- Email: [email protected]
Supplementary food reduces home ranges of European wild rabbits in an intensive agricultural landscape
Mammalian Biology 95 (2019) 35–40
Contents lists available at ScienceDirect
Mammalian Biology journal homepage: www.elsevier.com/locate/mambio
Original investigation
Supplementary food reduces home ranges of European wild rabbits in an intensive agricultural landscape Carlos Rouco a,∗,1 , Isabel C. Barrio a,∗∗,1,2 , Francesca Cirilli a , Francisco S. Tortosa a,b , Rafael Villafuerte c a
Department of Zoology, University of Cordoba. Campus de Rabanales, 14071 Córdoba, Spain Escuela Superior Politécnica Agropecuaria de Manabí, Calceta, Ecuador c Instituto de Estudios Sociales Avanzados (IESA-CSIC), Campo Santo de los Mártires, 14004 Córdoba, Spain b
a r t i c l e
i n f o
Article history: Received 1 October 2018 Accepted 22 January 2019 Available online 8 February 2019 Handled by Heiko G. Rödel Keywords: Food availability Use of space Lagomorph Management Vertebrate pest Wildlife damage
a b s t r a c t Understanding use of space in free ranging populations that cause damage to agriculture can help in the design of measures aimed at reducing their impact. Food availability is known to determine use of space in terrestrial vertebrates so, providing alternative food sources during a specific time period may help the management of vertebrate pests by reducing their ranging behavior. We investigated space use by a crop damaging species, the European wild rabbit (Oryctolagus cuniculus), in an intensively-managed agricultural landscape within its native range and evaluated the potential of food availability to restrict areas of rabbit activity. We determined the size of day-time home range (95% minimum convex polygon, MCP) and core area (50% MCP) of rabbits before and after providing additional food to one rabbit population, while an unsupplemented population served as a control. Rabbits in the study area had large home ranges in comparison with those previously reported in the literature, probably linked to the heterogeneous and unpredictable distribution of resources in intensively-managed Mediterranean agro-ecosystems. There was a general reduction in size of home ranges and core areas between the experimental phases, but we found evidence that additional feeding restricted the space use of rabbits. The wide-ranging behavior of rabbits documented in the present study might explain why even moderate rabbit densities can cause widespread damage to crops. These findings may facilitate the design of management tools to mitigate damage in agricultural areas where rabbits are considered an agricultural pest. ¨ Saugetierkunde. ¨ Published by Elsevier GmbH. All rights reserved. © 2019 Deutsche Gesellschaft fur
Introduction Overabundant herbivores can pose serious threats to crops (Conover, 2001; Tulloch et al., 2014; Fox et al., 2017). Community and ecosystem degradation as a consequence of human activities can favor range expansions and higher densities of generalist species (Goodrich and Buskirk, 1995), and intensively-managed ecosystems can provide gaps for opportunistic species (Vitousek et al., 1997). That seems to be the case of the European rabbit (Oryctolagus cuniculus) in some areas within its native range. Despite
∗ Corresponding author. ∗∗ Corresponding author at: Agricultural University of Iceland, Árleyni 22, 112 Reykjavik, Iceland. E-mail addresses: [email protected], [email protected] (C. Rouco), [email protected] (I.C. Barrio). 1 Both authors contributed equally to this work. 2 Present address: Agricultural University of Iceland, Árleyni 22, 112 Reykjavik, Iceland.
a sharp decline of the species in the last decades (Moreno et al., 2007; Delibes-Mateos et al., 2009), rabbit populations seem to be recovering in some agricultural areas of southern Spain (Carpio et al., 2017; Delibes-Mateos et al., 2018). Positive trends in rabbit numbers are probably associated with favorable conditions, such as the occurrence of soft soils that enable warren digging, and reduced predation pressure linked to predator control by hunters (Delibes-Mateos et al., 2008). In many areas where they have been introduced, rabbits have been described as one of the most damaging pests (Smith et al., 2007). Although in their native range they do not reach such high densities (Barrio et al., 2010a; Delibes-Mateos et al., 2014), increasing concerns arise because of the damage they cause to crops (Barrio et al., 2010b). Effective management of vertebrate pests in agricultural systems should incorporate knowledge of temporal and spatial dynamics of pest species (Van Vuren and Smallwood, 1996). In this sense, understanding space use of rabbits in these areas may assist in the design of effective measures aimed at reducing their impacts. However, most work on rabbit use of space has been conducted
https://doi.org/10.1016/j.mambio.2019.01.006 ¨ Saugetierkunde. ¨ Published by Elsevier GmbH. All rights reserved. 1616-5047/© 2019 Deutsche Gesellschaft fur
36
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
in areas where the species has been introduced (Hulbert et al., 1996; Stott, 2003; White et al., 2003; Moseby et al., 2005; Devillard et al., 2008) or in semi-natural habitats within its native range (Villafuerte, 1994; Lombardi et al., 2007). Information is scarce from agricultural areas within its native range where they cause damage to crops. Space use is a function of habitat productivity, resource distribution, the area used during migration or dispersal periods, or individual energy requirements (McLoughlin and Ferguson, 2000; Mitchell and Powell, 2004). Habitats with high resource availability allow individuals to meet their daily and seasonal needs within relatively small areas, but if resources are low or heterogeneous in space or time, larger areas might be needed (Ferguson et al., 1999; Johnson et al., 2002; Petrovan et al., 2017). In this sense, patchy spatial distribution and ephemeral availability of resources linked to intensively-managed semi-arid Mediterranean environments may force rabbits to range over longer distances to fulfill their nutritional requirements, potentially increasing the spread of damage to agricultural crops. In many terrestrial vertebrates, home range size decreases with increasing food availability (e.g. Hulbert et al., 1996), and experimental provision of food usually reduces home range sizes (Boutin, 1990). Alternative food availability reduces rabbit damage to crops (Barrio et al., 2010b) and might also affect space use of rabbits (Barrio et al., 2012) but the use of supplementary food as a management tool remains understudied. The aim of this study was 1) to investigate the space use of wild rabbits in an intensively-managed agricultural landscape; and 2) to evaluate the role of food availability in space use by rabbits. We determined home range and core area sizes before and after providing food to one rabbit population, while an unsupplemented population served as a control. We expected that an experimental increase in food availability would reduce home ranges and core areas sizes of wild rabbits, thereby potentially minimizing the extent of rabbits’ damage to crops.
Material and methods Study area The study was conducted in an agricultural area within Córdoba province, southern Spain (37◦ 33 N, 4◦ 37 W). Climate is dry Mediterranean, with average annual rainfall of 500 mm and average monthly temperatures 8–26 ◦ C. Intensive agriculture is the dominant land use in the area with the main crops being olive groves, vineyards, and cereals. Alternative food sources for rabbits (i.e. herbaceous vegetation other than crops) are scarce in the dominant crops because of extensive application of herbicides (Barrio et al., 2013). Rabbits occur in moderate numbers (Barrio et al., 2010a) and cause damage to crops, especially to vineyards early in the growing season (March-April; Barrio et al., 2013).
