Francisco Carro

Ecosystem Effects of Variant Rabbit Hemorrhagic Disease Virus, Iberian Peninsula

To the Editor: In this investigation, we found evidence for the apparent effects that a new variant of the rabbit hemorrhagic disease virus (RHDV) is having on native wild European rabbit (Oryctolagus cuniculus) populations on the Iberian Peninsula, and how this virus could threaten the conservation of endangered predators. Historically, European rabbits were extremely abundant on the Iberian Peninsula, which is in their native range. However, during the 20th century, the number of rabbits on the peninsula has declined >90%, mainly because of diseases (1). The first notable crisis among rabbits occurred during the 1950s concurrent with the arrival of myxomatosis among rabbit populations, which caused mortality rates of ≈90% (1), as registered in other regions. During the late 1980s, a calicivirus, RHDV, caused infections that made a strong impact on rabbit populations, causing initial mortality rates of 55%–75% in Iberia (1). Since their initial outbreaks, both diseases have become enzootic, and related mortality rates have decreased, in part because of increased host resistance, although the infections still play a major role in the dynamics of rabbit populations (2). In 2011, a new variant of RHDV, which appears to be closely related to an isolate originating in France that was described in 2010 (3), caused high mortality rates in some rabbit farms in Spain (4) and was also identified in an experimental wild rabbit plot in northern Spain (5). Since 2012, the new variant of RHDV has been detected in most rabbit farms in Spain (6), and in several wild populations distributed across Spain and Portugal (7), suggesting that it has rapidly spread throughout the Iberian Peninsula. This variant affects both of the wild rabbit subspecies (O. cuniculus cuniculus and O. c. algirus), and unlike the classical form of RHDV, it kills rabbits as young as 11 days of age and rabbits that have been vaccinated against classic RHDV (6,7). This scenario has raised concern for the survival of wild rabbit populations and its predators in this region. Data regarding rabbit trends seem to sustain this concern. For example, a long-term monitoring program in Aragon in northern Spain shows a notable decline in rabbit numbers during 2013 in populations that showed both long-term increasing and decreasing trends over the monitoring period (Figure, panels A, B, respectively). A similar trend has been observed in the main areas inhabited by the highly endangered Iberian lynx (Lynx pardinus). The lynx relies on rabbits for survival, because they represent >85% of the lynx’s diet (9). For instance, in Coto del Rey, the area within Donana National Park in southern Spain that traditionally held the highest rabbit densities and therefore represents the core of Iberian lynx populations in this national park, there was a decline in rabbits of >80% during 2012–2013 (Figure, panel C). Similar declines have been detected in low-density rabbit populations surveyed within Donana National Park (Figure, panel C). Rabbit numbers have also been progressively dropping in the proximity of the Yeguas River in Andujar and Cardena Natural Parks in southern Spain, where the largest Iberian lynx population currently lives: rabbit density was >3.5 rabbits/hectare in 2010 and <1 rabbit/hectare in 2013, a decline of ≈75% (10). In accordance with field surveys, hunters throughout Iberia claim that the number of rabbits harvested this season has decreased dramatically, pointing to a 70%–80% decline compared to the previous hunting season in some estates (A. Linares, pers. comm.). Figure Trends in rabbit abundance (number of rabbits/km) in Aragon and Donana National Park, northern and southern Spain, respectively, and in the number of Iberian lynx cubs born in the wild in Spain. A) Average rabbit abundance (+SD) of populations ... The European rabbit is a multifunctional keystone species of the Iberian Mediterranean ecosystem, where it serves as prey for >30 predatory animals, alters plant species composition and vegetation structure through grazing and seed dispersal, its excrement and urine have an effect on soil fertility and plant growth and provide feeding resources for invertebrates, and its burrows provide shelter for different species (9). Therefore, the decline in rabbit numbers could have potential cascading effects on ecosystem function. In fact, some of these effects may already be apparent on rabbit-reliant animals. On one hand, the sharp reduction in rabbit numbers observed in 2013 in the main lynx distribution area has been accompanied by a notable decrease in the number of lynx cubs born in the wild (Figure, panel D). On the other hand, the number of lynxes killed on roads doubled in 2013 (n = 14) in relation to 2012 (n = 7), and this has been linked to increased lynx displacements related to rabbit scarcity potentially associated with the impact of the new variant of RHDV (http://www.juntadeandalucia.es). The situation described exemplifies how emerging diseases can affect biodiversity conservation. It also highlights the importance of using wildlife monitoring schemes as detection tools for monitoring the impact of stochastic factors, such as the variant RHDV, on wildlife populations. Urgent management actions, designed within an Iberian rabbit conservation strategy that relies on a multidisciplinary framework, are needed to ensure the conservation of this keystone member of the Iberian Peninsula ecosystem and that of rabbit-reliant predators.

