12
Unexpected consequences of reintroductions: competition between increasing red deer and threatened Apennine chamois S. Lovari 1,2* , F. Ferretti 1,2* , M. Corazza 3 , I. Minder 1,2 , N. Troiani 3 , C. Ferrari 3 & A. Saddi 1 1 Research Unit of Behavioural Ecology, Ethology and Wildlife Management, Department of Life Sciences, University of Siena, Siena, Italy 2 Biodiversity and Conservation Network (BIOCONNET), Department of Life Sciences, University of Siena, Siena, Italy 3 Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy Keywords interspecific interactions; protected areas; reintroductions; Rupicapra; ungulates; vegetation change. Correspondence Sandro Lovari, Research Unit of Behavioural Ecology, Ethology and Wildlife Management, Department of Life Sciences, University of Siena. Via P.A. Mattioli 4, 53100, Siena, Italy. Email: [email protected] *Both authors contributed equally to this study. Editor: Iain Gordon Associate Editor: Kate Searle Received 18 July 2013; accepted 06 January 2014 doi:10.1111/acv.12103 Abstract Reintroductions are commonly used to restore the local biological diversity and/or save threatened taxa. In human-altered landscapes, we may expect that reintro- duced species affect taxa already present. In Abruzzo, Lazio and Molise National Park (central Apennines, Italy), a 30% decline in the abundance of ‘vulnerable’ Apennine chamois (2005: c. 650 individuals, 2010: c. 450 individuals) has been recorded, whereas red deer (reintroduced in 1972–1987: 81 individuals) have greatly increased (2010: > 2500 individuals). We investigated space and diet over- laps between red deer and Apennine chamois, and their effects on foraging behav- iour of the latter. We also compared the composition of grasslands with that recorded when the former were absent. In 2010–2011, we found out: (1) a great space (> 75%) and diet (> 90%) overlap between deer and chamois; (2) a significant increase of unpalatable plant species and a decreasing trend of the nutritious, most grazed species by chamois, in respect to when deer were absent; (3) irrespective from vegetation type, a significantly reduced bite rate of adult female chamois in patches used also by deer, compared with areas without deer. Our results suggest a negative effect of red deer on the availability of nutritious plant species in summer–autumn, possibly because of grazing and physical damage on the grass- land caused by trampling. Environmental conditions and access to high-quality forage in the warm season influence the winter survival of offspring of mountain ungulates. Our results indicate that interspecific overlap in resource use with an increasing, reintroduced population can threaten rare taxa. Reintroductions of potentially competing species should be avoided in areas where populations of threatened taxa exist. Introduction A reintroduction is the intentional movement and release of a taxon inside its indigenous range, from which it disap- peared in historical time (IUCN, 2012). Reintroductions are commonly used to restore ecosystems and save threatened taxa (Armstrong & Seddon, 2008; IUCN, 2012). If causes of extinction or limiting factors have been removed and a fea- sibility study has been carried out, reintroductions can enhance the viability and the conservation status of a taxon. Reintroductions may also have unexpected impacts that outweigh their benefits: for example the reintroduction of carnivores could generate cascade effects on other compo- nents of ecosystems, with potentially negative effects on some of them (Smith, Peterson & Houston, 2003). Reintro- duced large herbivores can show sharply increasing popula- tion dynamics (e.g. Leopold, 1943; Caughley, 1970; Forsyth & Caley, 2006), which may elicit competition with already present species. On the other hand, information is not avail- able on the effects of reintroduced populations of large herbivores on native ones. Interspecific competition occurs when two species use the same, limited resource, with negative effects of the superior competitor on numbers of the inferior one (de Boer & Prins, 1990). Competition occurs through exploitation, when indi- viduals deplete the amount of resource left available to others, or through interference, when a resource is actively disputed (Putman, 1996). In some cases, interspecific overlap in the use of food resources or habitat, or inverse numerical trends of populations living in sympatry have been considered as indirect potential indices of competition (Putman, 1996; Latham, 1999, for reviews). In these cases, exploitation of resources has been suspected to affect popu- lation dynamics, distribution, resource use and phenotypic quality of wild ungulates (e.g. Sinclair & Northon-Griffiths, 1982; Putman, 1996; Latham, 1999; Focardi et al., 2006; Animal Conservation. Print ISSN 1367-9430 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 359

Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

  • Upload
    a

  • View
    216

  • Download
    2

Embed Size (px)

Citation preview

Page 1: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

Unexpected consequences of reintroductions:competition between increasing red deer and threatenedApennine chamoisS. Lovari1,2*, F. Ferretti1,2*, M. Corazza3, I. Minder1,2, N. Troiani3, C. Ferrari3 & A. Saddi1

1 Research Unit of Behavioural Ecology, Ethology and Wildlife Management, Department of Life Sciences, University of Siena, Siena, Italy2 Biodiversity and Conservation Network (BIOCONNET), Department of Life Sciences, University of Siena, Siena, Italy3 Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy

Keywords

interspecific interactions; protected areas;reintroductions; Rupicapra; ungulates;vegetation change.

Correspondence

Sandro Lovari, Research Unit of BehaviouralEcology, Ethology and WildlifeManagement, Department of Life Sciences,University of Siena. Via P.A. Mattioli 4,53100, Siena, Italy.Email: [email protected]

*Both authors contributed equally to thisstudy.

Editor: Iain GordonAssociate Editor: Kate Searle

Received 18 July 2013; accepted 06January 2014

doi:10.1111/acv.12103

AbstractReintroductions are commonly used to restore the local biological diversity and/orsave threatened taxa. In human-altered landscapes, we may expect that reintro-duced species affect taxa already present. In Abruzzo, Lazio and Molise NationalPark (central Apennines, Italy), a 30% decline in the abundance of ‘vulnerable’Apennine chamois (2005: c. 650 individuals, 2010: c. 450 individuals) has beenrecorded, whereas red deer (reintroduced in 1972–1987: 81 individuals) havegreatly increased (2010: > 2500 individuals). We investigated space and diet over-laps between red deer and Apennine chamois, and their effects on foraging behav-iour of the latter. We also compared the composition of grasslands with thatrecorded when the former were absent. In 2010–2011, we found out: (1) a greatspace (> 75%) and diet (> 90%) overlap between deer and chamois; (2) a significantincrease of unpalatable plant species and a decreasing trend of the nutritious, mostgrazed species by chamois, in respect to when deer were absent; (3) irrespectivefrom vegetation type, a significantly reduced bite rate of adult female chamois inpatches used also by deer, compared with areas without deer. Our results suggesta negative effect of red deer on the availability of nutritious plant species insummer–autumn, possibly because of grazing and physical damage on the grass-land caused by trampling. Environmental conditions and access to high-qualityforage in the warm season influence the winter survival of offspring of mountainungulates. Our results indicate that interspecific overlap in resource use with anincreasing, reintroduced population can threaten rare taxa. Reintroductions ofpotentially competing species should be avoided in areas where populations ofthreatened taxa exist.

Introduction

A reintroduction is the intentional movement and release ofa taxon inside its indigenous range, from which it disap-peared in historical time (IUCN, 2012). Reintroductions arecommonly used to restore ecosystems and save threatenedtaxa (Armstrong & Seddon, 2008; IUCN, 2012). If causes ofextinction or limiting factors have been removed and a fea-sibility study has been carried out, reintroductions canenhance the viability and the conservation status of a taxon.Reintroductions may also have unexpected impacts thatoutweigh their benefits: for example the reintroduction ofcarnivores could generate cascade effects on other compo-nents of ecosystems, with potentially negative effects onsome of them (Smith, Peterson & Houston, 2003). Reintro-duced large herbivores can show sharply increasing popula-tion dynamics (e.g. Leopold, 1943; Caughley, 1970; Forsyth& Caley, 2006), which may elicit competition with already

present species. On the other hand, information is not avail-able on the effects of reintroduced populations of largeherbivores on native ones.

