Does early antipredator training increase the suitability of captive red-legged partridges (Alectoris rufa) for releasing? V. R. Gaudioso,* C. Sánchez-García,*1 J. A. Pérez,† P. L. Rodríguez,‡ J. A. Armenteros,* and M. E. Alonso* *Research Group on Game Species Breeding and Management, Departamento de Producción Animal, Facultad de Veterinaria, Campus de Vegazana, 24071, León, Spain; †Global Sigma S.L., Onzonilla 24231, León, Spain; and ‡Departamento de Nutrición Animal, Universidad de Extremadura, 10071, Cáceres, Spain ABSTRACT This study aimed to evaluate the postrelease survival and spatial distribution of farmbred red-legged partridges (Alectoris rufa) that were subject to a prerelease training program based on exemplary behavior and alarm calls given by adults that acted as experienced demonstrators in simulated predator encounters (wooden raptor models and humans). Two groups of partridges were released in this study: trained (intensively reared birds accompanied by tutors) and control (chicks reared without tutors). Releases were conducted in the fall and winter–spring during 2 consecutive years using a total of 44 trained and 40 control radio-tagged partridges. Trained partridges showed statistically higher mean values of survival (72.7 d), home range (13.04 ha), and dispersion (549.58 m) compared with nontrained partridges, with most non-
trained birds failing to survive more than 2 wk after release. Trained adult partridges showed the best survival results (105.2 d). Taking all birds into account, causes of death were attributed to terrestrial predators (45%), raptors (18.7%), hunting (11.3%), and unknown causes (25%). Although values of variables reported here were lower than those reported in wild counterparts, survival time and spatial behavior of trained birds were close to that of previous data of parent-reared partridges and higher than that of farm-bred birds. This study aimed to confirm the potential of prerelease training techniques in present-day rearing systems. Farm-bred game birds, which normally suffer from high predation rates after release, could highly benefit from the use of cost-effective training techniques based on learning from experienced adults.
Key words: Alectoris rufa, farm bred, red-legged partridge, release, training 2011 Poultry Science 90:1900–1908 doi:10.3382/ps.2011-01430
INTRODUCTION Game birds have been successfully reared in captivity throughout the world during the past century, and millions of birds have been released into the wild for shooting and conservation purposes (Sokos et al., 2008). However, rearing and releasing methods from early research projects (Leopold et al., 1938) have been questioned because a large percentage of birds are not capable of surviving or breeding in the wild after release (Roseberry et al., 1987; Brittas et al., 1992; Pérez et al., 2004; Alonso et al., 2005; Parish and Sotherton, 2007; Buner et al., 2011). One of the major causes of failure is the incorrect development and maintenance of antipredator responses
©2011 Poultry Science Association Inc. Received February 20, 2011. Accepted April 29, 2011. 1 Corresponding author:
[email protected]
(Pérez et al., 2010; Rantanen et al., 2010), attributed to isolation from predators (Gaudioso et al., 2011), absence of parents during rearing (Putaala, 1997), and habituation to humans (Csemerly et al., 1983). Some projects on seminatural rearing have been conducted over the past few decades (Gaudioso et al., 2002; Buner and Aebischer, 2008), and it has been demonstrated that birds’ antipredatory behavior, survival, and breeding success can be improved (Buner and Schaub, 2008; Buner et al., 2011), though these methods are costly, which hampers their viability. On the other hand, an experiment conducted on rock partridge (Alectoris graeca) chicks raised under intensive rearing methods (Zaccaroni et al., 2007) suggests that the use of lowcost treatments that cause an early fear experience in chicks result in better predator avoidance. This is the case for antipredator training, an alternative rearing technique used in a wide range of captivebred animals (Griffin et al., 2000) that has shown encouraging results for endangered species (van Heezik et al., 1999; Angulo, 2004). This method is based on
1900
1901
POSTRELEASE SURVIVAL OF TRAINED PARTRIDGES
providing a conditioned or an unconditioned stimulus to animals with the aim of inducing antipredator responses after correct predator recognition, especially in early stages of life (Griffin et al., 2000). In addition, it has been reported that the escape responses of experienced demonstrators improve the antipredator behavior of young learners (Shier and Owings, 2007), which confirms that social transmission of defensive patterns is possible under captive conditions. Taking the suggestions of Griffin et al. (2000) into account, prerelease antipredator training can be a useful tool for many species’ recovery programs, but little empirical research is available on game birds (Ellis et al., 1977; Zaccaroni et al., 2007). Moreover, evidence exists that incorrect training techniques lead to habituation or incorrect behavioral displays (Starling, 1991). With the aim of developing antipredator training techniques in game birds, a research program was conducted in the red-legged partridge (Alectoris rufa), a commonly hunted galliforme of Western Europe (Aebischer and Lucio, 1997). Following the guidelines proposed by World Pheasant Association–IUCN (2009), intensively reared broods of red-legged partridges accompanied by tutors, which acted as experienced demonstrators, were subjected to simulated predation encounters (conditioned stimulus). The objective was to create an effective stimulus and induce natural alarm calls and exemplary behavior in adult partridges with the aim of eliciting antipredator responses on intensively reared broods. The improvement of prerelease behavioral responses during training could indicate a better preparation for releasing but is not a predictor of postrelease survival (Dowell, 1990; van Heezik et al., 1999). Thus, the purposes of this research were to study the postrelease survival rate, home range, and causes of death of trained red-legged partridges reared in intensive systems and, consequently, to evaluate the effects of antipredator training.