Experimental design Two rabbit populations (>1.5 km) were selected to run the experiment during spring-summer 2009. Both populations were similar in terms of rabbit density (around 1.28 rabbits/ha, Barrio et al., 2010a; Delibes-Mateos et al., 2014), warren availability (0.37 and 0.42 warrens/ha; surveyed in a 0.5 km radius area for each population), habitat structure, in terms of herbaceous, shrub and tree cover (Barrio and Cirilli, unpublished data; assessed along 6 50 m randomly selected transects at each population), and carnivore presence (5.5 and 6 scats/km, assessed along a 2 km transect at each population), mainly red fox (Vulpes vulpes), although other predators like European polecat (Mustela putorius), common genet
(Genetta genetta), Egyptian mongoose (Herpestes ichneumon) and domestic dogs (Canis familiaris) were also present. The experiment was structured in two phases. In the first part of the experiment (phase 0; March-May), we assessed home ranges of both rabbit populations in an intensive agricultural landscape. In the second part of the experiment, we randomly chose one of the populations (group A) and provided it with supplementary food (i.e. fresh alfalfa Medicago sativa close to warren entrances), whereas the other population (group B) remained as a control. After a one-week acclimation period with supplementary food we started monitoring the animals again (phase 1; May-July). Supplementary food was placed close to the warren entrances of the focal group, to ensure that only rabbits from that group would have access to it. Rabbits readily consumed the supplementary food, so fresh alfalfa was provided twice a week to ensure it was never exhausted. The experiment thus covered the end of the breeding period (phase 0) and the annual peak in rabbit abundance (phase 1) when juveniles are recruited to the population (Gonc¸alves et al., 2002). We also estimated rabbit abundance by means of pellet counts in 10 randomly placed 0.5 m2 sampling points once in each site and at the end of each phase (May 20 and June 29). These counts represent accumulated pellets over time. Rabbit monitoring Rabbits were caught with ferrets (i.e. chased using trained ferrets into nets placed at the warren exits), and all were weighed and sexed at capture, but only adult rabbits (>900 g; range 935 to 1530 g, Villafuerte, 1994) were equipped with a radio collar (AVM Instrument Company, Ltd., U.S.A.). All collars had a motion link device, which generates a different pulse rate after 4 h of inactivity (mortality sensor). When rabbit locations did not change for more than two days and the activity sensor of the collar indicated that the rabbit was not moving, the collars were retrieved. We radio-collared a total of 30 adult rabbits during the entire experiment but locations were only available for the two phases of the experiment for 20 rabbits, 12 in group A (i.e. 5 ♂ and 7 ♀) and 8 in group B (i.e. 3 ♂ and 5 ♀). To locate rabbits in the field we used a portable receiver (R-1000 Communications Specialists, Inc., California, U.S.A.) and a handheld three-element Yagi antenna (BIOTRACK, Wareham, UK) with transmitters’ frequencies within the 150–152 MHz range. Rabbits were located daily from at least two mapped receiving points within the shortest time possible between fixes, by using standard triangulation techniques for mobile triangulation systems (White and Garrot, 1990). In order to reduce errors, bearings of the tagged animals (compass bearings from true North, Schmutz and White, 1990) were taken by the same two observers (ICB and FC), and we only located rabbits during the day, when they are less mobile (i.e. Villafuerte et al., 1993). We calculated the location error of our triangulation measurements by placing radio-collars in the field and recording their exact geographic position with a GPS. We located the collars from the mapped receiving points following the same procedure as for rabbits. We calculated location error for each triangulation (i.e. pair of locations) as the distance (m) between the true position of the radio-collar and the location obtained after triangulation (Schmutz and White, 1990; Kauhala et al., 2005). Location error increased for each triangulation with the maximum distance between the receiving point and the corresponding location (maximum location distance; R2 = 0.407; F1,98 = 67.32; p < 0.001). We further considered only those triangulations for which both location distances between the observer and the rabbit were < 2000 m, which yielded a median error estimate of 92.44 m (median absolute deviation = 70.48 m; n = 60; range = 5.19–377.60 m). Discarding extremely biased triangulations reduced our data to 76.6% of its original size (from 1503 to 1152 triangulations). Observer identity (FC or ICB) did
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
not have a significant effect on location error (ANOVA; F1,31 = 0.019; p = 0.890). Each rabbit was located once a day, for a total of 46 survey days during the first phase (i.e. phase 0) and 38 days during the second phase of the experiment (i.e. phase 1). Additionally, we used the “homing-in” method (White and Garrot, 1990) once a week, to locate resting sites and assess warren fidelity. Rabbits were considered to be attached to the same warren when most locations (>75%) occurred within their main warren or in the close vicinity (i.e. other warrens or surface refuges < 100 m from their main warren, Cowan, 1987). Within 3 months of the end of the experiment, 89% of the collars were recovered through non-specific hunting (44%) or ferreting (56%), i.e. not intended specifically at recovering the collars, but as part of the regular hunting season (October-December, and additionally in some areas July-September for rabbit control, Barrio et al., 2013) or ferreting for population control in the study area.
37
rabbit population, group A or B, and the phase of the experiment, phase 0 or phase 1), and sex of the rabbit, as male and female rabbits may use space differently, particularly during the breeding season (Devillard et al., 2008). Differences in rabbit abundance based on the pellet counts between the two populations in the two phases of the experiment, were assessed using a Linear Model (LM), where pellet density was included as a response variable, and treatment (as defined above) was included as a predictor variable. Modelling assumptions were validated by visually inspecting the residuals of the models. We performed all statistical analyses in R 3.5.1 (R Development Core Team, 2018), using the packages lme4 and lmerTest for calculating Satterthwaite approximations of p-values for LMMs. Global significance of variables with several levels (e.g. treatment) was assessed by comparing models with and without the predictor variable; F values and the associated p-values are reported in these cases. For comparisons between treatment levels in LMM t-values and the associated p-values are reported.
Home range size and core area size estimation We estimated home range sizes and core areas for each rabbit and phase of the experiment using the Minimum Convex Polygon method (MCP) with two levels of outlier exclusion: 95% MCP to estimate the activity area of the rabbits (hereafter ‘home range’) and 50% MCP to estimate the restricted core area of the home range (hereafter ‘core area’) of each individual (Devillard et al., 2008). Although the MCP has been criticized because it includes areas rarely visited and thus may overestimate home range (Laver and Kelly, 2008), its use is still widespread and helpful to compare results among studies. We use it here as a relative measure of home range size and for ease of comparisons with other published data. Other methods, like kernels or the k-nearest neighbours convex hull, are sensitive to aggregated data, with potential lack of convergence in the smoothing parameters (Devillard et al., 2008). Since we only used locations collected during the day, data was expected to be highly aggregated. Finally, kernel density estimates were not used because to the recommendation of gathering at least 30 observations per animal (ideally 50) to obtain an accurate estimate was not reached (Seaman et al., 1999). To calculate the appropriate number of locations needed to correctly estimate home range size we followed the incremental area analysis (Kenward, 2001), which assumes that home range estimates reach an asymptote with an adequate sample size. For each rabbit and phase, we drew the relationship between the estimated 95% MCP home range size and the number of locations used in the estimation, with a bootstrapping approach (500 random samples of k locations, varying k from 5 to the total number of locations for each rabbit). For each value of k we estimated the mean 95% MCP over the 500 bootstrap samples. The appropriate number of locations kopt to estimate home range size for each rabbit-phase combination was the value of k for which the estimated home range size was at least equal to 95% of the home range size estimated with the full set of locations (i.e. when the asymptote is reached, Devillard et al., 2008). The median value of kopt for each phase was calculated (kopt was 18.5 and 16.5 for phase 0 and phase 1, respectively). Statistical analysis To evaluate if our treatment of supplementary feeding affects home range and core area sizes of rabbits in an agricultural landscape, we built two Linear Mixed Effects Models (LMM), where the response variables were the home range and core area sizes, respectively. We included rabbit identity as a random effect to account for repeated measures of each rabbit in the two experimental phases. As predictor variables we included the additive effects of treatment (as a variable with four levels resulting from the combination of the
Results The mean (± SE) number of fixes collected per animal during phase 0 and phase 1 was 17.8 (± 1.7) and 33.7 (± 4.4), respectively. Warren fidelity was high throughout the study, with most animals (88.9%) remaining within their original group of warrens. We found no significant differences in rabbit abundance between groups and phases during the study (LM, F36,39 = 0.496, p = 0.688), as assessed by pellet counts (means ± SE: group A phase 0: 40.3 ± 50.4 pellets/m2 ; phase 1: 31.6 ± 20.4 pellets/m2 ; group B phase 0: 22.8 ± 27.0 pellets/m2 ; phase 1: 27.8 ± 26.8 pellets/m2 ). Effect of supplementary feeding on home range and core area size Before adding supplementary food (i.e. in phase 0) rabbits in group A had significantly larger home ranges and core areas than rabbits in group B (LMM; home range: t34.95 = -2.32, p = 0.026; core area: t35 = -3.96, p < 0.001; Fig. 1). For both populations home ranges and core areas were significantly larger during phase 0 than during phase 1 (Fig. 1), but these reductions were only significant for group A (LMM; home range: t18 = -2.80, p = 0.011; core area: t35 = -3.27, p = 0.002; Fig. 1). Supplementary food reduced rabbit home ˜ range in group A by 52%. Reductions in home range and core areas of the control population (i.e. group B) between the two phases ˜ (i.e. 25%) were not statistically significant (LMM; home range: t18 = -0.57, p = 0.579; core area: t35 = -0.90, p = 0.374; Fig. 1). Sex had no significant influence on home range or core area size (LMM; home range: t17 = -0.90, p = 0.374; core area: t35 = 1.44, p = 0.160). Discussion In the present study we report for the first time the space use of rabbits in intensively-managed agricultural landscapes where they cause damage to crops (Barrio et al., 2010b). The two rabbit populations differed in their home range sizes before the experimental addition of food, and both populations reduced their home range during the second phase of the experiment, but this reduction was stronger for rabbits with experimentally increased food availability. In light of our results, potential management implications can be derived, suggesting an avenue for future investigations. Space use of rabbits in agricultural landscapes Day-time home range sizes of rabbits inhabiting intensivelymanaged agricultural landscapes in Southern Spain were surprisingly large (average for both populations in phase 0:
38
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
Fig. 1. Home range (a) and core area sizes (b) of two rabbit populations in an agricultural landscape of southern Spain, in the two phases of a supplementary feeding experiment. Phase 0 reflects unmanipulated conditions for both populations (group A and B), while in phase 1 group A was provided with supplementary food and group B remained as a control. Group A included 12 rabbits and group B included 8 rabbits. Home range size (ha) was estimated with Minimum Convex Polygons (MCP) at 95% and core areas size estimated with MCP at 50%; means and standard errors are shown. Small-case letters on the bars indicate significant differences (p < 0.05) between groups. Note the differences in scaling between y-axes in (a) and (b).