Interspecific competition occurs when two species use thesame, limited resource, with negative effects of the superiorcompetitor on numbers of the inferior one (de Boer & Prins,1990). Competition occurs through exploitation, when indi-viduals deplete the amount of resource left available toothers, or through interference, when a resource is activelydisputed (Putman, 1996). In some cases, interspecificoverlap in the use of food resources or habitat, or inversenumerical trends of populations living in sympatry havebeen considered as indirect potential indices of competition(Putman, 1996; Latham, 1999, for reviews). In these cases,exploitation of resources has been suspected to affect popu-lation dynamics, distribution, resource use and phenotypicquality of wild ungulates (e.g. Sinclair & Northon-Griffiths,1982; Putman, 1996; Latham, 1999; Focardi et al., 2006;

bs_bs_banner

Animal Conservation. Print ISSN 1367-9430

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 359

Page 2: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

Richard et al., 2010). Conversely, field data (Ferretti et al.,2011) and anecdotal observations (Anthony & Smith, 1977;Forsyth, 1997) have suggested that competition may alsooccur through interference. However, few studies have pro-vided strong evidence of competition among wild ungulates(Forsyth & Hickling, 1998; Ferretti et al., 2011) and infor-mation on mechanisms of competition is also scarce (but seeFerretti et al., 2011).

The availability and quality of food resources in spring–summer are crucial to improve winter survival of offspring,which, in turn, influences the population dynamics of wildungulates, especially on mountains (e.g. Festa-Bianchet,1998a; Côté & Festa-Bianchet, 2001a; Pettorelli et al.,2007). In particular, body size and survival of offspringdepend on environmental variables and body conditions ofmothers, which, in turn, are affected by spring–summerfood resources (Clutton-Brock, Albon & Guinness, 1984,1986; Festa-Bianchet, 1998a,b; Côté & Festa-Bianchet,2001a-b; Pettorelli et al., 2005, 2007). In the warm months,the exploitation of food resources and/or the limitationof access to them by a competitor, through interference,could be the ultimate factor affecting the viability of anungulate population. We used the Apennine chamoisRupicapra pyrenaica ornata and the red deer Cervus elaphusto test the hypothesis that overlap in diet and habitat with areintroduced ruminant will alter the foraging efficiency ofanother ungulate. High overlap would negatively affect thelatter’s abundance and population persistence.

The Apennine chamois is a ‘vulnerable’ taxon, strictlyprotected under national and international legislation, listedon appendix II of the Bern Convention; annexes II and IV ofthe European Union Habitats and Species Directive; appen-dix II of Convention on International Trade in EndangeredSpecies of Wild Fauna and Flora; and listed as ‘especiallyprotected species’ under Italian law n. 157/1992 (Herrero,Lovari & Berducou, 2008). During the Holocene, theApennine chamois was distributed along the Apenninechain (Masini & Lovari, 1988), surviving only in theAbruzzo, Lazio and Molise National Park (ALMNP,central Italy) until 1991 (Dupré, Monaco & Pedrotti, 2001).Since 1991, there have been many releases of the Apenninechamois into other protected areas in the central Apennines(Lovari et al., 2010). Chamois numbers have decreased by atleast 30% within the ALMNP during the last decade (c. 650individuals in 2005 and c. 450 individuals in 2010; Latiniet al., 2011). Mortality of nearly all kids during winter, espe-cially in their core range, has determined the populationdecline (Latini et al., 2011).

A total of 45 red deer were reintroduced to the ALMNPin 1972, within the core area of the chamois range (density:0.5 indviduals per 100 ha; Apollonio & Lovari, 2001).Thirty-six other individuals were released in small groups(7–10 individuals per release, in four operations), in thefollowing 15 years (Apollonio & Lovari, 2001). No data areavailable on population dynamics of red deer in ALMNP in1972–2006, but not surprisingly, recent estimates indicate agreat increase of their densities with respect to the time oftheir release (2007: 9.0 individuals per 100 ha; 2010: 14.3

individuals per 100 ha, in the core range of the Apenninechamois; Latini, 2010). In the last 30 years, chamois densityhas about halved in the core area of their range (1984–1985:c. 38 individuals per 100 ha, Lovari, 1985; 2012: c. 20 indi-viduals per 100 ha, cf. Latini et al., 2012). In the warmmonths, red deer use the alpine grasslands, attended only bychamois 30 years ago (Lovari, 1984; Bruno & Lovari, 1989).Because of its flexible food habits (Hofmann, 1989), the reddeer shows a great overlap in diet and habitat use with otherungulate species (Putman, 1996). A negative effect of reddeer has been suggested for density (Latham et al., 1997)and body size (fawns: Richard et al., 2010) of roe deerCapreolus capreolus. A great overlap in the diet of red deerwith that of Northern chamois Rupicapra rupicapra hasbeen detected (Schröder & Schröder, 1984; Bertolino et al.,2009), suggesting the potential for competition.

We predicted that: (1) there is a diet/spatial overlapbetween Apennine chamois and red deer, both ‘intermediatefeeders’ (Hofmann, 1989), in the warm period, that issummer to mid-autumn; (2) an increase of the frequency ofunpalatable species and a decrease of that of preferred onesby chamois has occurred with respect to the time when deerdid not attend the area (cf. Ferrari, Rossi & Cavani, 1988);(3) the spatial overlap of red deer with adult female chamoisdecreases the latter’s foraging efficiency. A decrease inhighly nutritious food resources and an increase in less pal-atable ones should result in a greater search for food (thus agreater step rate, cf. Owen-Smith & Novellie, 1982) and alower bite rate of chamois in patches attended by bothspecies, than in those where only chamois graze; (4) red deerwill displace chamois from their feeding grounds, as theformer are much larger than the latter (Boitani et al., 2003;cf. Ferretti, Sforzi & Lovari, 2011).

Methods

Study area

Our 65-ha experimental area was the core distribution of theApennine chamois in ALMNP, upper Val di Rose (prevail-ing NE-SE aspects), above the treeline (mixed beech Fagussylvatica forests, c. 1700–1800 m a.s.l.) up to the top of M.Sterpi d’Alto and M. Boccanera (1966 and 1982 m a.s.l,respectively). Up to the late 1990s, our study area and itsneighbourhoods held the densest population of Apenninechamois (38 individuals per 100 ha, N = c.140 individuals,Lovari, 1985).

The study area lies in the cold axeric region and coldtemperate subregion (Blasi, 1994), with annual rainfall:1500 mm; summer rainfall: 260–270 mm; mean annual tem-perature: 4.7°C; no dry season. Snow cover lasts from lateNovember to May–June (Bruno & Lovari, 1989).

Vegetation (Fig. 1 and Supporting Information Appen-dix S1) is a mosaic composed by palatable graminoids(35.5%), unpalatable grass Brachypodium genuense (24.3%),clover-dominated Trifolium thalii patches (15.2%) androcks/screes with sparse vegetation (25.0%), ungrazed bylivestock since at least 50 years ago.

Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

360 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London

Page 3: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

In 2010 and 2011, respectively, 85 (39 adult females) and82 (33 adult females) chamois attended our study area (i.e.the maximum number of individuals observed in separategroups, at the same time in a day, divided by sex/age class;40% less than in 1985–1986, S. Lovari, unpubl. data), with apopulation structure strongly skewed to mature individuals(Latini et al., 2011). Our study area was used also by reddeer (mean density in ALMNP: 5 deer per 100 ha; meandensity in our study area, the core range of chamois: 14.3deer per 100 ha, in 2010; Latini, 2010: c. 1.3 tons per 100 haof deer biomass). Roe deer and wild boar Sus scrofa also livein ALMNP, but they only visit upper grasslands occasion-ally (i.e. their faeces were found in only 2% and 1%, ofsurveys in sampling plots, respectively, see later). In the last50 years, livestock has been absent from this area. The greywolf Canis lupus, brown bear Ursus arctos and golden eagleAquila chrysaetos visit the area.

Spatial overlap

In July–October, the extent of spatial overlap of red deerand chamois was estimated through pellet group counts(Mayle, Peace & Gill, 1999; Forsyth et al., 2007). Pellets ofred deer and chamois can be readily told apart through anumber of morphological differences (Mustoni et al., 2002).Presence/absence of pellet groups (>5 pellets, Mayle et al.,1999) was recorded in circular sampling plots (radius: 5 m),randomly placed onto a grid overlain to grasslands (1 plot

per cell; N = 38; cell size: 100 m; cf. Fattorini et al., 2011).Through a survey in October 2010, we assessed spatialoverlap in the previous months. The presence of pelletgroups of red deer should reflect the use of high-altitudemeadows (c. 1800–2000 m a.s.l.) by this ungulate, in theprevious months.

