The montane water vole, Arvicola scherman (formerly fossorial form of Arvicola terrestris; for taxonomic consideration see Musser & Carleton, 2005), is one of the most harmful rodent species in the European farmlands (Walther et al., 2008; Blant et al., 2009; Delattre & Giraudoux, 2009; Miñarro et al., 2012). These voles live underground, dig extensive burrow systems and feed preferably on roots, bulbs and tubers (Airoldi, 1976). In fruit crops, fossorial water voles feed on bark and roots and may kill the trees (Meylan, 1977; Walther et al., 2008). Additionally, injuries to the root system make the trees less productive and more susceptible to falling down by winds or high fruit load due to deficient anchorage. Its occurrence in crops can cause important economic losses, being estimated in German orchards between 50 and 40,000 €/ha/year (Walther et al., 2008).

In the Iberian Peninsula two forms of this species are currently recognised (Ventura & Gosálbez, 1989; Musser & Carleton, 2005): A. scherman monticola, which occurs in the Pyrenees, and A. scherman cantabriae, distributed along the Cantabrian region (NW Spain) and in the northern tip of Portugal. These taxa are geographically isolated and show significant morphological differences, being cantabriae 40% lighter (Ventura, 1993). Arvicola scherman is officially considered a pest in Spain and preventive actions to reduce its population density have been recommended (BOE, 2008). In Asturias (NW Spain) this species has become one of the main causes of economical loss in apple orchards (Miñarro et al., 2012), a crop that in 2010 occupied 10,324 ha in this region (INDUROT, 2010) supposing the 32.4% of the total planted area intended to this crop in Spain (31,812 ha), whose national production, for example in 2013, reached 546,400 tons (Faostat, http://faostat.fao.org).

The effect of seasonal environmental factors, such as the decrease of temperature or food availability, can vary with altitude, which in turn affects rodent reproduction at population scale (Dunmire, 1960; Bronson, 1979; Murie et al., 1980; Zammuto & Millar, 1985; Hille & Rödel, 2014). Until now, studies about reproduction of A. scherman populations have been conducted above 400 m a.s.l., where all of them showed a delimited breeding season (Airoldi, 1978; Morel, 1981; Pascal, 1981; Ventura & Gosálbez, 1990a; Ventura et al., 1991). However, populations located in apple orchards below 270 m a.s.l. in Asturias breed continuously throughout the year (unpublished own data). Furthermore, it must be kept in mind that favourable habitats with plenty of food, such as crops, may allow rodents to invest their extra energy in increasing the reproductive effort (Doonan & Slade, 1995; Koskela et al., 1998; Díaz & Alonso, 2003; Eifler et al., 2003). Particularly, pregnant females of A. scherman cantabriae were detected over the whole year and, consequently, the recruitment of young specimens was continuous (unpublished own data). The optimal investment hypothesis predicts that litter size produced by a female should give the best reproductive success in a particular environment (Mappes et al., 1995). Therefore, reproductive potential among populations of A. scherman could vary through phenotypic plasticity or microevolution driven by the corresponding environmental conditions (Williams et al., 2014).

It is worth noting that in both, semiaquatic (A. amphibius; see Musser & Carleton, 2005) and fossorial water voles, the number of implanted embryos is positively correlated with the body dimensions of the mother (van Wijngaarden, 1954; Pelikán, 1972; Wieland, 1973; Ventura & Gosálbez, 1990b). In that sense, the reproductive potential is closely related to the body condition in semiaquatic water vole populations, which reflects energy provisions (Evsikov et al., 2008). Likewise, a good body condition in pregnant females leads to a higher number of ovulated oocytes and implanted embryos, and decreases the risk of pregnancy failure (Evsikov et al., 2008; Nazarova & Evsikov, 2008; Yuzhik et al., 2015). Furthermore, mother body condition in A. amphibius has also effects on the reproductive success, life span, body mass (Nazarova & Evsikov, 2008) and maturation of young (Yakovleva et al., 1997). Conversely, a worsening of the body condition might lead to lower fitness in females (Evsikov et al., 2008).

Management of rodent pests requires effective, specific, environmentally benign, economically feasible and socially acceptable approaches (Jacob, 2013). Thus, and especially in organic farming, there is a need for environmentally sustainable strategies, avoiding the use of rodenticides which generate genetic resistance in target species and are a risk to non-target wildlife (Rattner et al., 2014). Anticoagulant rodenticides have been routinely applied in France to control fossorial water vole populations since the 1990s (Defaut et al., 2009) with negative effects on predators (Coeurdassier et al., 2014) and scavengers (Montaz et al., 2014). Enhancing the implementation and success of sustainable control methods entail a deep knowledge of relevant aspects of the pest biology and ecology (Delattre & Giraudoux, 2009; Jacob, 2013; Ranchelli et al., 2016).

