Abstract
To avoid the possible extinction of the last native population of western Hermann’s tortoise in the Iberian Peninsula it is essential to make sound management decisions. Knowledge of macro and microhabitat use and home range size has considerable practical value for land managers. With this aim we first studied the home range and habitat preferences in western Hermann’s tortoises by radio tracking 15 adults weekly from March 2008 to May 2009 in three localities within the Albera population range (NE Iberian Peninsula). We estimated home ranges with Fixed Kernel estimator (FK) and Minimum Convex Polygon (MCP) after checking tortoise site fidelity. We observed that home range size did not differ significantly between males and females (mean FK = 2.01 ha, mean MCP = 3.01 ha). Secondly, we studied macrohabitat selection using a vegetation map. Preferred habitats were open shrubland, open forest and barren land during the activity period, and dense forest, dense shrubland and open shrubland during the hibernation. Next, we assessed microhabitat selection along five periods of the annual cycle: hibernation, emergence from hibernation, spring, summer and autumn. We then located marked tortoises weekly and classified the plant species observed in each location. Principal component analyses showed that tortoises selected shrubs with trees during hibernation, bramble during summer and herbaceous habitat during the breeding season. All these results can provide guidelines for management programs that set aside areas of habitat critical to conserve viable populations, although it is also important to prevent mortality from forestry works. We therefore tested a new brush cutter head accessory to achieve tortoise-safe undergrowth clearing. To this aim we distributed 52 frozen hybrid tortoises among eight plots of 100 m2, cleared six of these plots with the accessory and two without it, and evaluated the scars of the blade on caparaces. We observed no damage in plots that were cleared with the accessory but scars in most carapaces in the plots cleared without it (with potential mortality ranging from 40% in neonates to 100% in adults). These results outline the importance of supporting habitat management decisions with proper field studies.
Introduction
Of 37 extant and recent tortoise species, 30 are considered globally threatened or extinct, and two more are near-threatened (IUCN, 2014). Of the four tortoise species that occur in the Mediterranean Basin: the spur-thighed tortoise (Testudo graeca), the marginated tortoise (Testudo marginata), the Kleinmann’s tortoise (Testudo kleinmanni) and the Hermann’s tortoise (Testudo hermanni); Kleinmann’s tortoise is considered critically endangered and the western form of the Hermann’s tortoise (T. h. hermanni) is considered endangered. This subspecies and the eastern form (T. h. boetggeri) have a strictly European range and occupy mostly Mediterranean and sub-Mediterranean climatic areas (Fritz et al., 2006). The western Hermann’s tortoise has a highly fragmented and reduced distribution which includes a single native population in northern Iberian Peninsula, within the Albera mountain range (eastern Pyrenees, hereafter, Albera population). There are different factors currently blamed for the endangerment of western Hermann’s tortoise, mainly illegal harvesting, road casualties, wildfires, high nest and young predation, and habitat loss arising from land use changes (Cheylan, 1984; Guyot and Clobert, 1997; Longepierre and Grenot, 1998; van Dijk et al., 2004; Vilardell et al., 2008; Bertolero, 2010; Bertolero et al., 2011; Couturier et al., 2014). Tortoises are particularly vulnerable to habitat loss and fragmentation (Pough, 2004). Thus, tortoise conservation and management would benefit from quantification of habitat use.
Habitat selection studies compare habitat and resource availability to patterns of their use by animals (Alldredge and Griswold, 2006). A detailed knowledge of the habitat preferences of threatened species is essential the development of appropriate measures for their conservation (Wiktander et al., 2001). Habitat selection in tortoises and other reptiles is mostly explained by climate and topography (Guisan and Hofer, 2003). Recent studies that have been carried out in the Albera population stress the importance of landscape complexity for Hermann’s tortoise conservation and management (Casamitjana et al., 2012; Couturier et al., 2014). Home range size and habitat use are among the information needed to improve the management of T. h. hermanni populations, being a must for the adoption of effective conservation plans (Börger et al., 2008).