The faecal accumulation rate technique (Mayle et al.,1999) was used in 2011. In late June, all pellet groups wereremoved from each plot, which were then visited again inlate August to count pellet groups and to estimate overlap insummer. If pellet groups of red deer/chamois were not foundin August, plots were visited again in late October, to assessspatial overlap in summer–autumn. We used the index ofJaccard (1901) to assess spatial overlap in the study area (I)and in the area used by chamois (ICAM):

I = + +( )α α β γ ;

ICAM = +( )α α β ,

where α = number of plots with pellet groups of bothspecies; β = number of plots with pellet groups of chamois;γ = number of plots with pellet groups of red deer.

Diet overlap

The diet composition of chamois and red deer were com-pared seasonally through the detection of food remains infaecal samples (Johnson et al., 1983) in spring (April–May), summer (July–August) and autumn (September–early November) 2010–2011 (chamois faecal samples, intotal: N = 59; red deer faecal samples: N = 54). Only freshsamples were collected, after observing defecations(chamois: n = 8 per season, 2010; n = 10–13 per season,2011; red deer: n = 8 per season, 2010; n = 8–11 per season,2011) and frozen within several hours, before analyseswere carried out. Differences in the seasonal percentagevolume of plant categories were tested by the Mann–Whitney U-test, while frequencies of occurrence were com-pared by the chi-square test (Sokal & Rohlf, 1995). Weconsidered the categories ‘trees/shrubs’, ‘forbs’, ‘grass’ and‘fruits’. Seasonal diet overlap (proportional volumes; rela-tive frequencies) was estimated through the index ofPianka (1973):

Ov o o o o== = =∑ ∑ ∑iAC iRDi

M

iACi

M

iRDi

M

1

2

1

2

1

where oi = proportion of food category i in the diet ofApennine chamois and red deer (0 = no overlap; 1 = max.overlap). In our study area, most plant families have specificindigestible features, for example trichomes and glandularcells, which allow detection of their presence in samples.Overlap in frequency of use of single forb families was inves-tigated. See Minder (2012) and Supporting InformationAppendix S1, for further details.

Figure 1 Vegetation map of the study area.

S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 361

Page 4: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

Vegetation change

Frequency of occurrence (presence/absence) and cover ofplant species were compared between 1982–1984 (reddeer absent) and 2010–2011 (red deer present) throughvegetation surveys in plots (100 m2 per area; n = 34; cf.Rossi, 1985) using the phytosociological method(Braun-Blanquet, 1964). We considered the most grazedspecies in 1982–1984, according to a scale of monthlygrazing frequency, and three unpalatable species, rare in1982–1984 (B. genuense, Carduus carlinaefolius, Carlinaacaulis; Rossi, 1985; Ferrari et al., 1988). Presence/absenceof signs of trampling (identified through footprints) by reddeer, absent in 1982–1984 (Rossi, 1985; Ferrari et al.,1988), were estimated visually.

Presence/absence and frequency/cover of plant specieswere compared between 1982–1984, and 2010–2011,through generalized linear models with binomial (presence/absence) and Poisson (cover) errors (Crawley, 2007). Statis-tical analyses were carried out through the R software (RDevelopment Core Team, 2009).

Effects of red deer on foraging efficiencyof Apennine chamois

The effects of usage of alpine grasslands by red deer on theforaging efficiency of adult female chamois (> 3 years old;Lovari, 1985) were assessed through behavioural observa-tions. Chamois in our study area were habituated to touristsand could be approached to up to 30 m without eliciting anyalarm response (Cederna & Lovari, 1985). Chamois wereobserved from vantage points, at a distance of 30–200 m,from dawn to dusk (2 days per week; mid-July to earlyNovember; Bruno & Lovari, 1989).

The foraging behaviour of chamois was recorded throughfocal animal sampling (Altmann, 1974). Observations werecarried out in 10-min bouts, divided by 1-min samplingintervals (Ruckstuhl, Festa-Bianchet & Jorgenson, 2003).Each 1-min focal sample was followed by an interval of 10 s,to record data on a checksheet (Bruno & Lovari, 1989;Ruckstuhl et al., 2003). We recorded (1) n. bites to grass permin (bite rate, an index of food intake rate; Bruno & Lovari,1989; Ruckstuhl et al., 2003); a bite was identified by adistinct jerking motion of the head (Bruno & Lovari, 1989);and (2) number of steps for food searching per min (steprate: an index of foraging continuity; Bruno & Lovari, 1989;Neuhaus & Ruckstuhl, 2002); a ‘foraging step’ is defined asa forward movement of one of the forelegs, with the headclose to the ground (Bruno & Lovari, 1989). When neces-sary, 10 × 50 binoculars and 20–60× spotting scopes wereused to allow the visibility of the mouth of chamois. At eachsampling event, we estimated the proportion of rock coveraround the focal animal (0–25%, 25.1–50%, > 50% of rockcover in a radius of five times the body length of an adultchamois). The geographic location of the focal animal wasrecorded after it vacated the area, using a hand-held globalpositioning system (GPSMAP 62s, Garmin Ltd., KansasCity, MO, USA). Locations were overlain on the vegetation

map of our study area (Fig. 1) and on maps of usage ofalpine grasslands by red deer (derived from our pellet groupcount surveys), to assess: (1) the type of vegetation (vegeta-tion with T. thalii; vegetation with graminoids) grazed bythe focal animal; and (2) whether it grazed in a grid cell alsoused by red deer. Because of their nocturnal activity, theobservability of red deer was so poor in our study area thatreliable, substantial information on the use of uppermeadows could only be collected through an indirectmethod.

We carried out short-term observation bouts (10 minper individual) on different individuals, to reducepseudoreplication of data. Daily movements of femalechamois herds were constant and predictable, allowing us tofollow them during our observation bouts. We recordeddata on individuals who could temporarily be distinguishedby their respective positions on the slope (Frid, 1997). Smallmorphological differences (Lovari, 1979) that were visible atclose range decreased the probability of recording data fromthe same individual more than once daily.

We recorded 364 sampling bouts (mean: 6.1 bouts perday; standard deviation: 0.6; 57.5 observation hours).Observation bouts were discarded when the focal animaldisappeared from sight after < 5 min. The effects of spatialoverlap with red deer on the bite and the step rates of adultfemale chamois were estimated through generalized linearmixed models, with Poisson errors (Crawley, 2007). Thenumber of bites (or the number of steps) in 1-min samplingintervals were fitted as response variables. In global models,explanatory variables were: presence of deer pelletgroups, season (summer: July–August; autumn: September–November), vegetation (patches with T. thalii; patches withgraminoids), rock cover, year (2010, 2011), time of the day(morning: 5:00–10:00 h; mid-day: 10:00–15:00 h, summer,10:00–14:00 h, autumn; afternoon: 15:00–20:00 h, summer,14:00–18:00 h, autumn) and the two-way interactionsbetween overlap with red deer and the other variables. Inparticular, we included the interaction year × overlap withred deer to test whether our results have been influenced bythe change of sampling technique of pellet group counts,between 2010 and 2011. The identity of the focal animalobserved in 10 1-min sampling intervals was fitted asrandom factor, to control for the effect of repeated measuresof 1-min sampling intervals taken in the same observationbout. Minimum adequate models were estimated by remov-ing the least significant term at each step, starting from thehighest level of interactions, until the elimination of termscaused a significant increase in the residual deviance(Crawley, 2007). The significance of changes in residualdeviance was assessed through F-like deletion tests(Crawley, 2007).

Behavioural interference

We recorded behavioural interspecific interactions whenchamois and red deer where at a mutual distance < 50 m(Anthony & Smith, 1977; Berger, 1985; Forsyth, 1997;Ferretti, Sforzi & Lovari, 2008; Ferretti et al., 2011). Inter-

Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

362 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London

Page 5: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

actions were classified following Ferretti et al. (2008; 2011;see Supporting Information Appendix S1).

Results

Spatial overlap

Both species used a large part of the study area (82–92% and58–76% of plots for red deer and chamois, respectively;Table 1). Spatial overlap in the study area (I) was 0.47–0.61,depending on season/year (Table 1). Spatial overlap was1.4–1.7 times greater in the areas grazed by chamois than inthe whole study area, as chamois shared 76–88% of theirgrazing areas with red deer (Table 1).