MATERIALS AND METHODS Rearing Methods and Description of Prerelease Training Program All birds were raised for 2 consecutive years on a private intensive game farm (in the province of León, northwest Spain, 997 m above sea level) that followed classical rearing methods for red-legged partridges (Sánchez-García et al., 2009; González-Redondo et al., 2010). Birds were hatched in an incubator and broods were raised to an average brood size of 800 chicks/ brooder house (Table 1). This game farm was chosen mainly because of its distance from urban environment and highways and the presence of raptors such as goshawk (Accipiter gentiles), sparrow hawk (Accipiter nisus), golden eagle (Aquila chrysaetos), short-toed eagle (Hieraaetus pennatus) and Eurasian eagle-owl (Bubo
Table 1. Rearing groups and brood size used in this study and number of partridges released per year (trained/control) with regard to life phase and sex Phase Rearing Year
Brood
2008
Trained Control Trained Control
2009
2008 2009
No. of chicks at start 800 800 800 800
No. of poults at 4 wk 763 778 685 774
Releasing Life phase
Females
Males
Adult Subadult Adult Subadult Total
4/5 6/5 6/6 5/4 21/20
5/5 6/5 6/5 6/5 23/20
bubo), which are natural predators of partridges in Spain (Duarte et al., 2008). Two groups of birds were reared in this study: trained (T; intensively reared birds accompanied by tutors) and control (C; chicks reared without tutors). Parent pairs of adult red-legged partridges that had hatched and reared their own brood were used in this study as tutors. Understanding that wild birds display better antipredator behavior than farm-reared birds (Pérez et al., 2010), each pair consisted of a farm-reared female and a wild male that were trapped in the wild complying with Spanish law. These birds were previously paired in seminatural breeding cages (early February, following the same methodology mentioned by Gaudioso et al., 2002) and maintained with their brood until their own chicks were 8 to 9 d old. Parent pairs were chosen because of the possible effects of parental behavior on antipredator patterns, not yet studied in the red-legged partridge but well documented in a similar study on domestic hens (Gallus gallus; Palleroni et al., 2005). It was expected that after conditioned predation events, tutors would produce alarm calls and show exemplary antipredator behavior in the presence of hatched chicks (Gyer et al., 1986). Because of the high number of chicks and disease and accident risks, each tutor pair was placed in a specific experimental cage in the brooder house before the arrival of the chicks (Figure 1). The cage was positioned in one corner of the brooder house so that adults could see the chicks, but physical contact with the brood was prevented until the protective ring was removed. The experimental cage was constructed with galvanized metal and wire mesh, and a feeding box (with commercial feed) and drinking trough were placed in the cage. Procedures were based on classical conditioned predatory stimulus carried out on gray partridges (Perdix
1902
Gaudioso et al.
Figure 1. Sketch of the brooder house, the specific metal cage for tutors, and the aerial predator test used in this study.
