Hinton Et Al. 2015

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Effects of anthropogenic mortality on Critically Endangered red wolf Canis rufus breeding pairs: implications for red wolf recovery

J OSEPH W. HINTON,KRISTIN E. BRZESKI D AVID R. RABON J R and M ICHAEL J. CHAMBERLAIN

Abstract Following precipitous population declines as a re- geographical ranges by anthropogenic mortality (Linnell sult of intensive hunting and th century predator-control et al., ; Cardillo et al., ; Ripple et al., ). Large programmes, hybridization of the Critically Endangered red carnivores may be at greater risk of extinction globally com- wolf Canis rufus with coyotes Canis latrans posed a signifi- pared to other groups of mammals because of inherent eco- cant challenge for red wolf recovery efforts. Anthropogenic logical characteristics such as large body size, reliance on mortality and hybridization continue to pose challenges; the large prey, social organization and restricted geographical increasing number of wolf deaths caused by humans has ranges (Purvis et al., ; Cardillo et al., ). Although limited wolf population growth, facilitated the encroach- large carnivores share similar ecological characteristics that ment of coyotes into eastern North Carolina, and affected may put them at risk, factors that affect carnivore popula- the formation and disbandment of breeding pairs. We as- tions at local and regional scales can vary significantly sessed the effects of anthropogenic mortality on Canis (Purvis et al., ; Ferguson & Larivière, ). As a result, breeding units during a -year period (–). Our re- conservation strategies developed to reduce anthropogenic sults show that deaths caused by people accounted for .% pressure on populations of large carnivores vary among re- of breeding pair disbandment, and gunshots were the pri- gions, reflecting diverse challenges to protecting and enhan- mary cause of mortality. Red wolves replaced congeneric cing threatened populations; for example, in South Africa breeding pairs . % of the time when pairs disbanded conservation fences are used to protect lions Panthera leo under natural conditions or as a result of management ac- from persecution and anthropogenic habitat degradation tions. Since the mid s anthropogenic mortality has (Hayward et al., ), and in the United States, Texas cou- caused annual preservation rates of red wolf breeding gars Puma concolor were introduced into south-west Florida pairs to decline by %, and replacement of Canis breeders to assist in genetic restoration of the endangered Florida by red wolves to decline by %. Our results demonstrate panther Puma concolor coryi population (Hedrick, ; that human-caused mortality, specifically by gunshots, Johnson et al., ). These examples demonstrate the im- had a strong negative effect on the longevity of red wolf portance of developing unique conservation strategies to ad- pairs, which may benefit coyotes indirectly by removing dress key threats to large carnivores. their primary competitor. Coyotes are exacerbating the de- In the eastern United States proactive conservation ac- cline of red wolves by pair-bonding with resident wolves tions were necessary to prevent extinction of the Critically whose mates have been killed. Endangered red wolf Canis rufus (Kelly et al., ; IUCN, ), which had been reduced to a single small, iso- Keywords Canis latrans, Canis rufus, conservation, coyote, lated population as a result of predator-control programmes group living, management, mortality, red wolf and excessive hunting. The last known red wolf population was intentionally extirpated from the wild in the sby the United States Fish and Wildlife Service (USFWS) Introduction when recovery in situ was deemed unlikely because of persecution, disease, poor habitat and hybridization with coy- ince the late th century populations of large carnivores otes Canis latrans (USFWS, ; Hinton et al., ). have been suppressed or extirpated throughout their S During the late s red wolves were reintroduced into eastern North Carolina, and the population currently com-