Diet overlap

Grass was the staple of chamois in spring/autumn and thatof red deer in autumn, whereas grass–forbs were the stapleof both species (summer) and that of deer (spring; Fig. 2).Trees/shrubs and fruits/ferns/mosses were minor fooditems (Fig. 2). The volume of grass in the diet of chamoisdecreased significantly in summer and increased in autumn,while that of forbs showed an opposite pattern (Fig. 2;Table 2). In the diet of red deer, the volume of grass andforbs did not change between spring and summer, but inautumn the volume of the former increased while that of thelatter decreased (Fig. 2; Table 2).

Grass and forbs were found in all faecal samples. Thefrequency of trees/shrubs decreased in summer andincreased in autumn in red deer, but not chamois (Fig. 2;Table 3). Summer food habits of chamois and deer werenot significantly different (Fig. 2; Table 4). In spring andautumn, grass was eaten significantly more by chamois,whereas deer ate more trees/shrubs (Fig. 2; Table 4).Forbs formed the greater proportion of the diet of deer inspring, whereas in autumn this category was eaten more bychamois than deer (Fig. 2; Table 4). The frequency ofLabiatae, Fabaceae, Caryophyllaceae, Compositae andPlantaginaceae was ≥ 50% for both ungulates (Fig. 3).

0

20

40

60

80

100

AC (N=18) RD (N=16) AC (N=20) RD (N=19) AC (N=21) RD (N=19)

% v

olu

me

Grass

Forbs

Trees/shrubs

Other

Spring Summer Autumn

**

***

***

*

***

*

AC (n = 18) AC (n = 20)RD (n = 16) RD (n = 19) RD (n = 19)AC (n = 21)

Figure 2 Seasonal diet composition of Apennine chamois (AP) and red deer (RD) in 2010/2011 in terms of volume (%) of main food categories.* = P < 0.05; ** = P < 0.01; *** = P < 0.001 (Mann-Whitney U-test).

Table 1 Number of sampling plots (N = 38) with pellet groups of chamois only, red deer only and both species and Jaccard indices of spatialoverlap

Season Only chamois Only red deer Overlap I ICAM

Summer/autumn 2010 7 9 22 0.55 0.76Summer 2011 4 16 18 0.47 0.82Summer/autumn 2011 3 12 23 0.61 0.88

I and ICAM: Jaccard indices, indicating spatial overlap in the study area and in the area used by chamois, respectively.

Table 2 Diet composition and overlap of Apennine chamois and reddeer, estimated through micro-hystological analyses of faeces:seasonal differences (Mann–Whitney U-test) of percentage volumesof plant categories

Species Category

Seasonal change: U (P-value)

Spring–summer Summer–autumn

Chamois Grass 35.0 (P < 0.001) 71.5 (P < 0.001)Forbs 45.0 (P < 0.001) 42.5 (P < 0.001)Trees/shrubs 159.5 (P > 0.05) 147.0 (P > 0.05)Fruits 162.0 (P > 0.05) 190.5 (P > 0.05)

Red deer Grass 148.0 (P > 0.05) 100.5 (P < 0.05)Forbs 106.5 (P > 0.05) 10.0 (P < 0.001)Trees/shrubs 62.0 (P < 0.01) 59.5 (P < 0.001)Fruits 128.0 (P > 0.05) 107.0 (P < 0.05)

S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 363

Page 6: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

Seasonal diet overlap was high (Ov > 0.90) at all scales ofanalyses (Table 5). Overlap was the greatest in summer(Ov = 0.97–0.99) and the lowest in spring (0.90–0.95;Table 5).

Vegetation change

Decreases in both the frequency of occurrence and coverproportion of 11 out of the 12 plant species most grazed bychamois were observed in 2010–2011 in comparison with1982–1984 (Table 6). Differences between periods were sig-nificant for 5 (frequency) and 8 (cover) species (Table 6).Conversely, frequency and cover of unpalatable speciesincreased significantly from 1982–1984 to 2010–2011(Table 6). Deer trampling was recorded in 60% of samplingplots.

Effects of red deer on foraging efficiencyof Apennine chamois

The bite rate of adult female chamois was significantlygreater in areas without red deer compared with those withred deer (Table 7; Fig. 4). Female chamois gave a median

value of 2.9 (summer) and 2.8 (autumn) more bites to grassper min in patches unused by deer than in patches with deer.The bite rate was significantly greater in summer than inautumn (Table 7; Fig. 4), in clover patches than in otherpatches, in 2011 than in 2010, and it was significantly lowerin patches with >25% rock cover than in areas with < 25%rock cover (Table 7).

The median step rates of female chamois were c. 15%(summer) and c. 7% (autumn) greater in areas attended bydeer than in unattended areas, even if this difference wasnot significant (Table 7; Fig. 4). The step rate of chamoiswas significantly greater in patches with 25.1–50.0% rockcover than in other patches (Table 7). The interactionYear × Overlap with red deer influenced significantlyneither the bite rate nor the step rate of chamois (generalizedlinear mixed models; P > 0.05), suggesting that our resultswere not influenced by the change of sampling technique ofpellet group counts, in 2011 (see Methods).

Behavioural interference

Out of 59.5 observation hours, only one interspecific‘contact’ was recorded: 1 hind and 2 female chamois grazedwith no apparent interaction. Six ‘contacts’ were seenoutside recording sessions, with no apparent interaction: inone case, one adult male chamois uttered an alarm whistle,without withdrawing, to a stag.

DiscussionAlthough increasing populations of introduced ungulatescan affect the density of other ungulates (e.g. fallow deer/roedeer: Putman & Sharma, 1987; Ferretti et al., 2011; Hima-layan tahr/Alpine chamois: Forsyth & Hickling, 1998), theeffects of increasing populations of reintroduced ungulateson autochtonous ones have not been assessed. This eventmay be especially harmful when local taxa are threatened.In this paper, we suggest that the recent decline of a vulner-able ungulate could be related to the increase of a reintro-duced one, through competition for a scarce food resource.

Mainly vegetation quality and quantity influence bodygrowth, survival, reproductive success and populationdynamics of ungulates (e.g. Clutton-Brock et al., 1984,1986; Côté & Festa-Bianchet, 2001b; Pettorelli et al., 2007).Among mammals, while body mass can still increaseafter adulthood, skeletal growth is restricted to early life(e.g. Clutton-Brock, Guinness & Albon, 1982; Lindström,1999; Lummaa & Clutton-Brock, 2002; Hewison et al.,

Table 3 Diet composition and overlap of Apennine chamois and red deer, estimated through micro-hystological analyses of faeces: frequencyof occurrence of plant categories and seasonal differences (chi-square test)

Species Category

Frequency of occurrence Seasonal change: χ2 (P-value)

Spring Summer Autumn Spring–summer Summer–autumn

Chamois Trees/shrubs 44% 55% 67% 0.11 (P > 0.05) 0.20 (P > 0.05)Fruits 0% 10% 19% 0.42 (P > 0.05) 0.14 (P > 0.05)

Red deer Trees/shrubs 100% 63% 95% 5.25 (P < 0.05) 5.88 (P < 0.05)Fruits 6% 21% 53% 0.58 (P > 0.05) 2.83 (P > 0.05)

Table 4 Diet composition and overlap of Apennine chamois and reddeer, estimated through micro-hystological analyses of faeces:interspecific differences (Mann–Whitney U-test) of volumes of plantcategories in the diets

Category

Interspecific differences: U (P-value)

Spring Summer Autumn

Grass 31.5 (P < 0.001) 147.5 (P > 0.05) 111.5 (P < 0.05)Forbs 63.0 (P < 0.01) 176.0 (P > 0.05) 110.5 (P < 0.05)Trees/shrubs 0.5 (P < 0.001) 148.0 (P > 0.05) 51.5 (P < 0.001)Fruits 135 (P > 0.05) 167.5 (P > 0.05) 116 (P < 0.05)

Table 5 Seasonal diet overlap between Apennine chamois and reddeer, estimated through micro-hystological analyses of faecalsamples and the Pianka index

Scale of analysis

Diet overlap (Pianka index)

Spring Summer Autumn

Large categories (% volume) 0.90 0.99 0.97Large categories (relative

frequencies)0.95 >0.99 0.97

Forb families (relativefrequencies)

0.94 0.97 0.92

Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

364 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London

Page 7: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

2005). In particular, the youngest cohorts in a populationrequire good food in summer to enhance body growth and,in turn, winter survival (Lindström, 1999; Lummaa &Clutton-Brock, 2002). Thus, a reduction of food resources(e.g. because of resource exploitation by a superior competi-tor) could have negative effects on winter survival, especiallyof young individuals.