mean ± SE = 9.63 ± 3.12 ha; Fig. 1) in comparison to those MCP estimates quoted in the literature (e.g. 6 ha Hulbert et al., 1996; 3.5 ha Moseby et al., 2005; < 2 ha Devillard et al., 2008). Rabbits are crepuscular animals, so we would expect even larger home range sizes at night (Villafuerte, 1994). Although seasonal differences have been documented with larger home ranges in spring (Lombardi et al., 2007; Devillard et al., 2008), our results are much larger than those referred in other agricultural landscapes (Daniels et al., 2003; Stott, 2003). In many mammal species, home range size depends on population density (Efford et al., 2016). The large home ranges found in our study could be explained in part by the moderate rabbit densities in our study area (1.28 rabbits/ha, Barrio et al., 2010a), compared to areas with considerably higher rabbit densities where rabbits had smaller home ranges (e.g. 5 rabbits/ha, Devillard et al., 2008). This phenomenon has been also reported for other game species in intensively managed agroecosystems in Europe (e.g. brown hares Lepus europaeus; Marboutin and Aebischer, 1996), or red legged partridges Alectoris rufa; Buenestado et al., 2008) or other vertebrate pest species like the brushtail possum (Trichosurus vulpecula) in New Zealand (Rouco et al., 2017). It has also been argued that enlarged home ranges could result from frequent human disturbance in these environments (Buenestado et al., 2008; Devillard et al., 2008). Large home range sizes might also be an adaptive strategy to cope with environmental heterogeneity and unpredictable resource distribution (Ferguson et al., 1999; Eide et al., 2004; Rouco et al., 2013), as well as low food availability (Petrovan et al., 2017). Larger home ranges would indicate an increased exploratory behavior in search for the scarce and patchily distributed food, to ensure meeting the individuals’ energetic requirements. Travelling long distances to feed on better quality forage has been described for rabbits inhabiting resource-limited environments (Trout, 2002) and hares (Petrovan et al., 2017). In addition, the low predation rates found in our study area may favor this strategy. Banks et al. (1999) found that in an area where red foxes had been removed, rabbits moved farther from cover than in an area where predators were present, due to a reduction in perceived predation risk. This behaviour has also been observed in rabbits held in seminatural conditions within the species native range (Rouco et al.,
2011). Thus, a combination of scattered food sources, reduced perceived predation risk and nearly constant human disturbance may be driving the large home ranges found in this agricultural area. Effects of food availability on space use of rabbits Home range size in lagomorphs has shown to be negatively correlated with the abundance of food (e.g. snowshoe hare Lepus americanus, Boutin, 1984; mountain hare Lepus timidus, Hulbert et al., 1996; Kauhala et al., 2005) and with rabbit density (Devillard et al., 2008). In the present study, we found a significant effect of supplementary feeding on the spatial behavior of rabbits, reducing their home range sizes. Both rabbit populations reduced their home range size and core area sizes across the phases of the experiment. Such reductions can be expected, since home ranges of rabbits are larger during the breeding season and decrease thereafter (Devillard et al., 2008). Our study overlapped with most of the rabbit breeding season in Mediterranean habitats (which peaks between March and April, Gonc¸alves et al., 2002), especially during the first phase. However, the addition of supplementary food in group A seemed to synergize home range reduction, likely due to both; easy access to food resources, and the end of the breeding season. It is noteworthy, that enhanced food availability did not locally increase rabbit abundance in the short term (the 2-month-long second phase of this experiment when supplementary food was provided); therefore, density-dependent factors may not be confounding the effects of food supplementation on home range sizes in the present study. However, this possibility needs to be taken into account if supplementary feeding is to be used as a management strategy, as it has the potential to increase rabbit densities in the medium and long term. Management implications Food availability has proven to reduce rabbit damage, at least to vineyards (Barrio et al., 2010b), and our results revealed that food availability does limit the ranging behavior of rabbits in an agricultural landscape. By having easy access to food, rabbits are
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
not forced to range widely to find less common food sources in order to reach their nutritional requirements. Therefore, the use of supplementary feeding could reduce the likelihood of rabbit damage to agriculture, potentially mitigating hunters-farmers conflict (Delibes-Mateos et al., 2014). In addition, reducing rabbits’ ranging behavior, in combination with other practices that reduce rabbit densities through modifying cultural systems or increasing the abundance of natural predators may prove effective in areas where rabbits are considered an agricultural pest. Compliance with ethical standards Manipulations of all animals reported in this study were approved by the Ethical Committee for Animal Experimentation of the University of Castilla La Mancha and in accordance with Spanish and European regulations (Law 32/2007, R.D. 1201/2005 and Council Directive 2010/63/EU). Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements Special thanks to C. Luna for his invaluable help in coordinating field activities, and all students, family and friends that collaborated in the fieldwork. C. Ferreira and F. Aparicio helped in setting up the experiment and provided technical advice. Funds for this study were provided by the Consejería de Agricultura (Junta de Andalucía), Federación Andaluza de Caza (FEDENCAFAC), and projects POII09-0099-2557 and CGL 2009-11665. ICB was supported by a pre-doctoral fellowship awarded by the Spanish Ministry of Education (AP2006-03576). C. Rouco was also supported by XXII Programa Propio de Investigación of the University of Córdoba and “Programa Operativo de Fondos FEDER Andalucía”. FST was supported by a PROMETEO grant (SENESCYT, Gobierno de Ecuador). References Banks, P.B., Hume, I.D., Crowe, O., 1999. Behavioural, morphological and dietary response of rabbits to predation risk from foxes. Oikos 85, 247–256. Barrio, I.C., Acevedo, P., Tortosa, F.S., 2010a. Assessment of methods for estimating wild rabbit population abundance in agricultural landscapes. Eur. J. Wildl. Res. 56, 335–340. Barrio, I.C., Bueno, C.G., Tortosa, F.S., 2010b. Alternative food and rabbit damage in vineyards of southern Spain. Agric., Ecosyst. Environ., Appl. Soil Ecol. 138, 51–54. Barrio, I.C., Villafuerte, R., Tortosa, F.S., 2012. Can cover crops reduce rabbit-induced damages in vineyards in southern Spain? Wildl. Biol. 18, 88–96. Barrio, I.C., Bueno, C.G., Villafuerte, R., Tortosa, F.S., 2013. Rabbits, weeds and crops: Can agricultural intensification promote wildlife conflicts in semiarid agro-ecosystems? J. Arid Environ. 90, 1–4. Boutin, S., 1984. Effect of late winter food addition on numbers and movements of snowshoe hares. Oecologia 62, 393–400. Boutin, S., 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems and the future. Can. J. Zool. 68, 203–220. Buenestado, F.J., Ferreras, P., Delibes-Mateos, M., Tortosa, F.S., Blanco-Aguiar, J.A., Villafuerte, R., 2008. Habitat selection and home range size of red-legged partridges in Spain. Agric., Ecosyst. Environ., Appl. Soil Ecol. 126, 158–162. Carpio, A.J., Soriano, M.A., Guerrero-Casado, J., Prada, L.M., Tortosa, F.S., Lora, Á., Gómez, J.A., 2017. Evaluation of an unpalatable species (Anthemis arvensis L.) as an alternative cover crop in olive groves under high grazing pressure by rabbits. Agric. Ecosyst. Environ. 246, 48–54. Conover, M., 2001. Resolving Human-wildlife Conflicts. The Science of Wildlife Damage Management. Lewis Publishers, Boca Raton. Cowan, D.P., 1987. Aspects of the social organisation of the European wild rabbit (Oryctolagus cuniculus). Ethology 75, 197–210. Daniels, M.J., Lees, J.D., Hutchings, M.R., Greig, A., 2003. The ranging behaviour and habitat use of rabbits on farmland and their potential role in the epidemiology of paratuberculosis. Vet. J. 165, 248–257.