JOSEPH W. HINTON (Corresponding author) and MICHAEL J. CHAMBERLAIN Warnell prises c.  individuals (USFWS, ). This represents the School of Forestry and Natural Resources, University of Georgia, Athens, first successful reintroduction of a large predator species Georgia 30621, USA. E-mail [email protected] that was completely extirpated from the wild. Restoration KRISTIN E. BRZESKI School of Renewable Natural Resources, Louisiana State of the red wolf also served as a model for subsequent rein- University Agricultural Center and Louisiana State University, Baton Rouge, Louisiana, USA troductions of the grey wolf Canis lupus to the Southwest  DAVID R. RABON,JR Endangered Wolf Center, Eureka, Missouri, USA and Greater Yellowstone Ecosystem (Phillips et al., ). Received  February . Revision requested  May . Red wolf recovery efforts in eastern North Carolina have Accepted  June . occurred in the presence of two factors that facilitated the

species’ decline and extirpation from the wild during the late th century: hybridization with coyotes and anthropogenic mortality. After several hybridization events occurred during the mid s a population and habitat viability assessment was conducted to re-evaluate long-term management of red wolves and determine how to monitor hybridization effectively and limit it to acceptable levels (Kelly et al., ). A unique approach to limit hybridization was implemented whereby coyotes and hybrids were sterilized and used as placeholders on the landscape to suppress coyote reproduction and prevent coyotes that consort with red wolves from producing hybrids (Hinton et al., ; Gese & Terletzky, ). By capturing, sterilizing and then releasing coyotes and hybrids back into the wild, the USFWS’s Red Wolf Recovery Program (hereafter Recovery Program) could manipulate canid breeding pairs of non-red wolves to suppress hybrid- FIG. 1 The location of the Red Wolf Recovery Area in North ization and introgression. Carolina, USA. Although sterilization has been effective at limiting hy-  bridization and introgression to below % in the wild red caused by natural and anthropogenic factors. Our study  wolf population (Gese et al., ), management strategies provides insight into causes of disbandment of red wolf for the wild population were not designed to address exces- breeding pairs, the subsequent formation of new breeding sive anthropogenic mortality, and no social scientists were pairs, and the relationship between anthropogenic mortality assigned to the Red Wolf Implementation Team because so- and hybridization between red wolves and coyotes. cial and public relations issues were left to non-profit organizations (the Red Wolf Coalition) and the USFWS to address (Stoskopf et al., ). Red wolf deaths caused by Study area gunshot have increased c. % since , with most kill- ings occurring during the North Carolina autumn and win- The Red Wolf Recovery Area (hereafter Recovery Area) ter hunting seasons (Bartel & Rabon, ). Anthropogenic consists of five counties (Beaufort, Dare, Hyde, Tyrrell mortalities complicate management of Canis breeding units and Washington) on the Albemarle Peninsula of eastern  by disrupting resident breeding pairs and facilitating high North Carolina (Fig. ). The study area encompasses    turnover of territories; research suggests that anthropogenic c. , km of federal, state and private lands consisting – mortality of both red wolves and eastern wolves Canis ly- primarily of an agricultural coastal bottomland matrix. caon facilitates hybridization with coyotes by disrupting Agricultural crops (i.e. corn, cotton, soybean and winter  the population’s social structure (Rutledge et al., ; wheat) and managed pine Pinus spp. account for c. and  Bohling & Waits, ). Anthropogenic mortality was also % of the land cover, respectively, and coastal bottomland  found to have a negative effect on the annual preservation forests and pocosin habitats account for c. %. The climate of red wolf breeding pairs (Sparkman et al., ). Bohling is typical of the mid-Atlantic: four distinct seasons, nearly  –  & Waits () assessed  hybridization events between equal in length, with annual precipitation of , , red wolves and coyotes, and reported that red wolves in- mm. Summers are typically hot and humid, with daily tem- – volved in hybridization were displaced from packs disrupted peratures of °C, and winters are relatively cool, with −– by anthropogenic mortality among the breeders. To further daily temperatures of °C. assess the effects of anthropogenic mortality on red wolf breeding units and successful management of red wolves, Methods we evaluated the management and fate of Canis breeding  pairs during a -year period. Specifically, we identified Field data collection the primary causes of disbandment and described how anthropogenic mortality disrupts breeding units and territor- As part of the Recovery Program’s long-term monitoring ial behaviour, and hinders conservation strategies designed and management, trapping was carried out annually during to facilitate red wolf recovery. Our primary objective was to autumn and winter to capture red wolves, coyotes and hy- identify processes responsible for disbandment of red wolf brids, and fit them with mortality-sensitive VHF radio col- breeding pairs and sterile placeholders. We also investigated lars (Teleonics, Mesa, USA). Collared individuals were if red wolves were replacing lost wolf breeders and sterile monitored twice per week from aircraft for the duration of placeholders on the landscape following disbandment their life. The canids were captured using padded foot-hold