Home range (HR) is the area traversed in the course of an animal “normal activities” (Burt, 1943), e.g., food gathering, mating and caring for young. Included within the HR is the core area (CA), known as the area with an intensive use as a center of activity (Hayne, 1949; Hodder et al., 1998). The HR size is considered an important indicator of the behavioral and resource requirements of an animal (Perry and Garland, 2002). It may be useful to compare the HR requirements of particular individuals dwelling in different habitats, distant populations within a species or even different species (White and Garrot, 1990). All of an animal’s routine requirements must be found within the HR, including shelter and suitable thermal conditions (Christian et al., 1984; Huey et al., 1989).
One of the few effective methods used to study HR of cryptic reptiles is radio telemetry (Kenward, 2001; Wone and Beauchamp, 2003). This technique offers the advantage of repeated observation of known individuals so that tortoises can be located throughout the year, even when dense vegetation precludes effective visual searching. Periodic monitoring of individuals with radiotracking has been used to study activity patterns, daily distances traveled, type and use of resting sites, size and shape of home range, spatial relationships between individuals and preferences in use of habitat (Palomeros and Delibes, 1992). Specifically, the long-term home range of adults T. hermanni were 1.6-0.7 ha in males and 2.4-1.5 ha in females after studies conducted in France, Greece and Italy (Swingland et al., 1986; Hailey, 1989; Calozai and Chelazzi, 1991). The radiotracked western Hermann’s tortoises used different vegetation types during the breeding season and females moved nearly twice as far as males to find nesting sites (Longepierre et al., 2001; Mazzotti et al., 2002). Movements between areas of low food availability and cultivated areas have also been reported (Guyot, 1996). However, the conservation of wild populations has to rely on precise knowledge of the landscape where they occur and their habitat use across the annual cycle, and this information is still lacking for many isolated Hermann’s tortoise populations.
Location of the three study areas in the Albera Nature Reserve, included in the Natura 2000 network, Catalonia, Spain.
Citation: Amphibia-Reptilia 36, 1 (2015) ; 10.1163/15685381-00002971
Current tortoise habitat in the Albera provides both goods (wood, firewood, cork, pasture, fruits and mushrooms) and social services (historical and cultural heritage, biodiversity conservation, hunting, outdoor recreation etc). However, most woodland areas have been abandoned since the 1950s or are managed with low frequency and intensity. As a result, the Albera forests are now more extensive and denser than a century ago, following a usual pattern in Mediterranean mountains (Debussche et al., 1999). Today, the most widespread forest management technique in the Albera is, likely, undergrowth clearing (Casamitjana et al., 2012), used to prevent and fight wildfires, to facilitate cork extraction or to prepare for cattle grazing. Clearing is performed with tractor-mounted flail mowers or with hand trimmers that, besides temporal habitat destruction, can produce tortoise mortality (pers. obs.). On the other hand, good clearing practices may increase the extent of the optimal micro and macrohabitat for tortoises and can thus be a key tool for their conservation.
Individual home ranges (m2) of western Hermann’s tortoise using minimum convex polygon (MCP) and fixed kernel estimators 95% (K95) and 50% (K50) in the three study areas (A, B and C). Sex, number of locations excluding consecutive repeated locations ad used for estimates (N), site-fidelity test results report p.
The present study was designed to produce basic and applied information to help revered the decline of the Albera western Hermann’s tortoise population. Our specific aims were: (1) to determine home range sizes of adult tortoises (2) to analyze tortoise macrohabitat use during their activity periods and hibernation, (3) to assess microhabitat use across a year, and, (4) to apply habitat selection data to habitat management action, and (5) to design and test a forestry brush cutter head accessory aimed to reduce tortoise mortality during thinning tasks.
Material and methods
Study area
The Albera Nature Reserve, included in the Natura 2000 network, encompasses 4207 ha of wildland and crops in the northeastern Iberian Peninsula (42°25′N, 3°3′E). Field work was conducted in the Western part of this reserve (110 to 757 m above sea level), which is covered mostly by Mediterranean shrubland (dominated by 1-2 m high shrubs) and oak (Quercus suber and Quercus ilex) woodlands. We selected three study areas (A, B and C) that hold tortoise populations and are relatively free from human activities (fig. 1). The three localities were covered by vineyards and olive tree groves until the 1980s when they were abandoned. Afterwards, some properties planted pines Pinus pinea and P. halepensis in A and B and Quercus suber in C, while in neglected areas shrubland and oak woodlands developed.