39
Delibes-Mateos, M., Ferreras, P., Villafuerte, R., 2008. Rabbit populations and game management: the situation after 15 years of rabbit haemorrhagic disease in central-southern Spain. J. Biodivers. Conserv. Bioresour. Manag. 17, 559–574. Delibes-Mateos, M., Ferreras, P., Villafuerte, R., 2009. European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula. Mamm. Rev. 39, 124–140. Delibes-Mateos, M., Ferreira, C., Rouco, C., Villafuerte, R., Barrio, I.C., 2014. Conservationists, hunters and farmers: the European rabbit Oryctolagus cuniculus management conflict in the Iberian Peninsula. Mamm. Rev. 44, 190–203. Delibes-Mateos, M., Farfán, M.A., Rouco, C., Olivero, J., Márquez, A.L., Fa, J.E., Vargas, J.M., Villafuerte, R., 2018. A large-scale assessment of European rabbit damage to agriculture in Spain. Pest Manage. Sci. 74, 111–119. Devillard, S., Aubineau, J., Berger, F., Bergerb, F., Leonard, Y., Roobrouckb, A., Marchandeau, S., 2008. Home range of the European rabbit (Oryctolagus cuniculus) in three contrasting French populations. Mamm. Biol. 73, 128–137. Efford, M.G., Dawson, D.K., Jhala, Y.V., Qureshi, Q., 2016. Density-dependent home-range size revealed by spatially explicit capture–recapture. Ecography 39, 676–688. Eide, N.E., Jepsen, J.U., Prestrud, P., 2004. Spatial organization of reproductive Arctic foxes Alopex lagopus: responses to changes in spatial and temporal availability of prey. J. Anim. Ecol. 73, 1056–1068. Ferguson, S.H., Taylor, M.K., Born, E.W., Rosing-Asvid, A., Messier, F., 1999. Determinants of home range size for polar bears (Ursus maritimus). Ecol. Lett. 2, 311–318. Fox, A.D., Elmberg, J., Tombre, I.M., Hessel, R., 2017. Agriculture and herbivorous waterfowl: a review of the scientific basis for improved management. Biol. Rev. 92, 854–877. Gonc¸alves, H., Alves, P.C., Rocha, A., 2002. Seasonal variation in the reproductive activity of the wild rabbit (Oryctolagus cuniculus algirus) in a Mediterranean ecosystem. Wildl. Res. 29, 165–173. Goodrich, J.M., Buskirk, S.W., 1995. Control of abundant native vertebrates for conservation of endangered species. Cons. Biol. 9, 1357–1364. Hulbert, I.A.R., Iason, G.R., Elston, D.A., Racey, P.A., 1996. Home-range sizes in a stratified upland landscape of two lagomorphs with different feeding strategies. J. Appl. Ecol. 33, 1479–1488. Johnson, D.D.P., Kays, R., Blackwell, P.G., Macdonald, D.W., 2002. Does the resource dispersion hypothesis explain group living? Trends Ecol. Evol. 17, 563–570. Kauhala, K., Hiltunen, M., Salonen, T., 2005. Home ranges of mountain hares Lepus timidus in boreal forests of Finland. Wildl. Biol. 11, 193–200. Kenward, R.E., 2001. A Manual for Wildlife Radiotagging. Academic Press, London. Laver, P.N., Kelly, M.J., 2008. A critical review of home range studies. J. Wildl. Manage. 72, 290–298. Lombardi, L., Fernández, N., Moreno, S., 2007. Habitat use and spatial behaviour in the European rabbit in three Mediterranean environments. Basic Appl. Ecol. 8, 453–463. Marboutin, E., Aebischer, N.J., 1996. Does harvesting arable crops influence the behaviour of the European hare Lepus europaeus? Wildl. Biol. 2, 83–91. McLoughlin, P.D., Ferguson, S.H., 2000. A hierarchical pattern of limiting factors helps explain variation in home range size. Ecoscience 7, 123–130. Mitchell, M.S., Powell, R.A., 2004. A mechanistic home range model for optimal use of spatially distributed resources. Ecol. Model. 177, 209–232. Moreno, S., Beltran, J.F., Cotilla, I., Kuffner, B., Laffite, R., Jordan, G., Ayala, J., Quintero, C., Jimenez, A., Castro, F., Cabezas, S., Villafuerte, R., 2007. Long-term decline of the European wild rabbit (Oryctolagus cuniculus) in south-western Spain. Wildl. Res. 34, 652–658. Moseby, K.E., De Jong, S., Munro, N., Pieck, A., 2005. Home range, activity and habitat use of European rabbits (Oryctolagus cuniculus) in arid Australia: implications for control. Wildl. Res. 32, 305–311. Petrovan, S.O., Dixie, J., Yapp, E., Wheeler, P.M., 2017. Bioenergy crops and farmland biodiversity: benefits and limitations are scale-dependant for a declining mammal, the brown hare. Eur. J. Wildl. Res. 63, 49. R Development Core Team, URL: 2018. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/. Rouco, C., Villafuerte, R., Castro, F., Ferreras, P., 2011. Responses of naïve and experienced European rabbits to predator odour. Eur. J. Wildl. Res. 57, 395–398. Rouco, C., Norbury, G.L., Smith, J., Byrom, A.E., Pech, R., 2013. Population density estimates of brushtail possums (Trichosurus vulpecula) in dry grassland in New Zealand. N. Z. J. Ecol. 37, 12–17. Rouco, C., Norbury, G.L., Anderson, D.P., 2017. Movements and habitat preferences of pest help to improve population control: the case of common brushtail possums in New Zealand dryland ecosystem. Pest Manage. Sci. 7, 287–294. Schmutz, J.A., White, G.C., 1990. Error in telemetry studies: effects of animal movement on triangulation. J. Wildl. Manage. 54, 506–510. Seaman, E., Millspaugh, J.J., Kernohan, B.J., Brundige, G.C., Raedeke, K.J., Gitzen, R.A., 1999. Effects of sample size on kernel home range estimates. J. Wildl. Manage. 63, 739–747. Smith, G.C., Prickett, A.J., Cowan, D.P., 2007. Costs and benefits of rabbit control options at the local level. Int. J. Pest. Manage. 53, 317–321. Stott, P., 2003. Use of space by sympatric European hares (Lepus europaeus) and European rabbits (Oryctolagus cuniculus) in Australia. Mammal. Biol. Zeitschrift für Säugetierkunde 68, 317–327. Trout, R.C., 2002. Rabbits in the farmland ecosystem. In: Tattersall, F., Manley, W. (Eds.), Farming and Mammals. Linnean Society, London.
40
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
Tulloch, A.I.T., Nicol, S., Bunnefeld, N., 2014. Quantifying the expected value of uncertain management choices for over-abundant Greylag Geese. Biol. Conserv. 214, 147–155. Van Vuren, D., Smallwood, K.S., 1996. Ecological management of vertebrate pests in agricultural systems. Biol. Agric. Hort. 13, 41–64. Villafuerte, R., 1994. Riesgo De Predación Y Estrategias Defensivas Del Conejo En El ˜ University of Córdoba, PhD thesis. Parque Nacional De Donana. Villafuerte, R., Kufner, M.B., Delibes, M., Moreno, S., 1993. Environmental factors influencing the seasonal daily activity of the European rabbit (Oryctolagus cuniculus) in a Mediterranean area. Mammalia 57, 341–347.
Vitousek, P.M., Mooney, H.A., Lubchenco, J., Melillo, J.M., 1997. Human domination of Earth’s ecosystems. Science 277, 494–499. White, G.C., Garrot, R.A., 1990. Analysis of Wildlife Radio-tracking Data. Academic Press, Inc., San Diego, CA. White, P.C.L., Newton-Cross, G.A., Gray, M., Ashford, R., White, C., Saunders, G., 2003. Spatial interactions and habitat use of rabbits on pasture and implications for the spread of rabbit haemorrhagic disease in New South Wales. Wildl. Res. 30, 49–58.