http://journals.cambridge.org Downloaded: 14 Oct 2015 IP address: 70.193.133.148 Anthropogenic mortality of the red wolf 3 traps (Victor no. Softcatch, Woodstream Corporation, Data analyses Lititz, USA), and coyotes and hybrids were taken to a local veterinary clinic and surgically sterilized by vasecto- We divided the study period into three phases: I (–), mies and tubal ligations (Gese & Terletzky, ). This pro- II (–) and III (–). Phase I represents when cess keeps hormonal systems intact to avoid disrupting the USFWS originally focused efforts to establish a wild red breeding and territorial behaviour (Seidler & Gese, ). wolf population (Phillips et al., ). Phase II represents Resident breeding pairs were identified as radio-collared when the USFWS adopted and implemented an adaptive individuals of breeding age ($  years old) who were tem- management plan to detect, monitor and manage hybrid- porally and spatially associated with one another and had ization as the Recovery Area was colonized by coyotes been defending a territory for $  months. Biologists con- (Stoskopf et al., ). Phase III represents when the firmed breeding pair status during spring den work (March– USFWS reported stagnant population growth and increased May) by locating dens and daybeds of females to verify the rates of red wolf mortality as a result of anthropogenic presence of litters for each radio-collared breeding pair dur- causes (USFWS, ; Bartel & Rabon, ). ing –. After , dens were investigated more thor- We used trapping data to estimate relative abundances of oughly; biologists sampled blood from pups each spring to red wolves, coyotes and their hybrids and to evaluate their verify parentage and construct a red wolf pedigree (Miller ratio before and after breeding pairs disbanded, by calculat- et al., ; Beck et al., ; Brzeski et al., ). We used ing the number of red wolves, coyotes and hybrids captured the red wolf population pedigree in combination with a com- each year. We analysed  years (–) of trapping data plete set of chronological and geographical data of Canis compiled by the Recovery Program, to calculate annual ra- breeding pairs in the Recovery Area to identify when breed- tios of red wolf to coyote and red wolf to hybrid. Most trap- ing pairs formed and disbanded. Red wolves paired with a ping was conducted in known and suspected territories of sterilized non-wolf mate were confirmed as congeneric red wolf breeding pairs, to capture and fit pups with radio breeding pairs through field data and occasionally by den collars or to target coyotes or hybrids suspected of pair- work if the non-wolf mate had not been sterilized. We de- bonding with red wolves. However, trapping also focused fined two types of breeding pairs: red wolf (two red wolves) on capturing resident coyotes and hybrids to use as place- and congeneric (red wolf with a coyote or a hybrid). holders and, to a lesser extent, to address complaints from Causes of breeding pair break-ups were categorized as the public regarding the presence of red wolves and coyotes natural causes (i.e. disease, intraspecific strife, malnutri- on private lands. Recovery Program biologists also coordi- tion), management actions (i.e. removal of coyote or hybrid nated with private fur trappers to opportunistically capture from congeneric pairs), anthropogenic (i.e. poison, trap- red wolves, coyotes and hybrids throughout the Albemarle ping, suspected or confirmed gunshot, vehicle collision), Peninsula. Although trapping was used to accomplish mul- or unknown. We separated management actions from an- tiple objectives and could not be standardized temporally or thropogenic causes because break-ups of breeding pairs spatially, we believe trapping efforts that were part of the through management are fundamentally different from large-scale, long-term monitoring efforts conducted across break-ups caused by other human activities, such as illegal the five-county Recovery Area provided the only reasonable and incidental killing. Attempts to remove coyotes from proxy for abundances of Canis species in eastern North congeneric pairs represent efforts to free individual red Carolina (Keane et al., ; Stephens et al., ). We wolves as potential mates for dispersing wolves and can be used ANOVA to determine differences in the numbers of eliminated by cessation of management protocols, whereas red wolves, coyotes and hybrids captured during each of illegal and incidental killing are indiscriminate and more the three phases and to determine variations in ratios difficult to eliminate. Causes of mortalities were categorized of red wolf to coyote and red wolf to hybrid during each as unknown in several situations: () there was not enough of the three phases. We used linear regression to assess if biomaterial present to determine the cause of death (e.g. these ratios were correlated with the percentage of breeders skeletal remains, hair mat only), () necropsy analyses lost to anthropogenic mortality. were inconclusive, or () multiple causes of death were sus- We calculated several metrics of pair preservation, re- pected in pending cases and were confirmed by necropsy. placement and disbandment to evaluate how Canis breeding Mortalities caused by management-related activities in- pairs changed during each phase. Because we categorized cluded deaths resulting from capture and handling and re- canids that were temporally and spatially associated with a actions to medical treatments. Mortalities caused by potential mate for $  months as breeding pairs, we calcu- gunshot included cases where foul play was suspected (e.g. lated duration of Canis breeding pairs in half-year incre- a cut or removed radio collar, bullet wounds), and con- ments. The annual preservation rate of Canis breeding firmed cases where x-rays or necropsy examinations yielded pairs was calculated as the number of Canis breeding pairs evidence of bullet fragments. Instances of poisoning were preserved (maintained from the previous year) divided by confirmed by necropsy and toxicological analysis. the total number of Canis breeding pairs present in a