perdix) and pheasants (Phasianus colchicus) by Dowell (1990) and Beani and Dessi-Fulgheri (1998). With the aim of understanding the effects of consecutive artificial predatory stimuli on tutors and considering that the antipredator behavior of broods may be influenced by age and escape ability, tests were carried out at 3 phases of chicks’ growth. In phase 1, first tests were carried out from d 1 to 5 of life because it has been suggested that in the species the sensitive period of imprinting ends 48 h after hatching (Csemerly et al., 1983). Chicks can flutter-fly from 11 to 12 d of age. In phase 2, tests continued from d 15 to 17 of life. After 1 mo of life, poults are able to complete a mediumdistance flight and have partial thermoregulation capability. In phase 3, tests were carried out from d 30 to 33 of life. Both T and C partridges were exposed to 4 types of tests. In the first test (the aerial predator test), an aerial predator model was used following classical methods of Tinbergen (1957). Taking into account that the goshawk (Accipiter gentilis) is a natural predator of the red-legged partridge in the area, a life-size wooden model of a flying female was chosen. The model was placed on a stick and hand-pulled across the windows at a steady pace of 5 m/s (Figure 1). The predatory stimuli lasted between 1 and 2 s. In the second test (the aerial predator control test), the stick without the raptor model was hand-pulled across the windows at the same speed as a control test. In the third test (the human predation test), a different operator entered the brooder house trying not making noise or cause disturbance for 10 s. According to Zaccaroni et al. (2007), when Alectoris graeca chicks are exposed to human disturbances at an early age,
stronger antipredatory responses and greater distances in escape reaction are displayed by birds at 5 mo of age. In our study, the aim of this experiment was to test the ability of tutors and chicks to produce fear responses in presence of humans and, consequently, no disturbance was caused. In the fourth test (the human predation control test), the first step involved opening the door of the brooder house. Opening the door partially for 2 to 3 s was considered a control test for any slight noise or movement caused. All tests were carried out in July and August of 2 consecutive years (2007–2008). To avoid possible effects at any moment of the day, tests were carried out in the morning–afternoon (0900–1400 h) and the evening (1500–1900 h). To prevent possible habituation, no more than 2 exposures tests were applied per day. In total, each brood was subjected to 40 to 50 tests before being changed to the flight pen. Adults were also changed to the pens with the whole brood after training and were not removed until the release date. Birds released in winter-spring spent a longer period with tutors in the pens. Partridges were subjected to health and genetic checks throughout the study period. Health checks consisted of detecting Eimeria spp. and helminths from feces analysis, and serum samples were used to establish the serotypes of Salmonella spp. (ELISA) in adults and poults after tests were conducted. In addition, feces were used to discard avian influenza and Newcastle virus, following the Spanish law (Millán, 2009). With the aim of excluding possible hybridization with Chukar partridge (Alectoris chukar) and inbreeding depression, birds were also subjected to a genetic check based on microsatellite analysis (Tejedor et al., 2008).
1903
POSTRELEASE SURVIVAL OF TRAINED PARTRIDGES Table 2. Characteristics, hunting management practices, and density of predators in the property where partridges were released (2008–2009), following the methods of Casas and Viñuela (2010) Item
Value
Surface covered (ha) Altitude (m) Rainfall (mm/yr) Hunters (n) Wild partridge density, autumn (birds/yr per ha) Hunting bag, average for entire study (birds/yr per ha) Raptors (n/100 ha) Hen harrier (Circus cyaneus) Western marsh harrier (Circus aeruginosus) Goshawk (Accipiter gentilis) Sparrowhawk (Accipiter nisus) Short-toed eagle (Circaetus gallicus) Booted eagle (Aquila pennata) Peregrine falcon (Falco peregrinus) Predator control period1 (n of individuals captured/individuals per 100 ha) Fox (Vulpes vulpes) Magpie (Pica pica) Feral dog (Canis familiaris) Water troughs (n/100 ha) Feeders (n/100 ha) Wild rabbit density (n/ha) Gamekeeper density (n/ha) 1During
5,950 760–880 995 120 0.21 0.11 0.5 0.15 0.06 0.1 0.06 0.08 0.07 34/0.16 73/1.67 6/0.08 None None 0.03 0.0002
the breeding season (April–May).
Study Site Partridges were released on private hunting property located in the province of León (lat 42°21′0.57″ N, long 5°28′39.19″ W; northern Spanish Meseta). The area is an optimal habitat for the species (Buenestado et al., 2008), with vineyards (65%); cultivated lands (25%) of barley (Hordeum districhon), alfalfa (Medicago sativa), and sunflower (Helianthus annuus); and arboreal species (10%; Cystius spp.). Because of the high diversity of avian fauna (especially raptors), the area is included in a special protection area for birds of the European Natura 2000 network (Sanz-Zuasti et al., 2004). This area was not affected by agricultural intensification and abandonment of traditional farming practices. Data on wild populations of partridges, game management, predators, control of predators, and shooting are given in Table 2.
Release Methodology and Radiotracking A total of 84 radio-tagged partridges (44 T, 40 C) were released in this study over 2 yr. Radiotracking followed procedures similar to those described by Pérez et al. (2004) and field work lasted until the battery ended (maximum 300 d) or the bird was found dead. The death was classified into 4 categories of probable causes of mortality: raptors, terrestrial predators, unknown causes, and hunting. Following Robinson et al. (2009), we refer to probable causes of mortality rather than cause-specific mortality because it is difficult to make unambiguous statements regarding causes of mortality due to potential scavenging (Larsen et al., 2008). With the aim of comparing the effects of life phase and sex on the survival of the birds, releases were con-
ducted in the fall using 3- to 4-mo-old birds (subadults) and in late winter–early spring using 9- to 10-mo-old birds (adults). Groups of 2 or 3 radio-tagged partridges were released using common crates (cages used for transporting animals) that were opened so that the birds could leave voluntarily and avoid any manipulation or forced release; this is considered a hard release (Buner et al., 2011). All releases were conducted at sunrise for 2 consecutive weeks in the same location, preventing bird concentration and trying not to attract predators (Church et al., 1984). Radiotracking was conducted daily the first week and the subsequent interval between consecutive locations was 4 ± 1.6 (SE) days. Information related to releases is given in Table 1.