Diet overlap was great between chamois and deer. Thus,one could expect that competition would arise whenresources are limited. No behavioural interference wasrecorded during our study. The lack of obvious interferencebetween red deer and chamois does not necessarily rule outinterference competition, in the past 30 years. However,Ferretti et al. (2011) reported substantial direct interactionsbetween roe deer and fallow deer, with the fallow being thesuperior competitor, in an area where they had beentogether for at least 50 years. Our results have shown thatthe quality of alpine grassland has decreased between 1982–1984 and 2010–2011, and the most grazed plant species bychamois (Rossi, 1985; Ferrari et al., 1988) have generally

0

20

40

60

80

100L

ab

iata

e

Le

gu

min

osa

e

Ca

ryo

ph

ylla

ce

ae

Co

mp

osita

e

Pla

nta

gin

ace

ae

Ge

ran

iace

ae

Cis

tace

ae

Plu

mb

ag

ina

ce

ae

Scro

ph

ula

ria

ce

ae

Ro

sa

ce

ae

Lilia

ce

ae

Um

be

llife

rae

Po

lyg

on

ace

ae

Ru

bia

ce

ae

Ra

nu

ncu

lace

ae

% f

req

ue

ncy o

f o

ccu

rre

nce

Apennine chamois

Red deer

Figure 3 Frequency of occurrence (%) offorbs (only families with frequency ofoccurrence > 5%) in the diet of Apenninechamois (N = 59) and red deer (N = 54) in2010/2011.

Table 6 Variation in frequency of occurrence (FO; %) and cover values [CV; ± standard error (SE)] of the most grazed species by Apenninechamois when no red deer were present in our study area (1982–1984) and those of unpalatable species, between 1982–1984 and 2010–2011

Species

FO (%) Variation in FO Variation in CV

1982–1984 2010–2011 B SE P B SE P

Palatable Bellis pusilla 29 32 0.14 0.53 n.s 0.07 0.15 n.sDoronicum columnae 59 32 −1.09 0.51 * −0.46 0.18 **Festuca spp 74 59 −0.67 0.52 n.s −0.03 0.13 n.sHeracleum sphondylium orsinii 59 12 −2.37 0.64 *** −0.92 0.26 ***Plantago atrata 91 82 −0.79 0.75 n.s −0.67 0.22 **Poa alpina 53 35 −0.72 0.50 n.s −0.31 0.14 **Ranunculus apenninus 88 74 −0.99 0.66 n.s −0.42 0.17 *Rumex acetosa 79 26 −2.37 0.58 *** −0.79 0.20 ***Taraxacum apenninum/Crepis aurea

glabrescens91 32 −3.07 0.71 *** −1.07 0.23 ***

Taraxacum officinale 35 26 −0.42 0.53 n.s −0.23 0.20 n.sTrifolium pratense semipurpureum 59 47 −0.47 0.49 n.s −0.24 0.15 n.sTrifolium thalii 88 62 −1.54 0.64 * −0.44 0.13 ***

Unpalatable Brachypodium genuense 3 62 3.98 1.07 *** 2.30 1.01 *Carduus carlinaefolius 35 94 3.38 0.81 *** 0.85 0.22 ***Carlina acaulis 9 29 1.46 0.71 * 0.67 0.37 n.s

Variations in FO and CV of three poorly palatable species were considered as well. Significance of difference was assessed using generalizedlinear models with binomial (presence/absence) errors. *** = P < 0.001; ** = P < 0.01; * = P < 0.05. n.s., not significant.

Table 7 Factors affecting bite and step rates of adult femaleApennine chamois (N = 3389 1-min sampling intervals, out of 364observation bouts collected in 2010–2011)

Model Variable Coefficient SE P

Bite rate Overlap with red deer (yes) −0.083 0.016 0.000Season (summer) 0.236 0.017 0.000Rock cover (>50.0%) −0.154 0.022 0.000Rock cover (25.1–50.0%) −0.057 0.018 0.001Year (2011) 0.032 0.015 0.036Vegetation type (patches

with Trifolium thalii)0.040 0.017 0.019

Intercept 3.204 0.020 0.000Step rate Rock cover (25.1–50.0%) 0.157 0.079 0.046

Intercept 0.889 0.084 0.000

Effects were estimated through generalized linear mixed models,with Poisson errors. The final model for step rate included also thenon significant effects of overlap with red deer, vegetation type andyear. SE, standard error.

S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 365

Page 8: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

decreased in frequency and/or cover. The diet of nursingfemale chamois depends on the availability of nutritiousvegetation dominated by T. thalii (Ferrari et al., 1988). Thisspecies, whose leaves are rich in proteins and highly digest-ible (Ferrari et al., 1988), has decreased significantly infrequency/cover with respect to the time when deer wereabsent. Conversely, unpalatable species have increased sig-nificantly in frequency and/or cover. In particular, the for-merly rare B. genuense (3% frequency) occurred in morethan 60% of relevés, in 2010–2011, covering more than 24%of grasslands. The strong vegetative reproduction and thecapacity to alter the ecology of an area make the B. genuensea greatly competitive plant (Catorci et al., 2011). Because ofthe high silica content and the hairs on its leaves, it is noteaten by chamois and red deer, except accidentally (I.Minder, unpubl. data). Pasture abandonment promotes thespread of this plant on calcareous grasslands, as moderatelivestock grazing may control it (Catorci et al., 2013). In ourstudy area, the heavy grazing selectivity of wild ungulatescould have altered the composition of plant communities,reducing the fitness of palatable plants and favouring thespread of scarcely palatable species (Augustine &McNaughton, 1998; Alm Bergvall et al., 2006). Red deerhave a body mass approximately four times greater thanthat of chamois and move in large herds (up to 90 individu-als in our study area), with a potentially great impact onvegetation, whereas female Apennine chamois are partial toT. thalii patches (Ferrari et al., 1988). Accordingly, 60% ofsampling plots showed deer trampling, while trampling wasabsent when only chamois grazed in the study area (Rossi,1985; Ferrari et al., 1988). Red deer may outcompetechamois not only by feeding over the same preferred foodresources, but also by altering the quality of grasslandthrough trampling.

The best food patches for chamois (i.e. T. thalii commu-nities) could not only be depleted by high densities of reddeer, but they may also be influenced by climatic conditions.Trifolium thalii communities are restricted to sites with along-lasting snow cover (Ferrari et al., 1988; Blasi, Di Pietro& Pelino, 2005). Fluctuations of temperature and snowmelt

affect the viability of snowbed vegetation (Schöb et al.,2009). Because of climate changes, the reduction of cold-adapted species and the increase of thermophilous ones havealready been recorded in European alpine ecosystems(including Apennines; Gottfried et al., 2012). In a nearbyApennine area (Mt. Greco massif), T. thalii communitiesalmost disappeared in years with scarce snowfalls (D’Angeliet al., 2011). In turn, reduction of T. thalii communitiesbecause of climate change could be an alternative reason perse for the observed decline of chamois, in our study area.Numbers of Apennines chamois have been increasing stead-ily in neighbour national parks (Mari & Lovari, 2006), aswell as on mountains relatively close (c. 7–8 km, in a straightline) to our study area (Lovari, 1977; Latini et al., 2011),suggesting that potential negative effects of climate changeon the quality of meadows are not yet affecting the viabilityof other chamois populations. Because of the rarity and thefragility of clover communities on the Apennines (Petraglia& Tomaselli, 2007), and their high nutrient value forchamois (Ferrari et al., 1988), the alteration or even a reduc-tion of spatial distribution of this community would inevi-tably lead to a decrease of nutritious pasture for chamois.