Radio tracking
We used trained detector dogs to capture five wild adult tortoises at each study area in spring (table 1). We considered individuals with no clearly visible new growth laminae in caparace scutes to be adults (Bertolero et al., 2005). We handled all tortoises with disposable latex gloves to minimize the potential spread of pathogens between tortoises. The captured tortoises were marked: (a) by drilling holes on their marginal scutes to provide a permanent unique identification number (Cagle, 1939), (b) with passive integrated transponders (FriendChip ISO FDX-B, AVID, Avid Identification Systems, Inc., Norco, CA, USA), to provide a permanent unique identification that allow us recognize them in case of loss the radio-transmitter and loss of drilled holes, and (c) with radio-transmitters (TinyLoc S.L., Spain) that weighed 11 g (<5% of the adult’s body weight, White and Garrot, 1990), had an average life of 12 months, and a range of detection of 1000-2000 m under optimal conditions. Transmitters were externally attached to the first and fourth marginal right rear scutes because any other position could hamper successful copulation with females. Tags were glued on with synthetic resin (Demotec 90, Ankapodol, Spain), that is innocuous and inconspicuous, and had no observable effect on the behavior of radio-tagged specimens (pers. obs.). We located marked tortoises once a week from March 2008 to May 2009 using a portable receiver (R2 Tracer, TinyLoc S.L.) and a hand-held Yagi directional antenna. During the radiotracking period two tortoises were lost in area B, presumably pillaged, and their transmitter was lost. We recorded the coordinates of every tortoise location with a handhelds GPS device (GARMIN eTrex®), and the plant species that the tortoise’s body was touching. The exact location of the sites is kept confidential due to the threatened status of this subspecies.
Home range and core area estimation
We documented site fidelity with Spatial Analyst and Animal Movement (AMAE) extension for ArcView 3.2 (Hooge and Eichenlaub, 2000) and using mean squared distance (MSD) from the center of activity. MSD was calculated for every individual and was compared to 1000 randomly generated paths for each animal to test the null hypothesis of random movement (Hart and Fujisaki, 2010). If MSD based on actual movements was significantly lower than the mean distance of the 1000 random paths, the individual was considered to exhibit site fidelity (Spencer et al., 1990). The test is a modified Monte Carlo random walk, starting at the location of release and constrained by the study area. It uses the actual sequence of distances between position estimates (normality assessed with g1 and g2 tests (Sokal and Rohlf, 1981)) to determine walk points.
Then, HR and CA were derived from the weekly GPS locations of tortoises. We estimated, for the tortoises that showed site fidelity, individual HR size with Minimum Convex Polygon (MCP; Mohr, 1947) and 95% Fixed Kernel (FK; Worton, 1987), while the CA was estimated with 50% FK, all estimators calculated using the Arc-View™ extension package Animal Movement (Hooge and Eichenlaub, 2000). We used MCP because it is frequently used for reptiles offering an approximation to the maximum HR area, and to compare our results with studies on other European tortoise populations (Hailey, 1989; Calzolai and Chelazzi, 1991; Bossuto et al., 2000; Longepierre et al., 2001; Bertolero, 2002; Mazzotti et al., 2002), even though it often includes areas never used by the animal (Row et al., 2006). For this reason we also used Kernel estimator because is the most widely used for quantifying intensity of use, and is one of the most consistent and accurate methods available (Worton, 1989). We then considered consecutive locations for a given tortoise to be independent because they differed by more than 144 hours; this is a sufficient time for the species to move between any two points in the HR. However, if the animal did not move between consecutive tracking events we considered them dependent and retained only the first one. The median home range was used as a measure of central trend because data were not normally distributed. Sexual differences in home range size and core area were examined using Mann-Whitney U-tests.