Data Analysis Survival was defined as the number of days the partridge stayed alive after release date and was calculated using a Kaplan-Meier test (Kaplan and Meier, 1958). Following the survival function of product-limit estimator, dead partridges were uncensored cases (1) and live partridges were censored cases (0). Because of the small sample size, Mantel-Cox test was used to assess possible differences between survival and variables considered. Home range analysis was conducted using Arc View software (version 3.2., Esri, Redlands, CA), with the Spatial Analyst and the Animal Movement Analysis extensions (Hooge and Eichenlaub, 1997). With the aim of comparing home range values with previous studies and considering the small number of locations found for some individuals, this was calculated using a 95% minimum convex polygon. Differences attributed to type of brood and age in the quantitative variables were analyzed with ANOVA
1904
Gaudioso et al.
Table 3. Mean values (±SE) of survival, home range (MCP), dispersion, and cause of deaths in trained (T) and control (C) partridges Cause of death1 (%) Group
Life phase
Release date
Survival (d)
C
Adult Subadult Overall Adult Subadult Overall
Winter–spring Fall
17.8 13.3 15.1 105.2 45.6 72.7
T
1R:
Winter–spring Fall
± ± ± ± ± ±
3.9 1.6 1.8 25.5 5.9 12.7
MCP (ha) 4.19 6.17 4.97 14.82 11.61 13.04
± ± ± ± ± ±
0.98 0.87 0.7 3.76 3.59 2.5
Dispersion (m) 373.39 445.19 401.6 627.64 486.38 549.58
± ± ± ± ± ±
67.9 69.9 49.14 94.23 63.68 55.34
R
TP
U
H
25 12.5 17.5 20 16.6 18.2
50 57.1 50 30 41.6 36.6
25 16.6 20 40 29.2 34.1
0 20.8 12.5 10 12.5 11.3
raptors; TP: terrestrial predators; U: unknown; H: hunting.
(Canavos, 1986), fitting a model with type of brood, sex, and their interaction as Yijk = μ + Ai + Bj + ABij + έijk, where Yijk = observation on the kth bird from type of brood i and age j, μ = general mean value, Ai = effect of type of brood (T or C), Bj = effect of sex, ABij = interaction between both factors, and έijk = error. The comparison between cause of death and the other variables considered was analyzed using the Kruskal-Wallis test (Siegel and Castellan, 1988). Possible correlations between survival time, home range, and dispersion were calculated using linear models. Differences with P < 0.05 were considered significant and all tests were conducted using SPSS (version 17.0 for Windows, StatSoft Inc., Tulsa, OK). Values of survival, home range size, and dispersion are reported as means with SE.
Ethical Note This study complied with the guidelines of Federation of Animal Science Societies (1999) and the guidelines of International Society for Applied Ethology (Sherwin et al., 2003). The experimental cage in which tutors were kept was designed to provide welfare and the training program was conducted to cause effective antipredator responses in intensively reared broods, avoiding prolonged distress.
hours. Considering all partridges released, survival time differed significantly between T and C groups (MantelCox test, χ2 = 32.14, df = 1, P < 0.05, Table 3). As shown in Figure 2, the survival rate for C birds was 50% during the first 2 wk, and none of these partridges survived for more than 53 d. No statistical differences were found between survival time and life phase (χ2 = 3.39, df = 1, P = 0.1). In C partridges, survival was not affected by life phase (χ2 = 1.9, df = 1, P = 0.16) or by the interaction of sex and life phase. With regard to T birds, adult birds showed higher survival values compared with the subadults (χ2 = 4.63, df = 1, P < 0.05), and 4 birds released in winter-spring survived more than 300 d (3 males and one female). However, as reported for C partridges, survival values were not affected by life phase and sex. As expected, linear correlations were detected between survival rate and home range (r = 0.61, P < 0.05) and dispersion (r = 0.52, P < 0.05) on an individual basis irrespective of group, life phase, and sex.