The foraging behaviour of chamois reflects the quality ofpasture in areas with or without red deer presence. We werecompelled to infer the use of grasslands by red deer throughpellet group counts, because of the poor observability ofdeer, in our study area. Diet analyses confirmed that deerfed mainly on species available in the upper grasslands, thatis on feeding grounds of chamois. It has been shown thatbharal Pseudois nayaur increased their diet breadth, when insympatry with one to two species of large herbivores, pre-sumably to include less nutritious food items because offorage constraints imposed by competitors (Namgail et al.,2007). On poor feeding grounds, with less opportunities toselect rich food patches, an increased use of less palatablespecies may be expected (e.g. Owen-Smith & Neiville, 1982;Brambilla et al., 2006), presumably leading to both a longerchewing and a reduction of bite rate (Moquin et al., 2010).Accordingly, our data show that, for female chamois, thebite rate was significantly affected by the spatial overlap

18

20

22

24

26

28

30

32

34

36

38

Summer Autumn

Nu

mb

er

of

bit

es

to

gra

ss

pe

r m

in

n = 86

10-min

intervals

n = 45

n = 142

n = 91

1

1,5

2

2,5

3

3,5

4

4,5

5

Summer Autumn

Nu

mb

er

of

ste

ps

pe

r m

in

Patches used by chamois only

Patches used by red deer and chamois

Figure 4 Bite rate and step rate (N of bites/min and N of steps/min, respectively; median ± interquartile range) of adult female Apenninechamois, in 2010–2011: effects of season and overlap with red deer. For significance, see Table 5.

Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

366 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London

Page 9: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

with red deer, irrespectively from the vegetation type. Thus,a negative effect of red deer on the food intake rate ofchamois may be suggested.

Movements for food searching depend greatly on pat-terns of distribution of food resources (e.g. Owen-Smith &Neiville, 1982; Bunnell & Gillingham, 1985). The step rateof female chamois increased mildly – not significantly – inareas attended by red deer, although further data arerequired (e.g. through the comparison between study areaswith/without red deer). Our results would also suggest thatthe step rate has not increased, and the bite rate hasdecreased (by c. 8%, in summer) with respect to 1984–1985,when deer were not present (Bruno & Lovari, 1989), whichmay support the view of a uniformly distributed poorforage, presently. On the other hand, we showed (1) a greatoverlap in diet and space between Apennine chamois andred deer; (2) a reduction of food resources with respect to thetime when deer were absent; (3) a negative effect of overlapwith red deer on the bite rate of chamois. These results arestrongly suggestive of a negative effect of red deer on foodresources of chamois.

The decrease of chamois in their core range has beendetermined by a great winter mortality of kids (Latini et al.,2011). Mortality determined by inbreeding depression canbe ruled out as released, daughter populations of Apenninechamois – which should be even more inbred than thesource population, i.e. ALMNP – show a high viability(Mari & Lovari, 2006). In the last decade, the decrease in thenumber of chamois in ALMNP has not been determined bya density-dependent local decrease of female fecundity, asbirth rates have remained high in the core range of chamois(median value number of kids : number of adult femalechamois, for 1976–1982: 0.70, Locati & Lovari, 1988; 2010:0.62, 2011: 0.75, Ferretti & Lovari, unpubl. data). Chamoisnumbers were stable during 1972–1987 (Lovari, 1985;Dupré et al., 2001), but increased during 1993–1999 (up to600 individuals), because of the protection accorded toperipheral areas (Dupré et al., 2001). The stability of thechamois population in its core range, on the last threedecades of the last century, militates strongly against arecent density-dependent increase of kid mortality. The pre-dation of bears (Fico, Locati & Lovari, 1984; Di Domenicoet al., 2012), wolves (Patalano & Lovari, 1993; Meriggi &Lovari, 1996; Grottoli, 2011) and golden eagles (Locati,1990; Bertolino, 2003) is negligible. No data on parasiteload are available from the 1980s, ruling out comparisonswith 2010–2011 (Latini et al., 2011). However, one shouldexpect that the parasite load will increase in individualsweakened by food depletion (Craig et al., 2008; Hugheset al., 2009).

A parallel decrease of chamois numbers has occurred inother areas of ALMNP, outside our present study area, withan intensity that seems approximately related to local deerpresence (Ferretti et al., unpubl. data). If red deer numbersare the main factor triggering depletion of summer foodresources for Apennine chamois, there may be reason ofconcern for the future of this vulnerable taxon. In the lastdecades, 80–200 red deer have been reintroduced to each of

several other Apennine national parks, where Apenninechamois have also been reintroduced, and their numbers areincreasing. The main reason for deer reintroductions hasbeen to provide a prey supply for the wolf, to reduce live-stock damage (e.g. Tassi, 1976; Boscagli, 1985). Most likely,park size, forest distribution pattern, dispersion and qualityof food resources differ between these areas, which maydetermine different ecological relationships between theseruminants. Our results indicate that an increase of red deerhas the potential to determine a decline of Apenninechamois, where they share the same limited food resource,for example T. thalii communities, rare and extra-zonal inthe Apennines (Ferrari et al., 1988), home of the vulnerableR. p. ornata. Pay-offs of reintroducing a locally extinct not-threatened species should be carefully considered, when itssharp increase may further endanger a threatened taxon,thus determining an ecological risk rather than a conserva-tion benefit (IUCN, 2012). In most European protectedareas, pristine habitats have been deeply altered by humans,making their restoration difficult. Thus, both short- andlong-term consequences of restoring operations (costs andbenefits) have to be very carefully considered beforehand.

AcknowledgementsWe are indebted to D. Febbo and G. Rossi for their con-tinuous support and backing. We thank the wardens M.Antonucci and M. D’Alessandro for their help in fieldwork,as well as the ALMNP staff for logistic support. We aregrateful to two anonymous reviewers, the Associate Editorand, especially, to D.M. Forsyth, who greatly improvedearlier drafts of this paper. We are grateful to D. Ubaldi forhis suggestions on vegetation analyses; to A. Catorci for hiscomments on B. genuense ecology; to C. Guacci for infor-mation on past grazing pressure. Financial support was pro-vided by the ALMNP Agency (partly within the ProjectLIFE09 NAT/IT/000183 Coornata, for some diet analyses).S.L. planned and supervised the research work, as well asparticipated in writing up all drafts; F.F. participated inresearch planning and wrote the first draft, conducted mostbehavioural observations and pellet group counts, as well asworked out relevant data; M.C. conducted most vegetationanalyses and participated in writing up all drafts; I.M. con-ducted food habit analyses and wrote about them; N.T.participated in vegetation analyses; C.F. supervised vegeta-tion analyses; A.S. conducted a part of behavioural obser-vations, in 2010.

References

Alm Bergvall, U., Rautio, P., Kesti, K., Tuomi, J. &Leimar, O. (2006). Associational effects of plant defencesin relation to within- and between-patch food choice by amammalian herbivore: neighbour contrast susceptibilityand defence. Oecologia 147, 253–260.

Altmann, J. (1974). Observational study of behaviour: sam-pling methods. Behaviour 49, 227–267.

S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 367

Page 10: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

Anthony, R.G. & Smith, N.S. (1977). Ecological relation-ships between mule deer and white-tailed deer in South-eastern Arizona. Ecol. Monogr. 47, 255–277.

Apollonio, M. & Lovari, S. (2001). Reintroduzioni di cervie caprioli nei parchi nazionali, con note sulleimmigrazioni naturali, In Progetto di monitoraggiodello stato di conservazione di alcuni Mammiferiparticolarmente a rischio della fauna Italiana: 462–475.Lovari, S. & Sforzi, A. (Eds). Roma: Ministerodell’Ambiente.

Armstrong, D.P. & Seddon, P.J. (2008). Directions in rein-troduction biology. Trends Ecol. Evol. 23, 20–25.

Augustine, D.J. & McNaughton, S.J. (1998). Ungulateeffects on the functional species composition of plantcommunities: herbivore selectivity and plant tolerance.J. Wildl. Manage. 62, 1165–1183.

Berger, J. (1985). Interspecific interactions and dominanceamong wild great basin ungulates. J. Mammal. 66, 571–573.

Bertolino, S. (2003). Herd defensive behaviour of chamois,Rupicapra rupicapra, in response to predation on theyoung by a golden eagle, Aquila chrysaetos. Mammalia49, 233–236.

Bertolino, S., di Montezemolo, N.C. & Bassano, B. (2009).Food-niche relationships within a guild of Alpineungulates including an intriduced species. J. Zool. 277,63–69.

Blasi, C. (1994). Fitoclimatologia del Lazio. Fitosociologia27, 151–175.

Blasi, C., Di Pietro, R. & Pelino, G. (2005). The vegetationof alpine belt karst-tectonic basins in the centralApennines (Italy). G Bot Ital 139, 357–385.

de Boer, W.F. & Prins, H.H.T. (1990). Large herbivoresthat strive mightily but eat and drink as friends.Oecologia 82, 264–274.