Contents lists available at ScienceDirect
Mammalian Biology journal homepage: www.elsevier.com/locate/mambio
Original investigation
Supplementary food reduces home ranges of European wild rabbits in an intensive agricultural landscape Carlos Rouco a,∗,1 , Isabel C. Barrio a,∗∗,1,2 , Francesca Cirilli a , Francisco S. Tortosa a,b , Rafael Villafuerte c a
Department of Zoology, University of Cordoba. Campus de Rabanales, 14071 Córdoba, Spain Escuela Superior Politécnica Agropecuaria de Manabí, Calceta, Ecuador c Instituto de Estudios Sociales Avanzados (IESA-CSIC), Campo Santo de los Mártires, 14004 Córdoba, Spain b
a r t i c l e
i n f o
Article history: Received 1 October 2018 Accepted 22 January 2019 Available online 8 February 2019 Handled by Heiko G. Rödel Keywords: Food availability Use of space Lagomorph Management Vertebrate pest Wildlife damage
a b s t r a c t Understanding use of space in free ranging populations that cause damage to agriculture can help in the design of measures aimed at reducing their impact. Food availability is known to determine use of space in terrestrial vertebrates so, providing alternative food sources during a specific time period may help the management of vertebrate pests by reducing their ranging behavior. We investigated space use by a crop damaging species, the European wild rabbit (Oryctolagus cuniculus), in an intensively-managed agricultural landscape within its native range and evaluated the potential of food availability to restrict areas of rabbit activity. We determined the size of day-time home range (95% minimum convex polygon, MCP) and core area (50% MCP) of rabbits before and after providing additional food to one rabbit population, while an unsupplemented population served as a control. Rabbits in the study area had large home ranges in comparison with those previously reported in the literature, probably linked to the heterogeneous and unpredictable distribution of resources in intensively-managed Mediterranean agro-ecosystems. There was a general reduction in size of home ranges and core areas between the experimental phases, but we found evidence that additional feeding restricted the space use of rabbits. The wide-ranging behavior of rabbits documented in the present study might explain why even moderate rabbit densities can cause widespread damage to crops. These findings may facilitate the design of management tools to mitigate damage in agricultural areas where rabbits are considered an agricultural pest. ¨ Saugetierkunde. ¨ Published by Elsevier GmbH. All rights reserved. © 2019 Deutsche Gesellschaft fur
Introduction Overabundant herbivores can pose serious threats to crops (Conover, 2001; Tulloch et al., 2014; Fox et al., 2017). Community and ecosystem degradation as a consequence of human activities can favor range expansions and higher densities of generalist species (Goodrich and Buskirk, 1995), and intensively-managed ecosystems can provide gaps for opportunistic species (Vitousek et al., 1997). That seems to be the case of the European rabbit (Oryctolagus cuniculus) in some areas within its native range. Despite
∗ Corresponding author. ∗∗ Corresponding author at: Agricultural University of Iceland, Árleyni 22, 112 Reykjavik, Iceland. E-mail addresses: [email protected], [email protected] (C. Rouco), [email protected] (I.C. Barrio). 1 Both authors contributed equally to this work. 2 Present address: Agricultural University of Iceland, Árleyni 22, 112 Reykjavik, Iceland.
a sharp decline of the species in the last decades (Moreno et al., 2007; Delibes-Mateos et al., 2009), rabbit populations seem to be recovering in some agricultural areas of southern Spain (Carpio et al., 2017; Delibes-Mateos et al., 2018). Positive trends in rabbit numbers are probably associated with favorable conditions, such as the occurrence of soft soils that enable warren digging, and reduced predation pressure linked to predator control by hunters (Delibes-Mateos et al., 2008). In many areas where they have been introduced, rabbits have been described as one of the most damaging pests (Smith et al., 2007). Although in their native range they do not reach such high densities (Barrio et al., 2010a; Delibes-Mateos et al., 2014), increasing concerns arise because of the damage they cause to crops (Barrio et al., 2010b). Effective management of vertebrate pests in agricultural systems should incorporate knowledge of temporal and spatial dynamics of pest species (Van Vuren and Smallwood, 1996). In this sense, understanding space use of rabbits in these areas may assist in the design of effective measures aimed at reducing their impacts. However, most work on rabbit use of space has been conducted
https://doi.org/10.1016/j.mambio.2019.01.006 ¨ Saugetierkunde. ¨ Published by Elsevier GmbH. All rights reserved. 1616-5047/© 2019 Deutsche Gesellschaft fur
36
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
in areas where the species has been introduced (Hulbert et al., 1996; Stott, 2003; White et al., 2003; Moseby et al., 2005; Devillard et al., 2008) or in semi-natural habitats within its native range (Villafuerte, 1994; Lombardi et al., 2007). Information is scarce from agricultural areas within its native range where they cause damage to crops. Space use is a function of habitat productivity, resource distribution, the area used during migration or dispersal periods, or individual energy requirements (McLoughlin and Ferguson, 2000; Mitchell and Powell, 2004). Habitats with high resource availability allow individuals to meet their daily and seasonal needs within relatively small areas, but if resources are low or heterogeneous in space or time, larger areas might be needed (Ferguson et al., 1999; Johnson et al., 2002; Petrovan et al., 2017). In this sense, patchy spatial distribution and ephemeral availability of resources linked to intensively-managed semi-arid Mediterranean environments may force rabbits to range over longer distances to fulfill their nutritional requirements, potentially increasing the spread of damage to agricultural crops. In many terrestrial vertebrates, home range size decreases with increasing food availability (e.g. Hulbert et al., 1996), and experimental provision of food usually reduces home range sizes (Boutin, 1990). Alternative food availability reduces rabbit damage to crops (Barrio et al., 2010b) and might also affect space use of rabbits (Barrio et al., 2012) but the use of supplementary food as a management tool remains understudied. The aim of this study was 1) to investigate the space use of wild rabbits in an intensively-managed agricultural landscape; and 2) to evaluate the role of food availability in space use by rabbits. We determined home range and core area sizes before and after providing food to one rabbit population, while an unsupplemented population served as a control. We expected that an experimental increase in food availability would reduce home ranges and core areas sizes of wild rabbits, thereby potentially minimizing the extent of rabbits’ damage to crops.
Material and methods Study area The study was conducted in an agricultural area within Córdoba province, southern Spain (37◦ 33 N, 4◦ 37 W). Climate is dry Mediterranean, with average annual rainfall of 500 mm and average monthly temperatures 8–26 ◦ C. Intensive agriculture is the dominant land use in the area with the main crops being olive groves, vineyards, and cereals. Alternative food sources for rabbits (i.e. herbaceous vegetation other than crops) are scarce in the dominant crops because of extensive application of herbicides (Barrio et al., 2013). Rabbits occur in moderate numbers (Barrio et al., 2010a) and cause damage to crops, especially to vineyards early in the growing season (March-April; Barrio et al., 2013).