Probable Causes of Death Causes of death were quite similar for T and C birds (χ2 = 1.47, df = 1, P = 0.22), not being affected by life
RESULTS No statistical differences were found between years and survival (χ2 = 8.71, df = 1, P = 0.3), home range (F1, 64 = 0.23, P = 0.63), and dispersion (F1, 64 = 0.01, P = 0.91). Following the methods of Gaudioso et al. (2011), this allowed us to subsequently consider data independent of years, using the ANOVA and the Kruskal-Wallis test to study the possible differences between T and C partridges.
Postrelease Survival A total of 1,039 radiolocations were carried out in this study, with approximately 1,530 field-effort man
Figure 2. Overall Kaplan-Meier survival function for trained and control partridges in this study.
POSTRELEASE SURVIVAL OF TRAINED PARTRIDGES
(χ2
phase = 0.004, df = 1, P = 0.94). Considering all birds, analysis indicated that predators were responsible for 63.7% of mortalities (n = 51). Based on signs (in most cases excrement) and tracks found near the carcasses, 36 partridges were killed by terrestrial predators (45%), the main source of death in this study, and 15 birds were predated by raptors (18.7%). Determining probable cause of death was very difficult in a considerable percentage of birds (n = 20, 25%), and the rest of the deaths were attributed to hunting (n = 9; 11.3%). Four necropsies were conducted but none of the deaths reported in this study were attributable to disease.
Home Range To increase the statistical significance when comparing home range and dispersion, partridges that survived less than 1 wk (20%). Determining probable cause of death was very difficult in a considerable percentage of the birds (25%), though scavenged carcasses suggest predation as the probable cause of death (Robinson et al., 2009). It is encouraging to see that the percentage of deaths attributed to raptors (18.7%) was lower compared with previous studies conducted in a similar area in northern Spain (41–50%, Pérez et al., 2004; 43%, Alonso et al., 2005), though a different predator density was recorded in those studies. This finding supports conclusions by van Heezik et al. (1999) and Mc Lean et al. (1999), indicating that birds can be instructed on predators and use this knowledge to avoid predation after release, though in general it does not lead to increased postrelease survival (Dowell, 1990; van Heezik et al., 1999). In contrast, all birds were not trained against terrestrial predators during the prerelease stage and this was the main source of death. Given the characteristics of the tests, the space limitation in the brooder house, and the possible negative consequences of brood reaction (chicks piling up and flattening against the ground), training against terrestrial predators using dummies, stuffed animals, or video animations inside the brooder house was discarded. However, further research will consider these predators.
1906
Gaudioso et al.
With regard to the home range and dispersion, T birds tended to have larger ranges compared with C birds (Table 3), not being affected by sex or age. Following the conclusions by Alonso et al. (2005) and Gaudioso et al. (2011), farm-bred partridges that survive longest tend to have a bigger home range and wider dispersion, trying to distract predator attention and avoid concentration at any one point. It is interesting to note, however, that values reported in both groups of birds were lower compared with wild partridges (26.91 ha, Pérez, 2006; 13.5–132.9 ha, Buenestado et al., 2008), probably because it was not possible to exclude the influence of competitive interactions with local partridges (Green, 1983). This study confirms that the prerelease training program conducted on captive red-legged partridges, using tutors as experienced demonstrators, improved the postrelease survival and spatial behavior of birds; survival time, home range, and dispersion were mainly affected by prerelease training. Considering that the only difference between T and C birds was the presence of experienced tutors, marked differences between both groups of birds could be explained by the effects of social learning on the development of antipredator behavior (Shier and Owings, 2007). The C birds would learn from conspecifics during training (Nicol, 2006), but the antipredatory skills acquired learning from other chicks would be poor compared with those of T birds, which acquired antipredator knowledge from tutors. Similar to parent-reared and fostered chicks of Gray and red-legged partridges (Anttila et al., 1995; Pérez, 2006; Buner and Schaub, 2008), experience of tutors would benefit predator-naïve individuals. As previously mentioned, values reported in T birds for winter–spring releases were close to those reported in parent-reared birds of the same age released in a similar area in Spain (average 107.48; Pérez, 2006). These results are consistent with earlier work by Shier and Owings (2007), who stated that postrelease survival in juvenile black-tailed prairie dogs (Cynomys ludovicianus) increased when animals were trained with experienced tutors. Research also agrees with previous conclusions of prerelease training programs tested in different species (Vilhunen et al., 2005; Oliveira and Young, 2007) and the postrelease survival values reported by Ellis et al. (1977) in masked bobwhite quails (Colinus virginianus) and Angulo (2004), who trained white-winged guans (Penelope albipennis) against aerial predators with a Harris’ hawk (Parabuteo unicinctus). Our study could have been improved by training against terrestrial predators, an important source of death in wild and farm-bred partridges, and a future study will examine the breeding success and social interactions of birds after release because released animals must not only survive to reproductive age, but must breed successfully and have offspring that also breed (Mathews et al., 2005).