The reproductive characteristics of fossorial water voles in the Iberian Peninsula are known exclusively from studies on a population from the Aran Valley placed at about 900 m a.s.l. in the Spanish Pyrenees (Ventura & Gosálbez, 1990a, b). Thus, regarding the lack of information on this subject on A. scherman from NW Spain and given the pest condition of the species in this geographic area, the main aim of this study was to determine the reproductive potential of fossorial water voles in the Cantabrian region (A. scherman cantabriae), specifically in apple orchards located at low altitude in Asturias. Since body size and the length of the breeding season differ substantially between Pyrenean and Asturian populations (Ventura & Gosálbez, 1989, 1990a; unpublished own data), differences in the reproduction potential between those populations can be expected. Thus, a further goal of the present research was to elucidate this question by comparing our results on A. scherman cantabriae with those previously reported for A. scherman monticola. The information obtained in this study could be useful to design effective control plans for fossorial water vole populations both in our study area and in others with similar environmental characteristics.

General results of this study reveal that A. scherman cantabriae inhabiting Asturian apple orchards shows higher reproductive potential than Pyrenean fossorial water voles. Specifically, during the study period each female was able to produce 7.3 litters in a year, a value that to our knowledge is the highest one reported for A. scherman and also in the closely related species A. amphibius (2.0 - 7.1 litters/year) (van Wijngaarden, 1954; Tupikova & Švecov, 1956; Hamar & Marin, 1962; Kminiak, 1968; Pelikán, 1972; Wieland, 1973; Ventura & Gosálbez, 1990b). On the contrary, the average litter size we found in A. scherman cantabriae (3.76 embryos per female) was among the smallest values reported for A. scherman and also for A. amphibius (Perry, 1943; Van Wijngaarden, 1954; Maksimov, 1959; Kminiak, 1968; Panteleyev, 1968; Stoddart, 1971; Pelikán, 1972; Wieland, 1973; Kratochvil, 1974; Blake, 1982; Evsikov et al., 1989; Ventura & Gosálbez, 1990b). As a result of these values, the potential number of offspring per female and year reached 28.25 in Cantabrian voles, which is higher than the value indicated for A. scherman monticola (23.5) (Ventura & Gosálbez, 1990b). Therefore, populations of A. scherman can show different reproductive potential in the Iberian Peninsula depending, at least partially, on the habitat, which might ultimately determine their role as agricultural pest.

The length of the breeding season is a critical factor in determining litter size in small mammals: reproduction can be extended throughout the year at lower elevations, whereas in higher elevations larger litters are needed to sustain an equal level of reproduction during a shorter breeding season (Dunmire, 1960; Smith & McGinnis, 1968; Spencer & Steinhoff, 1968; Innes, 1978; Tkadlec & Zejda, 1998). Specifically in Arvicola, this pattern was found in semiaquatic water voles (Kratochvil, 1974). In that sense, apple orchards in Asturias are located in a temperate hyperoceanic climate (Rivas-Martínez & Rivas-Sáenz, 2015), which implies benign weather condition that allows fossorial water voles to breed continuously along the year (unpublished own data), whereas the breeding season of A. scherman is limited to the period March-November in the Pyrenees (Ventura & Gosálbez, 1990a). These differences between Spanish populations can be explained by an adaptation to seasonal changes of each geographic zone, as occur in other rodent species (Hansen et al., 1999; Solonen, 2006). Although differences in litter size between the Cantabrian and Pyrenean populations can be related with an altitudinal effect, intrinsic factors could also be involved. For example, differences in ovulation rate between wild populations of the house mouse (Mus musculus) are mainly determined by body size, whereas the influence of extrinsic factors is low (Jacob et al., 2007). Therefore, a smaller litter size in the small-sized A. scherman cantabriae (Ventura & Gosálbez, 1989; Ventura, 1993) cannot be discarded as an own characteristic of the subspecies. Additionally, we found in our sample that the body size of the mother was significantly correlated with the number of implanted embryos, result that is concordant with that reported for A. scherman monticola (Ventura & Gosálbez, 1990b). Thus, an intrapopulation effect of the relationship between body size and litter size can be added to that found between these variables in an evolutionary context.

As expected and also as observed in A. scherman monticola (Ventura & Gosálbez, 1990b), the number of placental scars increased with age in our population. Differences in the range of this variable between Cantabrian (1-15) and Pyrenean (2-20; Ventura & Gosálbez, 1990b) A. scherman are probably due to differences, at a population level, in the relationship between the number of reproductive events and litter size, and also to differences in the persistence of placental scars.

