-game species. Additionally, the species can create damage to crops in some parts of the Iberian Peninsula where it is regarded as an agricultural pest. The scientific interest towards the species is becoming increasingly apparent most likely as a repercussion of declining population trends over the last decades. The latter has been the result of the impact of habitat deterioration, viral diseases, unsustainable hunting, and predation. In this paper, I present a review of the scientific literature currently available on the European rabbit in the Iberian Peninsula. I discuss knowledge gaps and highlight priority research guidelines to suppress them, in an attempt to provide a general perspective to target research efforts more effectively. This analysis is particularly relevant due to the current vulnerability of rabbit populations in Iberia and to the recent news of cuts in scientific funding in most Mediterranean countries.     

Influence of habitat management on the abundance and diet of wild rabbit (<Emphasis Type="Italic">Oryctolagus cuniculus algirus</Emphasis>) populations in Mediterranean ecosystems

During the last decades wild rabbit (Oryctolagus cuniculus) populations have been progressively declining in the Iberian Peninsula as a result of several factors, namely habitat deterioration. Hence, habitat management has become one of the most commonly used management techniques to restore wild rabbit populations. To test the efficacy of some of these measures (creation of pastures, opening firebreaks) in rabbit populations, two managed (M1 and M2) and two control areas (C1 and C2) were selected in the Portuguese Southwest (SW) Coast. In each study area, the influence of habitat management was tested assessing temporal changes in rabbit abundance obtained from pellet counts and in rabbits’ diet through microhistological analysis of fecal pellets. Rabbit densities were higher in managed than in control areas (mean annual values: M1–1.08 pellets/m²; M2–1.60 pellets/m²; C1–0.69 pellets/m²; C2–0.40 pellets/m²). In general, Gramineae was the most consumed plant group throughout the year and in all study areas. In control areas, consumption of alternative species with low nutritive value (e.g., Cistus ladanifer) was observed, especially in summer. Our data suggest a positive influence of habitat management on rabbit populations since in managed areas individuals presented an overall higher abundance and a more nutritive diet. In addition, there was no evidence that sown species were consumed in detriment to naturally occurring grasses, suggesting that in Mediterranean semi-arid regions clearing vegetation inside the scrubland might be sufficient to improve habitat conditions for rabbits.     

Habitat management as a generalized tool to boost European rabbit Oryctolagus cuniculus populations in the Iberian Peninsula: a cost‐effectiveness analysis

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Rabbit (Oryctolagus cuniculus) abundance and protected areas in central-southern Spain: why they do not match?

European rabbits (Oryctolagus cuniculus), a keystone species in the Iberian Mediterranean ecosystem, are the staple prey of the Iberian lynx (Lynx pardinus) and the Spanish imperial eagle (Aquila adalberti). These predators require medium to high rabbit densities and a low degree of human disturbance. We compared rabbit abundances in areas of central-southern Spain under three levels of protection and management: protected areas, intensively managed (nonprotected) hunting estates, and other nonprotected areas. We used pellet abundance indices to estimate rabbit density in 118 surveys conducted during the summers of 2002 and 2003. We observed greater rabbit abundance in intensively managed hunting estates compared to protected areas and other nonprotected areas, perhaps because policy makers did not consider rabbit numbers when selecting priority areas. Alternatively, differences in game management practices (e.g., predator control or habitat management) may explain the higher rabbit densities observed in managed hunting estates. Our results suggest that the best feeding conditions for the Iberian lynx and the Spanish imperial eagle occur in intensively managed hunting areas, where such predators are frequently persecuted. The conservation of these endangered predators may require efforts to increase rabbit densities in protected areas.     