To our knowledge, this is the first prerelease training program conducted on the red-legged partridge that proves a better survival of farm-bred trained birds. As suggested by Zaccaroni et al. (2007) and Sokos et al. (2008), game bird farmers and managers should consider introducing low cost treatments in current rearing systems to face the challenge of rearing birds suitable for restocking purposes. Taking into account the results of parent-reared game birds and results of training programs, using social transmission procedures based on experienced demonstrators may provide ecological, economical, and ethical advantages (Griffin et al., 2000; Vilhunen et al., 2005). The results shown here have implications for the conservation of related galliformes (World Pheasant Association–IUCN, 2009) and other endangered bird species.
ACKNOWLEDGMENTS This study is part of the second author’s PhD thesis, financially supported by the University of León (Spain). We are grateful to F. Buner, J. Ewald and N. Aebischer, who helped to improve this manuscript. Special thanks are extended to Gerardo, Luis Miguel, and Victor Molleda for their assistance on the game farm. We also thank the Pajares de los Oteros’ Hunting Society (León, Spain) for their permission and support throughout the field work. Courtnee L. Henry and Donal Savage provided linguistic revision on early drafts. This work was funded partially by the Junta de Castilla y León (Spain), the Excelentísima Diputación de León (Spain), and Caja España (Spain).
REFERENCES Aebischer, N. J., and A. Lucio. A. 1997. Red-legged partridge Alectoris rufa. Pages 208–209 in The EBCC Atlas of European Breeding Birds: Their Distribution and Abundance. W. J. M. Hagemeijer and M. J. Blair, ed. T. & A. D. Poyser, London, UK. Alonso, M. E., J. A. Pérez, V. R. Gaudioso, C. Díez, and R. Prieto. 2005. Study of survival, dispersal and home range of autumnreleased red-legged partridges (Alectoris rufa). Br. Poult. Sci. 46:401–406. Angulo, P. F. 2004. Dispersión, supervivencia y reproducción de la pava aliblanca Penelope albipennis Taczanowski 1877 (Cracidae) reintroducida a su hábitat natural en Perú. Ecologia Aplicada 3:112–117. Anttila, I., A. Putaala, and R. Hissa. 1995. Tarhattujen ja villien peltoyyn poikasten käyttäytymisestä. Suomen Riistu. 41:53–65. Beani, L., and F. Dessi-Fulgheri. 1998. Anti-predator behaviour of captive Grey partridges (Perdix perdix). Ethol. Ecol. Evol. 10:185–196. Brittas, R., V. Marcstrom, R. E. Kenward, and M. Karlbom. 1992. Survival and breeding success of reared and wild ring-necked pheasants. J. Wildlife Manage. 56:368–376. Buenestado, F. J., P. Ferreras, J. A. Blanco-Aguiar, F. S. Tortosa, and R. Villafuerte. 2009. Survival and causes of mortality among wild red-legged partridges Alectoris rufa in southern Spain: Implications for conservation. Ibis 151:720–730. Buenestado, F. J., P. Ferreras, M. Delibes-Mateos, F. S. Tortosa, J. A. Blanco-Aguiar, and R. Villafuerte. 2008. Habitat selection and home range size of red-legged partridges in Spain. Agric. Ecosyst. Environ. 126:158–162.
POSTRELEASE SURVIVAL OF TRAINED PARTRIDGES Buner, F., and N. J. Aebischer. 2008. Guidelines for Reestablishing Grey Partridges Through Releasing. Game and Wildlife Conservation Trust, Fordingbridge, UK. Buner, F., and M. Schaub. 2008. How do different releasing techniques affect the survival of reintroduced grey partridges Perdix perdix? Wildlife Biol. 14:26–35. Buner, F. D., S. J. Browne, and N. J. Aebischer. 2011. Experimental assessment of release methods for the re-establishment of a red-listed galliforms, the grey partridge (Perdix perdix). Biol. Conserv. 144:593–601. Canavos, G. C. 1986. Probabilidad y Estadística. Aplicaciones y Métodos. McGraw Hill, Madrid, Spain. Carvalho, J., D. Castro, M. Capelo, and R. Borralho. 1998. Redlegged partridge (Alectoris rufa) restocking programs: Their success and implications on the breeding populations. Game Wildlife Sci. 15:465–474. Casas, F., and J. Viñuela. 2010. Agricultural practices or game management: Which is the key to improve red-legged partridge nesting success in agricultural landscapes? Environ. Conserv. 