Pregnant females with macroscopic signs of resorption were also found in other populations of both A. scherman and A. amphibius (van Wijngaarden, 1954; Pelikán, 1972; Wieland, 1973; Ventura & Gosálbez, 1990b). In our sample, females in early pregnancy had similar embryonic implantation in each uterus, which suggests a balanced ovulation in both ovaries. Nevertheless, a significantly larger number of embryos implanted in the right uterus was observed for the total pregnant females, which might be due to embryo resorption. Indeed, an unequal uteri-functioning has been well described formerly in mouse and rat (Wiebold & Becker, 1987 and references therein). Moreover, Isakova et al. (2012) found in A. amphibius that an important percentage of embryos suffer a resorption in the uteri (16.7%) caused probably by mutation processes.

Body condition (relationship between the carcass mass and body length) indicates energy provision and plays an important role in the reproductive potential. Specifically, in A. amphibius it has been indicated that a good body condition in pregnant females leads to higher number of ovulated oocytes and implanted embryos, and decreases the risk of pregnancy failure (Evsikov et al., 2008; Nazarova & Evsikov, 2008; Yuzhik et al., 2015). This seems to agree with our results in A. scherman cantabriae regarding the increase of litter size with the BCI of the mother. Although a clear correlation between the number of implanted embryos and the body mass of the mother has also been reported in both A. scherman and A. amphibius (Ventura & Gosálbez, 1990b and references therein), our data suggest ultimately that the BCI is the key. Therefore, the body condition of the mother seems to be one of the main factors involved in the variation of the reproductive potential in Cantabrian voles.

The succession of monthly samplings during our two-year study involved a population control by removing specimens of both sexes from the burrow. Since the burrow system of fossorial water voles is generally inhabited by a breeding couple with their offspring (Airoldi, 1976, 1978; Morel, 1981; unpublished own data) and its maintenance and the storage of food are performed by the couple (Airoldi, 1976), the removal of the male mate might suppose a handicap for the female. In this situation, the female might face the maintenance of the burrow and the acquisition of food by its own until de arrival of a new partner which in turns can induce a decrease of the body condition, as we observed in mature non-pregnant females along this study period. Ultimately, this fact might have negative consequences on the reproductive success as it has been reported for several arvicoline species (Ostfeld, 1985).

As conclusions, the reproductive potential of A. scherman cantabriae in areas of NW Spain located at low altitude and with a temperate hyperoceanic climate is relatively high in comparison with that of fossorial water voles from the Pyrenees. Specifically, mild temperatures and enough resource availability along the whole year in our study area allow fossorial water voles to breed continuously and to perform a greater number of reproductive events per year than A. scherman monticola. Conversely, the favourable environmental conditions in the Pyrenean meadows are restricted to a part of the year, what leads voles to concentrate its energy in fewer but larger litters. Therefore, the smaller litter size in A. scherman cantabriae seems to fit with a different reproductive pattern, in which the variation in this parameter within the population may be due, at least in part, to the body condition of the mother.

Our results show that a female can produce almost 30 new specimens distributed along the whole year, what means a continuous and considerably high recruitment of juvenile specimens to the population. Such a situation suggests that management efforts should not be seasonal as they used to be so far, as it was generally assumed that reproduction stopped in winter. The recommended strategy was to increase control activity in winter in order to remove adults before the hypothetical breeding season, which was expected to start in spring. However, our results showing a continuous breeding season suggest extending these practices along the whole year. We do not mean to increase the effort (especially in the case of rodenticides given the associated environmental issues) but just that control practices could have a similar effect with independence of the time of the year. Also important to avoid secondary effects on non-target animals, surface signs of activity of A. scherman should be distinguished from those of Talpa occidentalis, an innocuous species inhabiting also apple orchards (Miñarro et al., 2012). For the same reason, alternative strategies, such as fences to avoid invasions from dispersal juvenile specimens from nearby source demes (Saucy & Schneiter, 1998; Saucy, 2002; Walther & Fuelling, 2010) should be also maintained all the year. The effectiveness of other sustainable control management strategies, such as frequent mowing (Morilhat et al., 2007; Jacob, 2008), livestock grazing (Defaut et al., 2009) or the use of repellents (Fischer et al., 2013) should be explored in our particular case. As mentioned for A. amphibius, mother body condition might also have other physiological consequences in the offspring, affecting the reproductive success, life span, body mass and maturation of young (Yakovleva et al., 1997; Nazarova & Evsikov, 2008). Since population density and the subsequent damage to crops could be ultimately proportional to the population growth, which in turn depends on the reproductive effort (Ostfeld, 1985; Cerqueira et al., 2006), further studies focused on the physiological consequences of management practices (those creating a more disadvantageous environment; Morilhat et al., 2007; Jacob, 2008; Defautet al., 2009) will be welcome to unravel their effect on the reproductive fitness in A. scherman, and to evaluate their feasibility as alternative control strategies.