Macrohabitat selection
To ascertain individual patterns of habitat use, we compared the observed number of radio-locations occurring in each habitat type to that to be expected based upon the proportion of each habitat that occurred within the HRs of the all tortoises radiotracked in each area together (global HR). The habitat type was obtained from landscape characterization based on manual photo interpretation of aerial orthoimages from 2008 (scale 1:5000, ©Institut Cartogràfic de Catalunya). Landscape patches were defined as vegetation areas of homogeneous height and cover. The minimum mapping unit was approximately 4 m2. The aerial photographs were digitized in vector format and the cover percentage of grass, shrub (up to 2 m) and tree (more than 2 m) were estimated following Etienne and Prado (1982). Afterwards, following Godron et al. (1968), the initial patch description was classified into nine habitat types (barren land, grassland, open shrubland, dense shrubland, wooded shrubland, wooded grassland-shrubland, open forest and dense forest) according to the estimated covers of shrub and tree, following an adaptation of the categories used in Roura-Pascual et al. (2005) (Appendix 1). We used ARCGIS v9.2 (©ESRI), to overlay GPS locations from each study tortoises with the vegetation map. The number of GPS locations within each of the nine habitat types was counted using the Hawth’s Tools extension. We then studied habitat use by performing a compositional analysis (Aebischer et al., 1993) based on a search for differences between available habitats and the habitats used by animals. Compositional analysis takes into account that each individual’s movements determine a trajectory through space and time, and habitat use is the proportion of that trajectory contained within each habitat type. We calculated the proportion of each tortoise’s observed locations in each habitat type (used habitat) and calculated the proportion of each habitat type within the global HR per each area (available habitat).
Habitat use was studied for winter inactivity period (hereafter referred to as ‘hibernation’), which included all the locations from November to February and for the activity period, which grouped the locations from March to October. We excluded consecutive repeated locations for the activity period because they denote inactivity (aestivation) and their inclusion in the analysis would have led to a description skewed towards their refuges instead of showing the habitat actually used for feeding, thermoregulation, egg-laying and courtship (Anadón et al., 2006). Missing values of use and availability were assigned values of 0.00001 (a value lower than any proportion of use or availability) as suggested by Aebischer et al. (1993). We analyzed these data using Resource Selection Analysis Software (Leban, 1999). For all statistical tests, probability values < 0.05 were considered significant.
Microhabitat selection
To investigate the seasonal change in microhabitat selection, we divided the year into five periods, consistent with the tortoise biological cycle: (1) hibernation, from 1st November to 28th February, when tortoises became inactive; (2) emergence from hibernation, 1st March to 30th April, when tortoises emerged and began to bask; (3) spring, 1st May to 30th June, main period of activity and nesting; (4) summer, 1st July to 31th August, when tortoises, influenced by high temperatures aestivate or reduce their activity in midday; (5) autumn, 1st September to 31th October, when late courtships occur and tortoises prepare to for hibernation. When a tortoise was radio-located, the plant species that touched its body and the number of physical contacts were noted. Plant species were grouped into six categories: aromatic, bramble, herbaceous, thorny shrub, tree and non-thorny shrubs (Appendix 2). The matrix including the number of contacts per plant category for each tortoise and biological season was analyzed with a Partial Principal Components Analysis (PCA), including tortoise sex as a covariate. The PCA was performed in Canoco (Ter Braak and Smilauer, 1998) to summarize microhabitat selection during the biological cycle in a reduced number of microhabitat gradients.
Habitat management
We first conducted a pilot study by reducing the shrub cover in 18 square plots of 100 m2 each, to provide open habitat that tortoises could used as nesting, feeding or thermoregulation areas (Vilardell et al., 2012). Plots located in study area C had already been cleared using brush cutters with two tooth blades to reduce shrub cover in May 2012. Based on this study and on previous results on habitat preferences, we conducted a larger habitat management trial in 2013.