Experimental design Two rabbit populations (>1.5 km) were selected to run the experiment during spring-summer 2009. Both populations were similar in terms of rabbit density (around 1.28 rabbits/ha, Barrio et al., 2010a; Delibes-Mateos et al., 2014), warren availability (0.37 and 0.42 warrens/ha; surveyed in a 0.5 km radius area for each population), habitat structure, in terms of herbaceous, shrub and tree cover (Barrio and Cirilli, unpublished data; assessed along 6 50 m randomly selected transects at each population), and carnivore presence (5.5 and 6 scats/km, assessed along a 2 km transect at each population), mainly red fox (Vulpes vulpes), although other predators like European polecat (Mustela putorius), common genet
(Genetta genetta), Egyptian mongoose (Herpestes ichneumon) and domestic dogs (Canis familiaris) were also present. The experiment was structured in two phases. In the first part of the experiment (phase 0; March-May), we assessed home ranges of both rabbit populations in an intensive agricultural landscape. In the second part of the experiment, we randomly chose one of the populations (group A) and provided it with supplementary food (i.e. fresh alfalfa Medicago sativa close to warren entrances), whereas the other population (group B) remained as a control. After a one-week acclimation period with supplementary food we started monitoring the animals again (phase 1; May-July). Supplementary food was placed close to the warren entrances of the focal group, to ensure that only rabbits from that group would have access to it. Rabbits readily consumed the supplementary food, so fresh alfalfa was provided twice a week to ensure it was never exhausted. The experiment thus covered the end of the breeding period (phase 0) and the annual peak in rabbit abundance (phase 1) when juveniles are recruited to the population (Gonc¸alves et al., 2002). We also estimated rabbit abundance by means of pellet counts in 10 randomly placed 0.5 m2 sampling points once in each site and at the end of each phase (May 20 and June 29). These counts represent accumulated pellets over time. Rabbit monitoring Rabbits were caught with ferrets (i.e. chased using trained ferrets into nets placed at the warren exits), and all were weighed and sexed at capture, but only adult rabbits (>900 g; range 935 to 1530 g, Villafuerte, 1994) were equipped with a radio collar (AVM Instrument Company, Ltd., U.S.A.). All collars had a motion link device, which generates a different pulse rate after 4 h of inactivity (mortality sensor). When rabbit locations did not change for more than two days and the activity sensor of the collar indicated that the rabbit was not moving, the collars were retrieved. We radio-collared a total of 30 adult rabbits during the entire experiment but locations were only available for the two phases of the experiment for 20 rabbits, 12 in group A (i.e. 5 ♂ and 7 ♀) and 8 in group B (i.e. 3 ♂ and 5 ♀). To locate rabbits in the field we used a portable receiver (R-1000 Communications Specialists, Inc., California, U.S.A.) and a handheld three-element Yagi antenna (BIOTRACK, Wareham, UK) with transmitters’ frequencies within the 150–152 MHz range. Rabbits were located daily from at least two mapped receiving points within the shortest time possible between fixes, by using standard triangulation techniques for mobile triangulation systems (White and Garrot, 1990). In order to reduce errors, bearings of the tagged animals (compass bearings from true North, Schmutz and White, 1990) were taken by the same two observers (ICB and FC), and we only located rabbits during the day, when they are less mobile (i.e. Villafuerte et al., 1993). We calculated the location error of our triangulation measurements by placing radio-collars in the field and recording their exact geographic position with a GPS. We located the collars from the mapped receiving points following the same procedure as for rabbits. We calculated location error for each triangulation (i.e. pair of locations) as the distance (m) between the true position of the radio-collar and the location obtained after triangulation (Schmutz and White, 1990; Kauhala et al., 2005). Location error increased for each triangulation with the maximum distance between the receiving point and the corresponding location (maximum location distance; R2 = 0.407; F1,98 = 67.32; p < 0.001). We further considered only those triangulations for which both location distances between the observer and the rabbit were < 2000 m, which yielded a median error estimate of 92.44 m (median absolute deviation = 70.48 m; n = 60; range = 5.19–377.60 m). Discarding extremely biased triangulations reduced our data to 76.6% of its original size (from 1503 to 1152 triangulations). Observer identity (FC or ICB) did
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
not have a significant effect on location error (ANOVA; F1,31 = 0.019; p = 0.890). Each rabbit was located once a day, for a total of 46 survey days during the first phase (i.e. phase 0) and 38 days during the second phase of the experiment (i.e. phase 1). Additionally, we used the “homing-in” method (White and Garrot, 1990) once a week, to locate resting sites and assess warren fidelity. Rabbits were considered to be attached to the same warren when most locations (>75%) occurred within their main warren or in the close vicinity (i.e. other warrens or surface refuges < 100 m from their main warren, Cowan, 1987). Within 3 months of the end of the experiment, 89% of the collars were recovered through non-specific hunting (44%) or ferreting (56%), i.e. not intended specifically at recovering the collars, but as part of the regular hunting season (October-December, and additionally in some areas July-September for rabbit control, Barrio et al., 2013) or ferreting for population control in the study area.
37
rabbit population, group A or B, and the phase of the experiment, phase 0 or phase 1), and sex of the rabbit, as male and female rabbits may use space differently, particularly during the breeding season (Devillard et al., 2008). Differences in rabbit abundance based on the pellet counts between the two populations in the two phases of the experiment, were assessed using a Linear Model (LM), where pellet density was included as a response variable, and treatment (as defined above) was included as a predictor variable. Modelling assumptions were validated by visually inspecting the residuals of the models. We performed all statistical analyses in R 3.5.1 (R Development Core Team, 2018), using the packages lme4 and lmerTest for calculating Satterthwaite approximations of p-values for LMMs. Global significance of variables with several levels (e.g. treatment) was assessed by comparing models with and without the predictor variable; F values and the associated p-values are reported in these cases. For comparisons between treatment levels in LMM t-values and the associated p-values are reported.
Home range size and core area size estimation We estimated home range sizes and core areas for each rabbit and phase of the experiment using the Minimum Convex Polygon method (MCP) with two levels of outlier exclusion: 95% MCP to estimate the activity area of the rabbits (hereafter ‘home range’) and 50% MCP to estimate the restricted core area of the home range (hereafter ‘core area’) of each individual (Devillard et al., 2008). Although the MCP has been criticized because it includes areas rarely visited and thus may overestimate home range (Laver and Kelly, 2008), its use is still widespread and helpful to compare results among studies. We use it here as a relative measure of home range size and for ease of comparisons with other published data. Other methods, like kernels or the k-nearest neighbours convex hull, are sensitive to aggregated data, with potential lack of convergence in the smoothing parameters (Devillard et al., 2008). Since we only used locations collected during the day, data was expected to be highly aggregated. Finally, kernel density estimates were not used because to the recommendation of gathering at least 30 observations per animal (ideally 50) to obtain an accurate estimate was not reached (Seaman et al., 1999). To calculate the appropriate number of locations needed to correctly estimate home range size we followed the incremental area analysis (Kenward, 2001), which assumes that home range estimates reach an asymptote with an adequate sample size. For each rabbit and phase, we drew the relationship between the estimated 95% MCP home range size and the number of locations used in the estimation, with a bootstrapping approach (500 random samples of k locations, varying k from 5 to the total number of locations for each rabbit). For each value of k we estimated the mean 95% MCP over the 500 bootstrap samples. The appropriate number of locations kopt to estimate home range size for each rabbit-phase combination was the value of k for which the estimated home range size was at least equal to 95% of the home range size estimated with the full set of locations (i.e. when the asymptote is reached, Devillard et al., 2008). The median value of kopt for each phase was calculated (kopt was 18.5 and 16.5 for phase 0 and phase 1, respectively). Statistical analysis To evaluate if our treatment of supplementary feeding affects home range and core area sizes of rabbits in an agricultural landscape, we built two Linear Mixed Effects Models (LMM), where the response variables were the home range and core area sizes, respectively. We included rabbit identity as a random effect to account for repeated measures of each rabbit in the two experimental phases. As predictor variables we included the additive effects of treatment (as a variable with four levels resulting from the combination of the
Results The mean (± SE) number of fixes collected per animal during phase 0 and phase 1 was 17.8 (± 1.7) and 33.7 (± 4.4), respectively. Warren fidelity was high throughout the study, with most animals (88.9%) remaining within their original group of warrens. We found no significant differences in rabbit abundance between groups and phases during the study (LM, F36,39 = 0.496, p = 0.688), as assessed by pellet counts (means ± SE: group A phase 0: 40.3 ± 50.4 pellets/m2 ; phase 1: 31.6 ± 20.4 pellets/m2 ; group B phase 0: 22.8 ± 27.0 pellets/m2 ; phase 1: 27.8 ± 26.8 pellets/m2 ). Effect of supplementary feeding on home range and core area size Before adding supplementary food (i.e. in phase 0) rabbits in group A had significantly larger home ranges and core areas than rabbits in group B (LMM; home range: t34.95 = -2.32, p = 0.026; core area: t35 = -3.96, p < 0.001; Fig. 1). For both populations home ranges and core areas were significantly larger during phase 0 than during phase 1 (Fig. 1), but these reductions were only significant for group A (LMM; home range: t18 = -2.80, p = 0.011; core area: t35 = -3.27, p = 0.002; Fig. 1). Supplementary food reduced rabbit home ˜ range in group A by 52%. Reductions in home range and core areas of the control population (i.e. group B) between the two phases ˜ (i.e. 25%) were not statistically significant (LMM; home range: t18 = -0.57, p = 0.579; core area: t35 = -0.90, p = 0.374; Fig. 1). Sex had no significant influence on home range or core area size (LMM; home range: t17 = -0.90, p = 0.374; core area: t35 = 1.44, p = 0.160). Discussion In the present study we report for the first time the space use of rabbits in intensively-managed agricultural landscapes where they cause damage to crops (Barrio et al., 2010b). The two rabbit populations differed in their home range sizes before the experimental addition of food, and both populations reduced their home range during the second phase of the experiment, but this reduction was stronger for rabbits with experimentally increased food availability. In light of our results, potential management implications can be derived, suggesting an avenue for future investigations. Space use of rabbits in agricultural landscapes Day-time home range sizes of rabbits inhabiting intensivelymanaged agricultural landscapes in Southern Spain were surprisingly large (average for both populations in phase 0:
38
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
Fig. 1. Home range (a) and core area sizes (b) of two rabbit populations in an agricultural landscape of southern Spain, in the two phases of a supplementary feeding experiment. Phase 0 reflects unmanipulated conditions for both populations (group A and B), while in phase 1 group A was provided with supplementary food and group B remained as a control. Group A included 12 rabbits and group B included 8 rabbits. Home range size (ha) was estimated with Minimum Convex Polygons (MCP) at 95% and core areas size estimated with MCP at 50%; means and standard errors are shown. Small-case letters on the bars indicate significant differences (p < 0.05) between groups. Note the differences in scaling between y-axes in (a) and (b).