TABLE 1 Numbers and ratios of red wolves Canis rufus, coyotes Canis latrans and hybrids captured in eastern North Carolina during –.

Total no. of canids Ratio of red wolf Ratio of red wolf captured No. of red wolves No. of coyotes No. of hybrids to coyote, to hybrid, Phase (mean ± SE) (mean ± SE) (mean ± SE) (mean ± SE) mean ± SE mean ± SE Phase I 193 (24.5 ± 3.7) 141 (17.6 ± 2.7) 26 (3.3 ± 4.0) 26 (3.3 ± 1.7) 7.1 ± 0.9 11.7 ± 2.5 (1991–1998) Phase II 327 (46.7 ± 5.3) 185 (26.4 ± 2.9) 47 (6.7 ± 4.3) 95 (13.6 ± 1.8) 4.0 ± 1.0 2.3 ± 2.6 (1999–2005) Phase III 624 (78.0 ± 6.1) 184 (23.0 ± 2.7) 343 (42.9 ± 4.0) 97 (12.1 ± 1.7) 0.71 ± 0.9 2.1 ± 2.5 (2006–2013)

given year. We calculated annual replacement rates of red wolves as the number of Canis breeding pairs disbanded (not maintained from the previous year) and replaced by red wolves divided by the total number of Canis breeding pairs disbanded for each given year. We calculated annual disbandment rate as the number of Canis breeding pairs disbanded as a result of anthropogenic causes divided by the total number of Canis breeding pairs disbanded in a given year. Because annual preservation replacement and dis- placement rates were reported as proportion data, we logit transformed these variables for analyses (Warton & Hui, ). FIG. 2 Number of red wolf Canis rufus and congeneric Canis We used linear regression to assess increasing or decreas- breeding pairs monitored in the Red Wolf Recovery Area (Fig. ) ing trends in annual preservation replacement and displace- during –. In Phase I (–) the U.S. Fish and ment rates of Canis breeding pairs. We also used ANOVA to Wildlife Service focused efforts to establish a wild red wolf determine variation among these rates across the three population, in Phase II (–) they focused efforts to phases. We described the primary causes of break-up of detect, monitor and manage hybridization in the Recovery Area, – Canis breeding pairs using contingency tables to compare and in Phase III ( ) they reported increasing rates of observed frequencies of breeding pair disbandment to ex- red wolf mortality as a result of anthropogenic causes. pected frequencies for each of the four primary causes of and Phase II, whereas ratios of red wolf to hybrid were simi- disbandment. We also used contingency tables to determine lar between Phase II and III but significantly higher during if disbanded Canis breeding pairs were replaced more often Phase I (Table ; F  = .,P=.). than expected by a red wolf or congeneric breeding pair. , During – we identified  Canis breeding pairs: Similarly, we assessed whether the mate of a disbanded  red wolf (.%) and  congeneric (.