This trial was conducted in 50 plots of 100 m2 each, distributed among five abandoned vineyards and olive groves, located in the three study areas (18 plots in A and 16 plots in B and C). Each plot was located 3 m apart from adjacent plots and had a high shrub cover (>65%) dominated by E. arborea. The initial shrub cover was reduced to 0-3% using a bush cutter on February 2013. A few plants such as Foeniculum vulgare, Spartium junceum, Rubus ulmifolius and E. arborea were preserved to mimic an ideal nesting site and provide some shelter for female tortoises. To avoid harming tortoises during clearing actions we used trained detector dogs to capture any tortoise occurring in the plot before cutting. Tortoises were returned after cutting was finished. The plots were then visited once a week from March until August to detect occurrence of tortoises. In August 2013 and 2014 we checked nest occurrence with trained detector dogs.
Test of a brush cutter head accessory
We designed a new accessory for the brush cutter heads used in current undergrowth clearing with the aim of reducing tortoise mortality. The accessory consists of an aluminum tube, welded in a collar nut M14x1.5 L/H that is attached to the angle transmission in the bottom of the brush cutter blade (fig. 2). To attach the accessory we used a spark plug socket wrench and one of the two through holes of the tube. We assessed the efficacy of this accessory at reducing tortoise mortality during a trial in August 2013. We distributed 104 frozen hybrid tortoises (5 yearlings of 5 cm plastron length, 5 juveniles of 10 cm plastron length and 3 adults of 16 cm plastron length per each plot) among eight plots of 100 m2 each, of the pilot study on habitat management. The frozen tortoises were randomly distributed under shrub regrowth (mean height of 73 cm). Thereafter, two plots were cleared with blades lacking the new head accessory, while the other six plots were cleared using it. We measured the impact (no damage, slight damage or scute damage, serious damage or broken bones and potential death or internal organs appear crushed) of the thinning in frozen hybrid tortoises according to the scars of the blade. The brush cutter used was STIHL FS550.
Half section views of the two designed brush cutter head accessories, the open habitat model (right), and the control regrowth model (left). A cutting line that passes only partially through the model view results in a partial section view. Measurements in centimeters.
Citation: Amphibia-Reptilia 36, 1 (2015) ; 10.1163/15685381-00002971
Results
The site fidelity test showed that 100% of all mean square distance values for actual movements by individual western Hermann’s tortoise were significantly () lower than corresponding values from simulated movements. Thus, all the radiotracked tortoises showed strong site fidelity (table 1). The average home range size of the 13 individuals was 2.01 ± 1.52 ha using 95% FK and 3.01 ± 2.4 ha using MCP. Home range and core area size did not significantly differ between the sexes (Mann-Whitney U-test, MCP: , , 95% FK: , ; 50% FK: , ).
We observed that the western Hermann’s tortoises used different macrohabitats during the activity season (, df = 7, ) and the hibernation season (, df = 6, ). Habitat availability also differed among study areas, which two of them lacking the grassland category (fig. 3). The most- to least-order of macrohabitat use during the activity period was Open shrubland > Open forest > Barren land > Wooded shrubland > Dense forest > Dense shrubland = Open woodland > Wooded grassland-shrubland. During hibernation the order was Dense forest > Dense shrubland > Open shrubland > Open forest > Barren land > Wooded shrubland > Wooded grassland-shrubland.
Habitat use and availability. Gray bars represent the mean proportion of habitat use by tortoise during the hibernation season. The white bars represent the mean proportion of habitat used by tortoises during the activity period. Error bars represent the standard error of habitat use. The black bars represent the proportion of habitat available within each study area.
Citation: Amphibia-Reptilia 36, 1 (2015) ; 10.1163/15685381-00002971
Partial principal component analysis (PCA) using the microhabitat categories described in Appendix 2. Loadings with absolute values greater than 0.5 are shown in bold.
The microhabitat analysis showed that the variables used explained 83% of the dataset variance (table 2). The first axis of the PCA explained 31% of total variance in microhabitat characteristics while the second axis explained a further 22% of the variance. The first component (PC1) was positively correlated with bramble and negatively with herbaceous. The second component (PC2) showed a positive correlation with thorny shrubs and with trees. The third component (PC3) was positively related to non-thorny shrubs and negatively with trees. The fourth component (PC4) gave a positive correlation with bramble (fig. 4).