mean ± SE = 9.63 ± 3.12 ha; Fig. 1) in comparison to those MCP estimates quoted in the literature (e.g. 6 ha Hulbert et al., 1996; 3.5 ha Moseby et al., 2005; < 2 ha Devillard et al., 2008). Rabbits are crepuscular animals, so we would expect even larger home range sizes at night (Villafuerte, 1994). Although seasonal differences have been documented with larger home ranges in spring (Lombardi et al., 2007; Devillard et al., 2008), our results are much larger than those referred in other agricultural landscapes (Daniels et al., 2003; Stott, 2003). In many mammal species, home range size depends on population density (Efford et al., 2016). The large home ranges found in our study could be explained in part by the moderate rabbit densities in our study area (1.28 rabbits/ha, Barrio et al., 2010a), compared to areas with considerably higher rabbit densities where rabbits had smaller home ranges (e.g. 5 rabbits/ha, Devillard et al., 2008). This phenomenon has been also reported for other game species in intensively managed agroecosystems in Europe (e.g. brown hares Lepus europaeus; Marboutin and Aebischer, 1996), or red legged partridges Alectoris rufa; Buenestado et al., 2008) or other vertebrate pest species like the brushtail possum (Trichosurus vulpecula) in New Zealand (Rouco et al., 2017). It has also been argued that enlarged home ranges could result from frequent human disturbance in these environments (Buenestado et al., 2008; Devillard et al., 2008). Large home range sizes might also be an adaptive strategy to cope with environmental heterogeneity and unpredictable resource distribution (Ferguson et al., 1999; Eide et al., 2004; Rouco et al., 2013), as well as low food availability (Petrovan et al., 2017). Larger home ranges would indicate an increased exploratory behavior in search for the scarce and patchily distributed food, to ensure meeting the individuals’ energetic requirements. Travelling long distances to feed on better quality forage has been described for rabbits inhabiting resource-limited environments (Trout, 2002) and hares (Petrovan et al., 2017). In addition, the low predation rates found in our study area may favor this strategy. Banks et al. (1999) found that in an area where red foxes had been removed, rabbits moved farther from cover than in an area where predators were present, due to a reduction in perceived predation risk. This behaviour has also been observed in rabbits held in seminatural conditions within the species native range (Rouco et al.,
2011). Thus, a combination of scattered food sources, reduced perceived predation risk and nearly constant human disturbance may be driving the large home ranges found in this agricultural area. Effects of food availability on space use of rabbits Home range size in lagomorphs has shown to be negatively correlated with the abundance of food (e.g. snowshoe hare Lepus americanus, Boutin, 1984; mountain hare Lepus timidus, Hulbert et al., 1996; Kauhala et al., 2005) and with rabbit density (Devillard et al., 2008). In the present study, we found a significant effect of supplementary feeding on the spatial behavior of rabbits, reducing their home range sizes. Both rabbit populations reduced their home range size and core area sizes across the phases of the experiment. Such reductions can be expected, since home ranges of rabbits are larger during the breeding season and decrease thereafter (Devillard et al., 2008). Our study overlapped with most of the rabbit breeding season in Mediterranean habitats (which peaks between March and April, Gonc¸alves et al., 2002), especially during the first phase. However, the addition of supplementary food in group A seemed to synergize home range reduction, likely due to both; easy access to food resources, and the end of the breeding season. It is noteworthy, that enhanced food availability did not locally increase rabbit abundance in the short term (the 2-month-long second phase of this experiment when supplementary food was provided); therefore, density-dependent factors may not be confounding the effects of food supplementation on home range sizes in the present study. However, this possibility needs to be taken into account if supplementary feeding is to be used as a management strategy, as it has the potential to increase rabbit densities in the medium and long term. Management implications Food availability has proven to reduce rabbit damage, at least to vineyards (Barrio et al., 2010b), and our results revealed that food availability does limit the ranging behavior of rabbits in an agricultural landscape. By having easy access to food, rabbits are
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
not forced to range widely to find less common food sources in order to reach their nutritional requirements. Therefore, the use of supplementary feeding could reduce the likelihood of rabbit damage to agriculture, potentially mitigating hunters-farmers conflict (Delibes-Mateos et al., 2014). In addition, reducing rabbits’ ranging behavior, in combination with other practices that reduce rabbit densities through modifying cultural systems or increasing the abundance of natural predators may prove effective in areas where rabbits are considered an agricultural pest. Compliance with ethical standards Manipulations of all animals reported in this study were approved by the Ethical Committee for Animal Experimentation of the University of Castilla La Mancha and in accordance with Spanish and European regulations (Law 32/2007, R.D. 1201/2005 and Council Directive 2010/63/EU). Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements Special thanks to C. Luna for his invaluable help in coordinating field activities, and all students, family and friends that collaborated in the fieldwork. C. Ferreira and F. Aparicio helped in setting up the experiment and provided technical advice. Funds for this study were provided by the Consejería de Agricultura (Junta de Andalucía), Federación Andaluza de Caza (FEDENCAFAC), and projects POII09-0099-2557 and CGL 2009-11665. ICB was supported by a pre-doctoral fellowship awarded by the Spanish Ministry of Education (AP2006-03576). C. Rouco was also supported by XXII Programa Propio de Investigación of the University of Córdoba and “Programa Operativo de Fondos FEDER Andalucía”. FST was supported by a PROMETEO grant (SENESCYT, Gobierno de Ecuador). References Banks, P.B., Hume, I.D., Crowe, O., 1999. Behavioural, morphological and dietary response of rabbits to predation risk from foxes. Oikos 85, 247–256. Barrio, I.C., Acevedo, P., Tortosa, F.S., 2010a. Assessment of methods for estimating wild rabbit population abundance in agricultural landscapes. Eur. J. Wildl. Res. 56, 335–340. Barrio, I.C., Bueno, C.G., Tortosa, F.S., 2010b. Alternative food and rabbit damage in vineyards of southern Spain. Agric., Ecosyst. Environ., Appl. Soil Ecol. 138, 51–54. Barrio, I.C., Villafuerte, R., Tortosa, F.S., 2012. Can cover crops reduce rabbit-induced damages in vineyards in southern Spain? Wildl. Biol. 18, 88–96. Barrio, I.C., Bueno, C.G., Villafuerte, R., Tortosa, F.S., 2013. Rabbits, weeds and crops: Can agricultural intensification promote wildlife conflicts in semiarid agro-ecosystems? J. Arid Environ. 90, 1–4. Boutin, S., 1984. Effect of late winter food addition on numbers and movements of snowshoe hares. Oecologia 62, 393–400. Boutin, S., 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems and the future. Can. J. Zool. 68, 203–220. Buenestado, F.J., Ferreras, P., Delibes-Mateos, M., Tortosa, F.S., Blanco-Aguiar, J.A., Villafuerte, R., 2008. Habitat selection and home range size of red-legged partridges in Spain. Agric., Ecosyst. Environ., Appl. Soil Ecol. 126, 158–162. Carpio, A.J., Soriano, M.A., Guerrero-Casado, J., Prada, L.M., Tortosa, F.S., Lora, Á., Gómez, J.A., 2017. Evaluation of an unpalatable species (Anthemis arvensis L.) as an alternative cover crop in olive groves under high grazing pressure by rabbits. Agric. Ecosyst. Environ. 246, 48–54. Conover, M., 2001. Resolving Human-wildlife Conflicts. The Science of Wildlife Damage Management. Lewis Publishers, Boca Raton. Cowan, D.P., 1987. Aspects of the social organisation of the European wild rabbit (Oryctolagus cuniculus). Ethology 75, 197–210. Daniels, M.J., Lees, J.D., Hutchings, M.R., Greig, A., 2003. The ranging behaviour and habitat use of rabbits on farmland and their potential role in the epidemiology of paratuberculosis. Vet. J. 165, 248–257.