Spatiotemporal interactions between wild boar and cattle: implications for cross-species disease transmission

Controlling infectious diseases at the wildlife/livestock interface is often difficult because the ecological processes driving transmission between wildlife reservoirs and sympatric livestock populations are poorly understood. Thus, assessing how animals use their environment and how this affects interspecific interactions is an important factor in determining the local risk for disease transmission and maintenance. We used data from concurrently monitored GPS-collared domestic cattle and wild boar (Sus scrofa) to assess spatiotemporal interactions and associated implications for bovine tuberculosis (TB) transmission in a complex ecological and epidemiological system, Doñana National Park (DNP, South Spain). We found that fine-scale spatial overlap of cattle and wild boar was seasonally high in some habitats. In general, spatial interactions between the two species were highest in the marsh-shrub ecotone and at permanent water sources, whereas shrub-woodlands and seasonal grass-marshlands were areas with lower predicted relative interactions. Wild boar and cattle generally used different resources during winter and spring in DNP. Conversely, limited differences in resource selection during summer and autumn, when food and water availability were limiting, resulted in negligible spatial segregation and thus probably high encounter rates. The spatial gradient in potential overlap between the two species across DNP corresponded well with the spatial variation in the observed incidence of TB in cattle and prevalence of TB in wild boar. We suggest that the marsh-shrub ecotone and permanent water sources act as important points of TB transmission in our system, particularly during summer and autumn. Targeted management actions are suggested to reduce potential interactions between cattle and wild boar in order to prevent disease transmission and design effective control strategies.

Synchrony between fruit maturation and effective dispersers' foraging activity increases seed protection against seed predators

The evolution of pollination and seed dispersal mutualisms is conditioned by the spatial and temporal co-occurrence of animals and plants. In the present study we explore the timing of seed release of a myrmecochorous plant (Helleborus foetidus) and ant activity in two populations in southern Spain during 2 consecutive years. The results indicate that fruit dehiscence and seed shedding occur mostly in the morning and correspond to the period of maximum foraging activity of the most effective ant dispersers. By contrast, ant species that do not transport seeds and/or that do not abound near the plants are active either before or after H. foetidus diaspores are released. Experimental analysis of diet preference for three kinds of food shows that effective ant dispersers are mostly scavengers that readily feed on insect corpses and sugars. Artificial seed depots suggest that seeds deposited on the ground out of the natural daily time window of diaspore releasing are not removed by ants and suffer strong predation by nocturnal rodents Apodemus sylvaticus. Nevertheless, important inter-annual variations in rodent populations cast doubts on their real importance as selection agents. We argue that traits allowing synchrony between seed presentation and effective partners may constitute a crucial pre-adaptation for the evolution of plant–animal mutualisms involving numerous animal partners.

Independent lineage of lymphocytic choriomeningitis virus in wood mice (Apodemus sylvaticus), Spain.

To clarify the presence of lymphocytic choriomeningitis virus (LCMV) in Spain, we examined blood and tissue specimens from 866 small mammals. LCMV RNA was detected in 3 of 694 wood mice (Apodemus sylvaticus). Phylogenetic analyses suggest that the strains constitute a new evolutionary lineage. LCMV antibodies were detected in 4 of 10 rodent species tested.

Small-scale indirect effects determine the outcome of a tripartite plant–disperser–granivore interaction

The microhabitat in which plants grow affects the outcome of their interactions with animals, particularly non-specialist consumers. Nevertheless, as most research on this topic has dealt with either mutualists or antagonists, little is known about the indirect effects of plant microhabitats on the outcome of tripartite interactions involving plants and both mutualists (e.g. seed dispersers) and antagonists (e.g. granivores). During three consecutive years, we analysed small-scale variations in the interaction of a perennial myrmecochore, Helleborus foetidus, with its seed dispersers and consumers as a function of the intensity of plant cover. Most seeds were released during the day and were rapidly removed by ants. Nevertheless, the proportion of ant-removed seeds was higher for plants located in open microhabitats than for plants surrounded by dense vegetation and rocky cover. Ant sampling revealed that seed removers were equally abundant, irrespective of the level of cover. By contrast, a few tiny ant species that feed on the reward without transporting the seeds were more abundant in highly covered microhabitats, irrespective of hellebore diaspore availability. These “cheaters” decrease the chance of removal by removers and increase the probability of seeds remaining on the ground until night, when granivore mice Apodemus sylvaticus become active. Mice also preferred foraging in covered microhabitats, where they consumed a larger proportion of seeds. Therefore, the density of cover indirectly increased seed predation risk by attracting more seed predators and cheater ants that contribute to increase seed availability for seed predators. Our results emphasize the importance of considering the indirect effects of plant microhabitat on their dispersal success. They highlight the indirect effect of cheaters that are likely to interfere in mutualisms and may lead to their collapse unless external factors such as spatio-temporal heterogeneity in seed availability constrain their effect.