Results of the partial principal components analysis (PCA) relating the seasonal change in microhabitat selection by radiotracked tortoises. Tortoise codes are given in table 1. Grey dots indicate all the locations included in the analysis. In the middle panel, vectors show the relationships between vegetation categories (see table 2) and PCA axes 1 and 2.
Citation: Amphibia-Reptilia 36, 1 (2015) ; 10.1163/15685381-00002971
Trained dogs located four tortoises near three plots of two areas before starting the habitat management trial. The first tortoise located after clearing was observed in April in the edge between two plots and subsequently four more adult tortoises were observed. All these specimens, three of them females, were basking in the plots. In August 2013 dogs found two nests in two plots of different study areas, while in August 2014 dogs also found five nests in five plots of different study areas (one of this being predated in September).
The carapaces of the frozen hybrid tortoises placed in the plots that were cleared with the head accessory remained intact. In contrast, we observed scars in most carapaces in the plots cleared without the accessory (40% no damage and 60% death for neonates, 60% serious damage and 40% death for juveniles and 100% death for sub-adults and adults).
Discussion
MSD results indicate that the radiotracked western Hermann’s tortoise adults showed strong site fidelity as has been previously described (Chelazzi and Francisci, 1979; Lecq et al., 2014). Tortoises are opportunistic in selecting wintering or nesting areas although they mainly return to the same areas in successive years as a result of their site fidelity (Averill-Murray et al., 2002a, 2002b). This result is important because (1) it suggests that the Albera re-stocking programme conducted to establish viable tortoise populations would improve with temporary outdoor enclosures (Capalleras et al., 2011) and (2) it shows that large-scale land use changes and habitat disturbances may impair this population (Hailey, 2000).
Average FK and MCP home range size (in ha) of tortoises radiotracked in this study, compared with results obtained in other studies.
We then estimated that western Hermann’s tortoise in Albera had a minimum home range of approximately three ha to complete their annual activity cycle (table 1). In males, we observed a mean HR size similar to that found in another Catalan population (Bertolero, 2002), while female HR size was larger than some European populations (Swingland et al., 1986; Hailey, 1989; Calzolai and Chelazzi, 1991; Huot-Daubremont, 1991; Bossuto et al., 2000; Mazzoti et al., 2002) (table 3). Home-range size may change as a result of food availability and habitat productivity (Pons et al., 2008) and our results suggest that large female HRs are related with the currently limited nesting sites that probably favour high levels of nest predation (Vilardell et al., 2008, 2012). In addition, the large HR sizes of females may be a function of the quality of the habitat (Pough, 2004) and may be a consequence of the loss of nesting areas or habitat quality that have occurred throughout the last decades (Fahrig, 2007).
Macrohabitat analysis shows that tortoises preferred open canopy locations like open shrubland, open forest or barren land during the activity period and close canopy locations when they were in hibernation. Their preferences have been justified by the thermoregulation and feeding requirements of tortoises (Anadón et al., 2006) and have been associated with a high occurrence of tortoises (Couturier et al., 2014). Open shrubland, open forest and barren land were therefore selected over other habitat types because they could provide shelter, egg-lying, thermoregulation and feeding sites for tortoises. In addition, we detected that some radiotracked tortoises used human-altered sites as powerlines. Other authors described that gravid females of other chelonian species nested on the edge of the powerlines and in recent clearcuts (Litzgus and Mousseau, 2004; Beaudry et al., 2010). Thus, disturbances, together with cropland abandonment, can produce a change towards early-successional vegetation preferred by these tortoises (Ernst, 1967; Burke et al., 2000). Nevertheless, grasslands were negatively selected during the activity period, suggesting that their possible expansion to promote stockbreeding is not beneficial to tortoises, even though grassland have been described as the preferred habitat for the eastern form T. h. boetggeri (Rozylowicz and Popescu, 2013).
However, at a microhabitat scale, western Hermann’s tortoise preferred a combination of shrubland and trees during hibernation, herbaceous habitats and bramble during the emergence and the breeding seasons and mainly bramble during the summer.