37:177–186. Church, K. E., W. F. Porter, and D. E. Austin. 1984. Procedures for introducing gray partridge into unoccupied range in New York. Pages 54–57 in Perdix III: Gray Partridge/Ring Necked Pheasant Workshop. R. T. Dumke, R. B. Stiehl, R. B. Kahl, ed. Wis. Dept. Nat. Resour., Campbellsport, WI. Csemerly, D., D. Mainardi, and S. Spanó. 1983. Escape reaction of captive re-legged partridges (Alectoris rufa) reared with or without visual contact with man. Appl. Anim. Ethol. 11:177–182. Dowell, S. D. 1990. The ontogeny of anti-predator behaviour in game bird chicks. PhD Thesis. University of Oxford, UK. Duarte, J., M. A. Farfán, and J. C. Guerrero. 2008. Importancia de la predación en el ciclo anual de la perdiz roja. Pages 133–141 in Especialista en Control de Predadores. J. L. Garrido, ed. Federación Española de Caza, Madrid, Spain. Duarte, J., M. A. Farfán, and J. M. Vargas. 2010. New data on mortality, home range and dispersal of red-legged partridge (Alectoris rufa) released in a mountain range. Eur. J. Wildlife Res. 57:675–678. doi:10.1007/s10344-010-0467-9. Duarte, J., and J. M. Vargas. 2004. Field interbreeding of released farm-reared red-legged partridges (Alectoris rufa) with wild ones. Game Wildlife Sci. 21:55–61. Ellis, D. H., S. J. Dobrott, and J. G. Goodwin. 1977. Reintroduction techniques for masked bobwhites. Pages 345–354 in Endangered Birds: Management Techniques for Preserving Threatened Species. S. A. Temple, ed. University of Wisconsin Press, Madison. Federation of Animal Science Societies. 1999. Guidelines for the Care and Use of Agricultural Animals in Agricultural Research and Teaching. 1st rev. ed. Federation of Animal Science Societies, Champaign, IL. Gaudioso, V. R., M. E. Alonso, R. Robles, J. A. Pérez, and J. A. Olmedo. 2002. Effects of housing type and breeding system on the reproductive capacity of the red-legged partrigde (Alectoris rufa). Poult. Sci. 81:169–172. Gaudioso, V. R., J. A. Pérez, C. Sánchez-García, J. A. Armenteros, J. M. Lomillos, and M. E. Alonso. 2011. Isolation from predators: A key factor in the failed release of farmed red-legged partridges (Alectoris rufa) to the wild? Br. Poult. Sci. 52:155–162. González-Redondo, P., M. Delgado-Pertínez, S. Toribio, F. A. Ruiz, Y. Mena, F. P. Caravaca, and J. M. Castel. 2010. Characterisation and typification of the red-legged partridge (A. rufa) game farms in Spain. Span. J. Agric. Res. 8:624–633. Gortázar, C., R. Villafuerte, and M. Martín. 2000. Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragón. Z. Jagdwiss. 46:23–30. Green, R. E. 1983. Spring dispersal and agonistic behaviour of the red-legged partridge (Alectoris rufa). J. Zool. 201:541–555. Griffin, A. S., D. T. Blumstein, and C. S. Evans. 2000. Training captive-bred or translocated animals to avoid predators. Conserv. Biol. 14:1317–1326. Gyer, M., S. Marakashian, and P. Marler. 1986. Avian alarm calling: Is there an audience effect? Anim. Behav. 34:1570–1572.
1907
Hooge, P. N., and B. Eichenlaub. 1997. Animal movement extension to Arcview. Version 1.1. Alaska Biological Science Center, United States Geological Survey, Anchorage, AK. Kaplan, E. L., and P. Meier. 1958. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53:457–481. Larsen, R. T., D. F. Bentley, and J. T. Flinders. 2008. Implications of woodrats and other scavengers for avian telemetry studies. J. Wildlife Manage. 72:1152–1155. Leopold, A., O. S. Lee, and H. G. Anderson. 1938. Wisconsin pheasant movement study, 1936–37. J. Wildl. Manage. 2:3–12. Mathews, F., M. Orros, G. McLaren, M. Gelling, and R. Foster. 2005. Keeping fit on the ark: Assessing the suitability of captivebred animals for release. Biol. Conserv. 121:569–577. McLean, I. G., C. Hölzer, and B. J. S. Studholme. 1999. Teaching predator recognition to a naive bird: Implications for management. Biol. Conserv. 87:123–130. Millán, J. 2009. Diseases of the red-legged partridge (Alectoris rufa L.): A review. Wildlife Biol. Pract. 5:70–88. Nicol, C. 2006. How animals learn from each other. Appl. Anim. Behav. Sci. 100:58–63. Oliveira, F., and R. J. Young. 