39
Delibes-Mateos, M., Ferreras, P., Villafuerte, R., 2008. Rabbit populations and game management: the situation after 15 years of rabbit haemorrhagic disease in central-southern Spain. J. Biodivers. Conserv. Bioresour. Manag. 17, 559–574. Delibes-Mateos, M., Ferreras, P., Villafuerte, R., 2009. European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula. Mamm. Rev. 39, 124–140. Delibes-Mateos, M., Ferreira, C., Rouco, C., Villafuerte, R., Barrio, I.C., 2014. Conservationists, hunters and farmers: the European rabbit Oryctolagus cuniculus management conflict in the Iberian Peninsula. Mamm. Rev. 44, 190–203. Delibes-Mateos, M., Farfán, M.A., Rouco, C., Olivero, J., Márquez, A.L., Fa, J.E., Vargas, J.M., Villafuerte, R., 2018. A large-scale assessment of European rabbit damage to agriculture in Spain. Pest Manage. Sci. 74, 111–119. Devillard, S., Aubineau, J., Berger, F., Bergerb, F., Leonard, Y., Roobrouckb, A., Marchandeau, S., 2008. Home range of the European rabbit (Oryctolagus cuniculus) in three contrasting French populations. Mamm. Biol. 73, 128–137. Efford, M.G., Dawson, D.K., Jhala, Y.V., Qureshi, Q., 2016. Density-dependent home-range size revealed by spatially explicit capture–recapture. Ecography 39, 676–688. Eide, N.E., Jepsen, J.U., Prestrud, P., 2004. Spatial organization of reproductive Arctic foxes Alopex lagopus: responses to changes in spatial and temporal availability of prey. J. Anim. Ecol. 73, 1056–1068. Ferguson, S.H., Taylor, M.K., Born, E.W., Rosing-Asvid, A., Messier, F., 1999. Determinants of home range size for polar bears (Ursus maritimus). Ecol. Lett. 2, 311–318. Fox, A.D., Elmberg, J., Tombre, I.M., Hessel, R., 2017. Agriculture and herbivorous waterfowl: a review of the scientific basis for improved management. Biol. Rev. 92, 854–877. Gonc¸alves, H., Alves, P.C., Rocha, A., 2002. Seasonal variation in the reproductive activity of the wild rabbit (Oryctolagus cuniculus algirus) in a Mediterranean ecosystem. Wildl. Res. 29, 165–173. Goodrich, J.M., Buskirk, S.W., 1995. Control of abundant native vertebrates for conservation of endangered species. Cons. Biol. 9, 1357–1364. Hulbert, I.A.R., Iason, G.R., Elston, D.A., Racey, P.A., 1996. Home-range sizes in a stratified upland landscape of two lagomorphs with different feeding strategies. J. Appl. Ecol. 33, 1479–1488. Johnson, D.D.P., Kays, R., Blackwell, P.G., Macdonald, D.W., 2002. Does the resource dispersion hypothesis explain group living? Trends Ecol. Evol. 17, 563–570. Kauhala, K., Hiltunen, M., Salonen, T., 2005. Home ranges of mountain hares Lepus timidus in boreal forests of Finland. Wildl. Biol. 11, 193–200. Kenward, R.E., 2001. A Manual for Wildlife Radiotagging. Academic Press, London. Laver, P.N., Kelly, M.J., 2008. A critical review of home range studies. J. Wildl. Manage. 72, 290–298. Lombardi, L., Fernández, N., Moreno, S., 2007. Habitat use and spatial behaviour in the European rabbit in three Mediterranean environments. Basic Appl. Ecol. 8, 453–463. Marboutin, E., Aebischer, N.J., 1996. Does harvesting arable crops influence the behaviour of the European hare Lepus europaeus? Wildl. Biol. 2, 83–91. McLoughlin, P.D., Ferguson, S.H., 2000. A hierarchical pattern of limiting factors helps explain variation in home range size. Ecoscience 7, 123–130. Mitchell, M.S., Powell, R.A., 2004. A mechanistic home range model for optimal use of spatially distributed resources. Ecol. Model. 177, 209–232. Moreno, S., Beltran, J.F., Cotilla, I., Kuffner, B., Laffite, R., Jordan, G., Ayala, J., Quintero, C., Jimenez, A., Castro, F., Cabezas, S., Villafuerte, R., 2007. Long-term decline of the European wild rabbit (Oryctolagus cuniculus) in south-western Spain. Wildl. Res. 34, 652–658. Moseby, K.E., De Jong, S., Munro, N., Pieck, A., 2005. Home range, activity and habitat use of European rabbits (Oryctolagus cuniculus) in arid Australia: implications for control. Wildl. Res. 32, 305–311. Petrovan, S.O., Dixie, J., Yapp, E., Wheeler, P.M., 2017. Bioenergy crops and farmland biodiversity: benefits and limitations are scale-dependant for a declining mammal, the brown hare. Eur. J. Wildl. Res. 63, 49. R Development Core Team, URL: 2018. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/. Rouco, C., Villafuerte, R., Castro, F., Ferreras, P., 2011. Responses of naïve and experienced European rabbits to predator odour. Eur. J. Wildl. Res. 57, 395–398. Rouco, C., Norbury, G.L., Smith, J., Byrom, A.E., Pech, R., 2013. Population density estimates of brushtail possums (Trichosurus vulpecula) in dry grassland in New Zealand. N. Z. J. Ecol. 37, 12–17. Rouco, C., Norbury, G.L., Anderson, D.P., 2017. Movements and habitat preferences of pest help to improve population control: the case of common brushtail possums in New Zealand dryland ecosystem. Pest Manage. Sci. 7, 287–294. Schmutz, J.A., White, G.C., 1990. Error in telemetry studies: effects of animal movement on triangulation. J. Wildl. Manage. 54, 506–510. Seaman, E., Millspaugh, J.J., Kernohan, B.J., Brundige, G.C., Raedeke, K.J., Gitzen, R.A., 1999. Effects of sample size on kernel home range estimates. J. Wildl. Manage. 63, 739–747. Smith, G.C., Prickett, A.J., Cowan, D.P., 2007. Costs and benefits of rabbit control options at the local level. Int. J. Pest. Manage. 53, 317–321. Stott, P., 2003. Use of space by sympatric European hares (Lepus europaeus) and European rabbits (Oryctolagus cuniculus) in Australia. Mammal. Biol. Zeitschrift für Säugetierkunde 68, 317–327. Trout, R.C., 2002. Rabbits in the farmland ecosystem. In: Tattersall, F., Manley, W. (Eds.), Farming and Mammals. Linnean Society, London.
40
C. Rouco, I.C. Barrio, F. Cirilli, et al. / Mammalian Biology 95 (2019) 35–40
Tulloch, A.I.T., Nicol, S., Bunnefeld, N., 2014. Quantifying the expected value of uncertain management choices for over-abundant Greylag Geese. Biol. Conserv. 214, 147–155. Van Vuren, D., Smallwood, K.S., 1996. Ecological management of vertebrate pests in agricultural systems. Biol. Agric. Hort. 13, 41–64. Villafuerte, R., 1994. Riesgo De Predación Y Estrategias Defensivas Del Conejo En El ˜ University of Córdoba, PhD thesis. Parque Nacional De Donana. Villafuerte, R., Kufner, M.B., Delibes, M., Moreno, S., 1993. Environmental factors influencing the seasonal daily activity of the European rabbit (Oryctolagus cuniculus) in a Mediterranean area. Mammalia 57, 341–347.
Vitousek, P.M., Mooney, H.A., Lubchenco, J., Melillo, J.M., 1997. Human domination of Earth’s ecosystems. Science 277, 494–499. White, G.C., Garrot, R.A., 1990. Analysis of Wildlife Radio-tracking Data. Academic Press, Inc., San Diego, CA. White, P.C.L., Newton-Cross, G.A., Gray, M., Ashford, R., White, C., Saunders, G., 2003. Spatial interactions and habitat use of rabbits on pasture and implications for the spread of rabbit haemorrhagic disease in New South Wales. Wildl. Res. 30, 49–58.