Boitani, L., Lovari, S. & Vigna Taglianti, A. (2003).Mammalia III: Carnivora – Artiodactyla, In Faunad’Italia, Vol. XXXVIII. Bologna: Calderini.

Boscagli, G. (1985). Il lupo: Udine: Lorenzini.Brambilla, P., Bocci, A., Ferrari, C. & Lovari, S. (2006).

Food patch distribution determines home range size ofadult male chamois only in rich habitats. Ethol. Ecol.Evol. 18, 185–193.

Braun-Blanquet, J. (1964). Pflanzensoziologie, 3rd edn:Wien, New York: Springer.

Bruno, E. & Lovari, S. (1989). Foraging behaviour ofadult female Apennine chamois in relation toseasonal variation in food supply. Acta Theriol. 34, 513–523.

Bunnell, F.L. & Gillingham, M.P. (1985). Foraging behav-iour: dynamics of dining out, In Bioenergetics of wild her-bivores: 53–79. Hudson, R.J. & White, R.G. (Eds). BocaRaton: CRC Press.

Catorci, A., Ottaviani, G., Vitasovic Kosic, I. & Cesaretti,S. (2011). Effect of spatial and temporal patterns of stress

and disturbance intensities in a sub-Mediterranean grass-land. Plant Biosyst. 146, 352–367.

Catorci, A., Antolini, E., Tardella, F.M. & Scocco, P.(2013). Assessment of interaction between sheep andpoorly palatable grass: a key tool for grassland manage-ment and restoration. J. Plant Interact. http://dx.doi.org/10.1080/17429145.2013.776706

Caughley, G. (1970). Eruption of ungulate populations,with emphasis on Himalayan tahr in New Zealand.Ecology 51, 53–72.

Cederna, A. & Lovari, S. (1985). The impact of tourism onchamois feeding activities in an area of the AbruzzoNational Park, Italy, In The biology and management ofmountain ungulates: 216–225. Lovari, S. (Ed.). London:Croom Helm.

Clutton-Brock, T.H., Guinness, F.E. & Albon, S.D. (1982).Red deer. Behavior and ecology of two sexes: Chicago:Chicago University Press.

Clutton-Brock, T.H., Albon, S.D. & Guinness, F.E. (1984).Maternal dominance, breeding success and birth sexratios in red deer. Nature 308, 358–360.

Clutton-Brock, T.H., Albon, S.D. & Guinness, F.E. (1986).Great expectations: dominance, breeding success and off-spring sex ratios in red deer. Anim. Behav. 34, 460–471.

Côté, S. & Festa-Bianchet, M. (2001b). Reproductivesuccess in female mountain goats: the influence of ageand social rank. Anim. Behav. 62, 173–181.

Côté, S.D. & Festa-Bianchet, M. (2001a). Birthdate, massand survival in mountain goat kids: effects of maternalcharacteristics and forage quality. Oecologia 127, 230–238.

Craig, B.H., Tempest, L.J., Pilkington, J.G. & Pemberton,J.M. (2008). Metazoan–protozoan parasite co-infectionsand host body weight in St Kilda Soay sheep. Parasitol-ogy 135, 433–441.

Crawley, M.J. (2007). The R Book: Chichester: John Wiley& Sons, Ltd.

D’Angeli, D., Testi, A., Fanelli, G. & Bianco, P.M. (2011).A focus on the landscape mosaics: vegetation map of‘Serra Rocca Chiarano – Monte Greco’ S.C.I (Abruzzo,Central Apennines).

Di Domenico, G., Tosoni, E., Boitani, L. & Ciucci, P.(2012). Efficiency of scat-analysis lab procedures for beardietary studies: the case of the Apennine brown bear.Mamm. Biol. 77, 190–195.

Dupré, E., Monaco, A. & Pedrotti, L. (2001). Pianod’azione nazionale per il Camoscio appenninico(Rupicapra pyrenaica ornata). Quad Cons. Natura 10,1–139. Min. Ambiente – Ist. Naz. Fauna Selvatica.

Fattorini, L., Ferretti, F., Pisani, C. & Sforzi, A. (2011).Two-stage estimation of ungulate abundance in Mediter-ranean areas using pellet group count. Envir Ecol Stat.18, 291–314.

Ferrari, C., Rossi, G. & Cavani, C. (1988). Summer foodhabits and quality of female, kid and subadult Apennine

Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

368 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London

Page 11: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

chamois, Rupicapra pyrenaica ornata Neumann, 1899(Artiodactyla, Bovidae). Z. Sauegetierk. 53, 170–177.

Ferretti, F., Sforzi, A. & Lovari, S. (2008). Intoleranceamongst deer species at feeding: roe deer are uneasy ban-queters. Behav. Process. 78, 487–491.

Ferretti, F., Sforzi, A. & Lovari, S. (2011). Behavioural inter-ference between ungulate species: roe are not on velvetwith fallow deer. Behav. Ecol. Sociobiol. 65, 875–887.

Festa-Bianchet, M. (1998a). Birthdate and survival inbighorn lambs (Ovis canadensis). J. Zool. 214, 653–661.

Festa-Bianchet, M. (1998b). Condition-dependent reproduc-tive success in bighorn ewes. Ecol. Lett. 1, 91–94.

Fico, R., Locati, M. & Lovari, S. (1984). A case of brownbear predation on Abruzzo chamois. Säugetierkd. Mitt.31, 185–187.

Focardi, S., Aragno, P., Montanaro, P. & Riga, F. (2006).Inter-specific competition from fallow deer Dama damareduces habitat quality for the Italian roe deer Capreoluscapreolus italicus. Ecography 29, 407–417.

Forsyth, D.M. (1997). Ecology and management of Himala-yan thar and sympatric chamois in the Southern Alps,New Zealand. Ph.D. Thesis, University of Lincoln.

Forsyth, D.M. & Caley, P. (2006). Testing the irruptiveparadigm of large-herbivore dynamics. Ecology 87, 297–303.

Forsyth, D.M. & Hickling, G.J. (1998). Increasing Himala-yan tahr and decreasing chamois densities in the easternSouthern Alps, New Zealand: evidence for interspecificcompetition. Oecologia 113, 377–382.

Forsyth, D.M., Barker, R.J., Morriss, G. & Scroggie, M.P.(2007). Modeling the relationship between fecal pelletindices and deer density. J. Wildl. Manage. 71, 964–970.

Frid, A. (1997). Vigilance by Dall’s sheep: interactionsbetween predation risk factors. Anim. Behav. 53, 799–808.

Gottfried, M., Pauli, H., Futschik, A. et al. (2012).Continent-wide response of mountain vegetation toclimate change. Nature Climate Change 2, 111–115.

Grottoli, L. (2011). Assetto territoriale ed ecologiaalimentare del lupo (Canis lupus) nel Parco Nazionaled’Abruzzo, Lazio e Molise. PhD Thesis. Università diRoma La Sapienza.

Herrero, J., Lovari, S. & Berducou, C. (2008). Rupicaprarupicapra. IUCN 2010. IUCN Red List of ThreatenedSpecies. Version 2010 (www.iucnredlist.org).

Hewison, A., Gaillard, J., Kjellander, P., Toïgo, C., Liberg,O. & Delorme, D. (2005). Big mothers invest more indaughters: reversed sex allocation in a weaklypolygynous mammal. Ecol. Lett. 8, 430–437.

Hofmann, R.R. (1989). Evolutionary steps ofecophysiological adaptation and diversification of rumi-nants: a comparative view of their digestive system.Oecologia 78, 443–457.

Hughes, J., Albon, S.D., Irvine, R.J. & Woodin, S. (2009).Is there a cost of parasites to caribou? Parasitology 136,253–265.

IUCN (2012). IUCN Guidelines for Reintroductions andother conservation translocations: Gland: SSC/Reintroduction Specialist Group.

Jaccard, P. (1901). Étude comparative de la distributionflorale dans une portion des Alpes et des Jura. Bull. Soc.Vaud. Sci. Nat. 37, 547–579.

Johnson, M.K., Wofford, H. & Pearson, H.A. (1983).Microhistological techniques for food habits analyses. Res.Pap. SO-199, Department of Agriculture Forest ServiceSouthern Forest Experiment Station, New Orleans.