2007. The behavioural responses of Nile tilapia (Oreochromis niloticus) to anti-predator training. Appl. Anim. Behav. Sci. 106:144–154. Palleroni, A., M. Hauser, and P. Marler. 2005. Do responses of galliform birds vary adaptively with predator size? Anim. Cogn. 8:200–210. Parish, D. M. B., and N. W. Sotherton. 2007. The fate of released captive-reared grey partridges Perdix perdix: Implications for reintroduction programmes. Wildlife Biol. 13:140–149. Pérez, J. A. 2006. Determinación de los principales parámetros ecoetológicos de la perdiz roja (A. rufa L.) y su aplicación a la evaluación de animales destinados a la repoblación. PhD Thesis. University of León, Spain. Pérez, J. A., M. E. Alonso, V. R. Gaudioso, J. A. Olmedo, C. Díez, and D. J. Bartolomé. 2004. Use of radiotracking techniques to study a summer repopulation with red-legged partridge (Alectoris rufa) chicks. Poult. Sci. 83:882–888. Pérez, J. A., M. E. Alonso, R. Prieto, D. J. Bartolomé, and V. R. Gaudioso. 2010. Influence of the breeding system on the escape response of red-legged partridges (Alectoris rufa). Poult. Sci. 89:5–12. Putaala, A. 1997. Survival and breeding success of wild and released grey partridges (Perdix perdix). PhD Thesis. Acta Universitatis Ouluensis, Oulu, Finland. Rantanen, E. M., F. Buner, P. Riordan, N. Sotherton, and D. W. Macdonald. 2010. Vigilance, time budgets and predation risk in reintroduced captive-bred grey partridges Perdix perdix. Appl. Anim. Behav. Sci. 127:43–50. Robinson, A. C., R. T. Larsen, J. T. Flinders, and D. L. Mitchell. 2009. Chukar seasonal survival and probable causes of mortality. J. Wildlife Manage. 73:89–97. Roseberry, J. L., D. L. Ellsworth, and W. D. Klimstra. 1987. Comparative post-release behaviour and survival of wild, semi-wild, and game farm bobwhites. Wildlife Soc. Bull. 15:449–455. Sánchez-García, C., M. E. Alonso, R. Prieto, V. González, and V. R. Gaudioso. 2009. Una visión sobre la avicultura para la producción de caza en España. ITEA-Animal. 105:169–183. Sanz-Zuasti, J., J. A. Arranz, and I. Molina. 2004. ZEPA OterosCampos (León). Pages 136–139 in La Red de Zonas de Especial Protección para las Aves (ZEPA) de Castilla y León. Junta de Castilla y León, Consejería de Medio Ambiente, Valladolid, Spain. Sherwin, C. M., S. B. Christiansen, I. J. H. Duncan, H. W. Erhard, D. C. Lay, J. A. Mench, C. E. O’Connor, and C. J. Petherick. 2003. Guidelines for the ethical use of animals in applied animal behaviour research. Appl. Anim. Behav. Sci. 81:291–305. Shier, D. M., and D. H. Owings. 2007. Effects of social learning on predator training and postrelease survival in the juvenile black-tailed prairie dogs (Cynomys ludovicianus). Anim. Behav. 73:567–577. Siegel, S., and N. J. Castellan. 1988. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York, NY.
1908
Gaudioso et al.
Sokos, C. K., P. K. Birtsas, and E. P. Tsachalidis. 2008. The aims of galliforms release and choice of techniques. Wildlife Biol. 14:412–422. Starling, A. E. 1991. Captive breeding and release. Ornis Scand. 22:255–257. Tejedor, M. T., L. V. Monteagudo, and M. V. Arruga. 2008. Microsatellite markers for the analysis of genetic variability and relatedness in red-legged partridge (A. rufa) farms in Spain. Res. Vet. Sci. 85:62–67. Tinbergen, N. 1957. On antipredator responses: A reply. J. Comp. Physiol. Psychol. 50:412–414. van Heezik, Y., P. J. Seddon, and R. F. Maloney. 1999. Helping reintroduced houbara bustards avoid predation: Effective anti-
predator training and the predictive value of pre-release behaviour. Anim. Conserv. 2:155–163. Vilhunen, S., H. Hirvonen, and M. V. M. Laakkonen. 2005. Less is more: Social learning of predator recognition requires a low demonstrator to observer ratio in Arctic charr (Salvelinus alpinus). Behav. Ecol. Sociobiol. 57:275–282. World Pheasant Association–IUCN. 2009. Guidelines for the Reintroduction of Galliformes for Conservation Purposes. World Pheasant Association, Newcastle-upon-Tyne, UK, and IUCN, Gland, Switzerland. Zaccaroni, M., M. Ciuffreda, M. Paganin, and L. Beani. 2007. Does an early aversive experience to humans modify antipredator behaviour in adult Rock partridges? Ethol. Ecol. Evol. 19:193–200.