Is blood collected from shot Iberian ibex (Capra pyrenaica) useful for monitoring their physiological status

Blood samples were analysed from 175 shot Iberian ibexes, and good-quality samples were obtained in more than 56% of cases. Sixty-eight of these samples from healthy animals were then used to characterize standard values for the species. Values for 10 blood parameters [monocytes, cholesterol, creatinine, albumin, beta-globulin, gamma-globulin, albumin/globulin (A/G) ratio, calcium (Ca), phosphates and iron (Fe)] from shot ibexes did not differ from those obtained from healthy captured and physically restrained animals. Blood samples from mange-infested ibexes (n=31) were also analysed and showed higher values for eosinophils and gamma-globulin than samples from healthy animals, but lower values for cholesterol, direct bilirubin, albumin, alpha-2-globulins and chloride. Values from blood parameters can provide useful information about the health and nutritional status of animals, and blood values may thus provide a complementary source of information for animals shot in Andalusia that will prove to be useful for monitoring the physiological status of ibex populations. The protocol described here provides guidelines for quick sample collection after an animal’s death and standardized instructions for sample storage, transport and analysis.

Efficient identification of Microtus cabrerae excrements using noninvasive molecular analysis

Noninvasive sampling is a potentially cost-effective and efficient means of monitoring wild animals that precludes the need for captures and avoids undue disturbance. Nevertheless, it is generally difficult to separate faeces deposited by Microtus cabrerae from that of other sympatric rodents of similar body size on the basis of just morphological features and content. Species identification methods in many noninvasive studies involve mtDNA analysis. Here we report the first use of species-specific primers targeting the SRY gene in a noninvasive molecular identification of Cabrera’s vole. This noninvasive molecular-based technique may thus provide us with a potential tool for further genetic and ecological study of this threatened species of Iberian vole.

Relation between physical condition and reproductive activity in a population of Iberian hares, Lepus granatensis in northern Iberian peninsula

Abstract. The aim of this study was to analyze the relation between physical condition, measured as the Kidney Fat Index (KFI), and some reproductive parameters of Lepus granatensis in Navarra province, Spain. Samples were collected between October 2001 and January 2003, totaling 174 hares (87 males and 87 females). All the hares were sexed and classified in three age categories (immature, young and adult). Fertile males and females were present in all monthly samples. Kidney weight was greater in females than in males for all the age classes and kidney weight variation along the year was not significant. Ranges of perirenal fat accumulated were larger in females but mean weight of fat for all hares was similar in males and females. Body weight and kidney fat weight was directly related both for males and females. Global pattern of fat deposition along the year was similar for both sexes. The amount of perirenal fat in adult fertile hares reaches maximum values just before the main reproduction period and reproductive state conditioned kidney fat levels. Pregnancy induces fat deposition in females and factors such as the number of embryos and the stage of gestation influence kidney fat levels.

Long-term patterns in Iberian hare population dynamics in a protected area (Doñana National Park) in the southwestern Iberian Peninsula: Effects of weather conditions and plant cover

The Iberian hare (Lepus granatensis) is a widely distributed endemic species in the Iberian Peninsula. To improve our knowledge of its population dynamics, the relative abundance and population trends of the Iberian hare were studied in the autumns of 1995-2012 in a protected area (Doñana National Park) by spotlighting in 2 different habitats: marshland and ecotones. The average relative abundance was 0.38 hare/km (SD = 0.63) in the marshland and 3.6 hares/km (SD = 4.09) in ecotones. The Iberian hare population exhibited local interannual fluctuations and a negative population trend during the study period (1995-2012). The results suggest that its populations are in decline. The flooding of parts of the marshland in June, July and October favor hare abundance in the ecotone. Hare abundance in the marshland increases as the flooded surface area increases in October. These effects are more pronounced if the rains are early (October) and partially flood the marsh. By contrast, when marsh grasses and graminoids are very high and thick (as measured using the aerial herbaceous biomass [biomass marshland] as a proxy), the abundance of hares decreases dramatically as does the area of the marsh that is flooded (in November).

Contribución del seguimiento ecológico a largo plazo a la investigación y la gestión en la plataforma LTSER-Doñana

Bonache, J., de Mingo-Sancho, G., Serrada, J., Amengual, P., Perales, J., Martinez, R., Rodado, S., Albornos, E. 2016. Long-term monitoring and evaluation in Spanish National Parks Network. Ecosistemas 25(1): 31-48. Doi.: 10.7818/ECOS.2016.25-1.05 The Spanish National Parks Network, consisting of a selection of natural spaces containing a representative sample of the main existing natural systems in Spain, is a very appropriate setting for research and long-term monitoring, in which the rules protects and promotes the improvement of knowledge and its application to management. In this regard, the National Parks Agency develops, in collaboration with the Autonomous Communities and with specific Scientific advise, a Research Program and a Monitoring and Evaluation Plan of the National Parks Network, latter having programs of ecological, sociological monitoring and functional. The article briefly explains the various monitoring initiatives underway, with examples of outcomes in each: mapping of natural systems, productivity monitoring through remote sensing, monitoring plant health, common bird monitoring, studies of social perception etc. Future prospects and areas for improvement of long-term monitoring in the National Parks Network are explained taking into account the synergies with the LTER Network, which is useful for monitoring in National Parks, especially concerning the application of comparable protocols and information management.