Effect of wildfires and post-fire forest treatments on rabbit abundance

One of the main factors involved in the decline in the European wild rabbit in the Iberian Peninsula is the loss of suitable habitats caused by abandonment of agricultural and grazing activities. Nowadays, Mediterranean landscapes suffer from wildfires that affect extensive areas and produce considerable habitat changes. However, little is known about the influence of wildfires and post-fire treatments on rabbit abundance to address policies to recover their populations. To do so, we studied abundances of this species in four types of plots during three consecutive years after a wildfire in Catalonia (NE Spain): (A) unburnt forests, (B) burnt forests with removal of burnt trees but with branches left, (C) burnt forests with removal of burnt trees and branches, and (D) non-forested burnt plots. Rabbits progressively colonised burnt plots, where their abundance increased for at least 5 years after the fire, but decreased or even disappeared in unburnt ones, indicating that forest fires have a positive effect on rabbit populations. Although abundances did not differ between the three burnt plot types, plots with removal of burnt branches had the highest increase in abundance. In addition, soil covered by branches or by dense vegetation appeared negatively correlated with abundance, indicating that this could hinder rabbit movements, while some plant species could benefit rabbits by providing high quality food. Thus, post-fire treatments favourable to rabbit populations might therefore be a good way of increasing the conservation and economic value of areas affected by forest fires.     

Extensive intragenic recombination and patterns of linkage disequilibrium at the CSN3 locus in European rabbit

Kappa-casein (CSN3) plays an important role in stabilising the Ca-sensitive caseins in the micelle. The European rabbit (Oryctolagus cuniculus) CSN3 has previously been shown to possess two alleles (A and B), which differ deeply in their intronic regions (indels of 100 and 1550 nucleotides in introns 1 and 4, respectively). Furthermore, a correlation between several reproductive performance traits and the different alleles was described. However, all these data were exclusively collected in rabbit domestic breeds, preventing a deeper understanding of the extensive polymorphism observed in the CSN3 gene. Additionally, the techniques available for the typing of both indel polymorphisms were until now not suitable for large-scale studies. In this report, we describe a simple, PCR-based typing method to distinguish rabbit CSN3 alleles. We analyse both ancient wild rabbit populations from the Iberian Peninsula and France, and the more recently derived English wild rabbits and domestic stocks. A new allele (C) showing another major indel (250 bp) in intron 1 was found, but exclusively detected in Iberian wild rabbits. In addition, our survey revealed the occurrence of new haplotypes in wild populations, suggesting that intragenic recombination is important in creating genetic diversity at this locus. This easy and low cost single-step PCR-based method results in an improvement over previous described techniques, can be easily set up in a routine molecular laboratory and would probably be a valuable tool in the management of rabbit domestic breeds.     

Influence of livestock,habitat type,and density of roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis>) on parasitic larvae abundance and infection seroprevalence in wild populations of roe deer from central Iberian Peninsula

Livestock farming is a common human activity that not only modifies natural habitat but also may lead to interactions with other wild animal species. We studied whether health status of roe deer (Capreolus capreolus) is influenced by density, livestock, and type of habitat. We analyzed 208 samples (120 fecal and 88 sera) from roe deer populations of central Iberian Peninsula to evaluate both presence and abundance of parasitic oocysts, eggs, and/or larvae, especially of gastrointestinal and bronchopulmonary parasites, as well as the prevalence of five infectious diseases (infectious bovine rhinotracheitis (IBR), pestivirosis (BVD/BD), paratuberculosis (PTB), bluetongue (BT), and brucellosis). Fecal samples were collected in transects in pine and oak forests and endoparasites were detected by means of coprological techniques. Serum samples were obtained from hunted individuals and the serological testing for the infectious pathogens was performed by ELISA and Rose Bengal tests. Livestock and habitat type were associated both with the presence and the number of bronchopulmonary nematode L1-larvae per gram of feces (lpg), which was higher in areas with livestock and in pine forests. However, roe deer density neither influenced parasite presence nor lpg values. Regarding infectious pathogens, only seropositive samples for PTB and pestivirus were obtained indicating a possible transmission between domestic and wild ungulates in the study area. The low prevalence found is consistent with other studies in the Iberian Peninsula suggesting that roe deer have little contact with the infectious agents studied. Our results highlight that both habitat type and livestock significantly mediate abundance of parasitic larvae in roe deer, being higher under competition scenarios and in habitats of lower quality, a valuable aspect to be considered in future management and conservation strategies.     