Hibernation sites had a high cover of litter, woody and herbaceous species in the lowest layer and a high shrub cover that may provide stable temperatures for overwintering (Steen et al., 2007). In addition, we showed that bramble is used during summer dormancy. The bramble located in Albera valley bottoms forms dense thickets, and provides predator protection and thermoregulation. Therefore, any management aimed to reducing bramble thickets should be carefully planned to avoid an excessive reduction of its extent and any harm to hidden tortoises. Our data suggest that microhabitat patchiness provides the resources required by tortoises (Anadón et al., 2006; Rozylowicz and Popescu, 2013; Couturier et al., 2014).
Knowledge of macro and microhabitat use and home range size has considerable practical value for land managers. Macrohabitat use included a mosaic of microhabitat patches used during different phases of tortoises’ cycle. This mosaic mainly results from natural and human-induced disturbances which may suppress or create new habitats for Hermann’s tortoise. The results of this study can help to understand local extinctions due to the multiple habitats that tortoises require. Furthermore, they can provide guidelines for management programs that set aside areas of habitat critical to the species’ needs, to conserve viable populations and prevent mortality from forestry works. A successful management will sometimes require disturbances or direct intervention to create or maintain landscape patchiness (Law and Dickman, 1998). Thus, the results of the habitat management trial indicate the benefits of newly created open areas that can shape mosaic landscape favorable to the tortoise requirements. The occurrence of nests, detected with dogs, suggests a colonization of the new areas similar to that of burned areas (Couturier et al., 2011). However, this management may produce direct mortality that needs to be assessed and that depends on the specific thinning technique used (Casamitjana et al., 2012). Therefore, we recommend that thinning in areas inhabited by tortoise should use the new brush cutter head accessory. In relation to this accessory, we further improved the design covering the tube to prevent it to fill with soil and stones. In addition, we manufactured a second model in which the aluminum tube was replaced with an aluminum bar of 8 mm that did not catch on branches of shrubs. This second model makes it possible to open habitat, while the first could be used to control regrowth.
In patchy landscapes open areas coexist with dense cover, offering refuge areas essential during the summer and the winter. The protection of the habitat mosaics in which Albera population remains would also help the recovery of other open-habitat declining species (Fiers et al., 1997), such as the Bonelli’s Eagle (Hieraaetus fasciatus) and the European Rabbit (Oryctolagus cuniculus). However, thinning should be done in October and November to avoid excessive disturbance during the tortoise hibernation. Thinning should not be carried out in summer, when this activity is prohibited due to fire risk, or in spring, due to possible damage to birds’ nests. Finally, it is advisable to pile up the branches and wood debris. These piles can be a useful refuge for tortoises and also for bird species (Rost et al., 2010), for some species of rodents (Manning and Edge, 2008), and for the European rabbit (Catalán et al., 2008; Joan Real, pers. comm.), a keystone of Mediterranean ecosystems.
Given that human interaction with tortoise habitat is necessary and will continue into the future, it is vital to review some aspects of land use and management. In the Albera it is essential to improve the dialogue among scientists, landowners and managers to apply the best management practices for the conservation of the Hermann’s tortoise population.
Acknowledgements
This manuscript benefited from the comments of Beate Pfau and four anonymous referees. We thank Bartomeu Borràs, Eduardo Villanueva, David Estany, Josep Rost and Enric Capalleras for their valuable help during the study. We are especially grateful to the estate owners (adhered to the Albera Stewardship Network) that permitted us to conduct the trials. Financial support for this study came from Predoctoral Grant (2007 BR) from the Universtiy of Girona, Catalan Agency for the Management of University and Research (in support of local or regional projects) and from Catalan Government, that also processed us for capture permit. The trials comply with the current laws of Catalonia.
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Footnotes
Associate Editor: Luca Luiselli.
Habitat types used to characterize the landscape based on manual photo interpretation of aerial orthoimages. Cover categories are: 0 (0%), 1 (1-10%), 2 (10-25%), 3 (25-50%), 4 (50-75%), and 5 (75-100%).
Vegetation categories used in the microhabitat study. The main plant species of each category that are included in the tortoise’s diet are shown; however, aromatic plants are usually rejected.