Latham, J. (1999). Interspecific interactions of ungulates inEuropean forests: an overview. For. Ecol. Manage. 120,13–21.

Latham, J., Staines, B.W. & Gorman, M.L. (1997). Correla-tions of red (Cervus elaphus) and roe (Capreoluscapreolus) deer densities in Scottish forests with environ-mental variables. J. Zool. 242, 681–704.

Latini, R. (2010). Relazione dell’attività di pellet groupcount. Monitoraggio ungulati selvatici – ANNO 2010.Ente Parco Nazionale d’Abruzzo, Lazio, Molise, unpub-lished report.

Latini, R., Gentile, L., Asprea, A., Pagliaroli, D., Argenio,A. & Di Pirro, V. (2011). Stato dell’arte delle azioni A4 eC2 – Dicembre 2011. Ente Parco Nazionale d’Abruzzo,Lazio e Molise, unpublished report.

Latini, R., Asprea, A. & Pagliaroli, D. (2012). Conteggi insimultanea e monitoraggio della popolazione diCamoscio appenninico nel PNALM: nota sintetica deirisultati estivi 2012. Ente Parco Nazionale d’Abruzzo,Lazio, Molise, unpublished report.

Leopold, A. (1943). Deer irruptions. Wis. Cons. Bull. 8,3–11.

Lindström, J. (1999). Early development and fitness in birdsand mammals. Trends Ecol. Evol. 14, 343–348.

Locati, M. (1990). Female chamois defends kids from eagleattacks. Mammalia 54, 155–156.

Locati, M. & Lovari, S. (1988). La socialità nel camoscioappenninico Rupicapra pyrenaica ornata (Neumann,1899): confronto tra i sessi e suggerimenti di gestione.Atti I Convegno Nazionale di Biologia della Selvaggina,Bologna: 561.

Lovari, S. (1977). The Abruzzo chamois. Oryx 14, 47–50.Lovari, S. (1979). Etologia di campagna: Torino: Bollati

Boringhieri.Lovari, S. (1984). Il popolo delle rocce: Torino: Rizzoli.Lovari, S. (1985). Behavioural repertoire of the Abruzzo

chamois, Rupicapra pyrenaica ornata Neumann,1899 (Artiodactyla: Bovidae). Säugetierkd. Mitt. 32, 113–136.

Lovari, S., Artese, C., Damiani, G. & Mari, F. (2010).Re-introduction of Apennine chamois to the Gran Sasso-Laga National Park, Abruzzo, Italy, In Globalre-introduction perspectives: additional case-studies fromaround the globe: 281–284. Soorae, P.S. (Ed.). AbuDhabi: IUCN/SSC Re-introduction Specialist Group.

S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 369

Page 12: Unexpected consequences of reintroductions: competition between reintroduced red deer and Apennine chamois

Lummaa, V. & Clutton-Brock, T. (2002). Early develop-ment, survival and reproduction in humans. Trends Ecol.Evol. 17, 141–147.

Mari, F. & Lovari, S. (2006). Il camoscio appenninico: unritorno in corso, In Salvati dall’arca: 131–142. Fraissinet,M. & Petretti, F. (Eds). Udine: Perdisa.

Masini, F. & Lovari, S. (1988). Systematics, phylogeneticrelationships and dispersal of the chamois Rupicapra spp.Quat. Res. 30, 339–349.

Mayle, B.A., Peace, A.J. & Gill, R.M.A. (1999). How manydeer? A field guide to estimating deer population size:Edinburgh: Forestry Commission Field Book 18.

Meriggi, A. & Lovari, S. (1996). A review of wolf predationin Southern Europe: does the wolf prefer wild prey towildstock? J. Appl. Ecol. 33, 1561–1571.

Minder, I. (2012). Local and seasonal variations of roe deerdiet in relation to food resource availability in a Mediter-ranean environment. Eur. J. Wildl. Res. 58, 215–225.

Moquin, P., Curry, B., Pelletier, F. & Ruckstuhl, K.E.(2010). Plasticity in the rumination behaviour of bighornsheep: contrasting strategies between the sexes? Anim.Behav. 79, 1047–1053.

Mustoni, A., Pedrotti, L., Tosi, G. & Zanon, E. (2002).Ungulati delle Alpi: biologia, riconoscimento, gestione:Trento: Nitida Immagine.

Namgail, T., Mishra, C., de Jong, C.B., van Wieren, S.E. &Prins, H.H.T. (2007). Effects of herbivore species richnesson the niche dynamics and distribution of blue sheep inthe Trans-Himalaya. Divers. Distrib. 15, 940–947.

Neuhaus, P. & Ruckstuhl, K.E. (2002). Foraging behaviourin Alpine ibex (Capra ibex): conseguences of reproductivestatus, body size, age and sex. Ethol. Ecol. Evol. 14, 373–381.

Owen-Smith, N. & Neiville, P. (1982). What should a cleverungulate eat? Am. Nat. 119, 151–178.

Patalano, M. & Lovari, S. (1993). Food habits and trophicniche overlap of the wolf (Canis lupus, L. 1758) and thered fox Vulpes vulpes (L. 1758) in a Mediterraneanmountain area. Rev. Ecol. 48, 279–294.

Petraglia, A. & Tomaselli, M. (2007). Phytosociologicalstudy of the snowbed vegetation in the NorthernApennines (Northern Italy). Phytocoenologia 37, 67–98.

Pettorelli, N., Gaillard, J.M., Yoccoz, N.G., Duncan, P.,Maillard, D., Delorme, D., Van Laere, G. & Toïgo, C.(2005). The response of fawn survival to changes inhabitat quality varies according to cohort quality andspatial scale. J. Anim. Ecol. 74, 972–981.

Pettorelli, N., Pelletier, F., von Hardenberg, A.,Festa-Bianchet, M. & Côté, S.D. (2007). Early onset of

vegetation growth vs. rapid green-up: impacts on juvenilemountain ungulates. Ecology 88, 381–390.

Pianka, E.R. (1973). The structure of lizard communities.Ann. Rev. Ecol. Syst. 4, 53–74.

Putman, R.J. (1996). Competition and resource partitioningin temperate ungulate assemblies: London: Chapman &Hall.

Putman, R.J. & Sharma, S.K. (1987). Long term changes inNew Forest deer populations and correlated environmen-tal change. Symp. Zool. Soc. Lond. 58, 167–179.

R Development Core Team (2009). R: a language and envi-ronment for statistical computing: Vienna: R Foundationfor Statistical Computing.

Richard, E., Gaillard, J.M., Saïd, S., Hamann, J.L. &Klein, F. (2010). High red deer density depresses bodymass of roe deer fawns. Oecologia 163, 91–97.

Rossi, G. (1985). Osservazioni sull’alimentazione delcamoscio appenninico (Rupicapra pyrenaica ornata).Primo contributo. MSc Thesis, Università di Bologna.

Ruckstuhl, K.E., Festa-Bianchet, M. & Jorgenson, J.T.(2003). Bite rates in Rocky Mountain bighorn sheep(Ovis canadensis): effects of season, age, sex and repro-ductive status. Behav. Ecol. Sociobiol. 54, 167–173.

Schöb, C., Kammer, P.M., Choler, P. & Veit, H. (2009).Small-scale plant species distribution in snowbeds and itssensitivity to climate change. Plant Ecol. 200, 91–104.

Schröder, J. & Schröder, W. (1984). Niche breadth andoverlap in red deer Cervus elaphus, roe deer Capreoluscapreolus and chamois Rupicapra rupicapra. A. Zool.Fenn. 172, 85–86.

Sinclair, A.R.E. & Northon-Griffiths, M. (1982). Does com-petition or facilitation regulate migrant ungulate popula-tions in the Serengeti? A test of hypotheses. Oecologia 53,364–369.

Smith, D.W., Peterson, R.O. & Houston, D.B. (2003).Yellowstone after wolves. Bioscience 53, 330–340.

Sokal, R.R. & Rohlf, F.J. (1995). Biometry: the principlesand practice of statistics in biological research, 3rd edn:New York: W. H. Freeman.

Tassi, F. (1976). La reintroduzione degli ungulati nell’-Appennino Centrale. Camerino and Roma: SOS Fauna:Animali in Pericolo Di Estinzione.

Supporting informationAdditional Supporting Information may be found in theonline version of this article at the publisher’s web-site:

Appendix S1. Supplementary online material.

Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

370 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London