Biotic and abiotic factors modulating wild boar relative abundance in Atlantic Spain

The population dynamics of wild ungulates, particularly wild boar (Sus scrofa), are modulated by biotic (e.g. predation) and abiotic (environmental) determinants. Despite the evident potential interference of predation in the environmental patterns of wild boar population abundance, studies including both predation and abiotic factors are scarce. Here, using spatially explicit predictive models, we investigated the effects of habitat features on the relative abundance of wild boar populations and how the abundance of boars is related to frequency of Iberian wolf (Canis lupus signatus; hereafter, wolf) in the area. Wild boar relative abundance was determined by hunting bag statistics, including hunting effort-related variables (in order to avoid problems derived from modeling rates) as covariates, while wolf attacks to livestock were considered as a proxy of wolf frequency in the drive. After modeling, variation partitioning procedures were used to determine the relative importance of each factor and their overlaid effects. Our results showed that wild boar and wolf relative abundances are associated. According to previous knowledge on the wild boar ecology, we found that the species abundance is positively related to the percentage of surface occupied by mature forest and heather providing high food diversity and refuge, but these environmental variables achieved a low explanatory capacity in the models in relation to wolf frequency. The holistic approach followed in this study was attended to open new perspectives for thinking on the wolf-livestock conflict and to adequate wild boar management strategies taking into account hunting interests and natural processes.     

Spatio-temporal trends and risk factors for Trichinella species infection in wild boar (Sus scrofa) populations of central Spain: a long-term study

In south-central Spain, the harvest of Eurasian wild boar (Sus scrofa) has increased significantly during recent decades in association with more intensive management actions to increase hunting yields and with consequent effects on the health status of the wild boar populations. We investigated the spatio-temporal trends and the risk factors related to the prevalence of Trichinella spp. in wild boar in order to obtain the annual probability of occurrence for these parasites in the Ciudad Real province of south-central Spain. Based on muscle samples collected during the hunting seasons from 1998/1999 to 2009/2010, the mean prevalence for Trichinella spp. in 95,070 wild boar was 0.2% (95% confidence interval 0.17-0.23). A subsample of 1,432 wild boar was also tested by ELISA. No correlation was observed between the prevalence of infection detected by serology and by the artificial digestion of muscle. The presence of Trichinella infections in wild boar showed a decreasing trend during the study period and was negatively related with fenced wild boar populations. The predicted 'favourability' for Trichinella infections disappeared almost completely after the 2006/2007 hunting season. Risk maps based on biogeographical tools showed, however, that most hunting estates presented favourable risk factors for these parasites during at least one of the hunting seasons studied.     

First description of sarcoptic mange in wild European rabbit (Oryctolagus cuniculus)

The European wild rabbit (Oryctolagus cuniculus) is a keystone species in the Iberian Mediterranean ecosystems being the staple prey of protected and endangered predators. Wild rabbits were once widespread, but the introduction of two viral diseases, myxomatosis in the 1950s and the rabbit hemorrhagic disease in 1989, resulted into a dramatic decline of its populations. Sarcoptic mange is a highly contagious parasitic infection caused by Sarcoptes scabiei. The first cases of sarcoptic mange in a wild rabbit population are recorded from a hunting area in Majorca (Balearic Islands, Spain). Five of 32 inspected rabbits (14.7%) were affected, with similar prevalences in summer and autumn. Sarcoptes scabiei were obtained from the edge of the lesions of two of the rabbits. The most frequently observed lesions were small areas of alopecia and crusts in the limbs. Affected limbs presented also a marked hypertrichosis and an apparent abnormal growth of the nails. One rabbit also presented lesions around mouth and nostrils. Parasitized rabbits were in significant lower body condition than healthy ones. According to previous reports of mange epizooties in other naïve wild species that caused marked short-term effects in their populations, this disease may pose a risk for the conservation of wild rabbit and their predators. Whether mange is endemic in rabbits from Majorca or it has been introduced is unknown. Game managers are encouraged to be aware of introducing sarcoptic mange during rabbit translocations.

     

Habitat and reproductive phenology of wild boar (Sus scrofa) in the western Iberian Peninsula

We examined the reproductive phenology of wild boar populations in four regions of the western Iberian Peninsula during the 1999/2000 hunting season (October–February). To estimate conception dates and birth distribution frequencies, we used foetal weights. Regions differed significantly, and we detected a relationship between region and birth distribution frequencies. Throughout the year, food availability had a major influence on the distribution of farrowing. Although a short period of high food availability leads to highly synchronous births, even in relatively harsh environmental conditions, adult females that exploit low-quality food items appear to be able to give birth at any time of the year.