%) pairs breeding pair accepted a red wolf or coyote as a new mate (Fig. ). The percentage of Canis breeding pairs disbanded more often than expected. We defined acceptance of a by anthropogenic mortality increased during this period new mate as when individual canids from disbanded breed-  (R = .,P. .) and the annual preservation rates of ing pairs were observed to be temporally and spatially asso- Canis breeding pairs declined steadily (F  = ., ciated with a new canid for $  months. , P=.). The annual replacement rates of Canis breeding pairs by red wolves were lowest during Phase III     Results (F, = . ,P= . ), whereas the annual rates of disbandment from anthropogenic causes were highest during –        During , canids were captured: red wolves Phase III (F, = . ,P= . ). Ratios of red wolf to coy- (.%),  coyotes (.%) and  genetically identified ote were negatively correlated with anthropogenic disband-  hybrids (.%). Captures of red wolves did not vary across ment (Fig. ; R = .,P, .), and were lowest during      the three phases (Table ; F, = . ,P= . ), whereas Phase III, when breeder loss as a result of anthropogenic coyote captures were highest during Phase III mortality was highest (Table ). We observed no correlation   ,   (F, = . ,P . ) and hybrid captures were lowest between human-caused disbandment and observed ratios of    ,        during Phase I (Table ; F, = . ,P . ). Ratios of red wolf to hybrid (R = . ,P= . ). red wolf to coyote declined from Phase I to Phase III Mortality, pooled across all causes, was responsible for   ,     (F, = . ,P . ) but were similar between Phase I most disbandment in Canis breeding pairs ( . %).

http://journals.cambridge.org Downloaded: 14 Oct 2015 IP address: 70.193.133.148 Anthropogenic mortality of the red wolf 5

    F, = . ,P=. ) but the duration of congeneric breeding pairs declined steadily (x = . ± SE ., . ± SE . and . ± SE . years in Phases I, II and III, respectively;     F, = . P= . ). Overall, the duration of red wolf breeding pairs was longer than that of congeneric pairs (x =   ±     ±       . SE . vs x = . . years; F, = . ,P= . ).

Discussion

Early in red wolf recovery efforts, when there were fewer coyotes and anthropogenic mortalities, wolves replaced wolf breeders. However, since the early s the coyote population and the number of red wolf mortalities caused FIG. 3 Annual ratios of red wolves to coyotes Canis latrans by gunshots have increased, with coyotes typically replacing among canids captured by the Red Wolf Recovery Program regressed against the annual percentage of Canis breeding pairs red wolves following deaths caused by humans, specifically disbanded because of anthropogenic mortality in eastern North those caused by gunshot. Coyote populations have increased Carolina (Fig. ) during –. in North Carolina (DeBow et al., ) and the Recovery Area, which is evident from our trapping data: the number of coyote captures was highest during –. Since the Primary causes of mortality responsible for disbandment of mid s the North Carolina Wildlife Resources Canis breeders corresponded with those reported to affect Commission has increased opportunities for coyote hunting red wolf survival (J.W. Hinton et al., unpubl. data). in an attempt to reduce the abundance of coyotes. However, Anthropogenic causes accounted for .% of deaths, red wolves are often mistaken for coyotes by hunters, and, whereas natural causes and management actions accounted by proxy, are subject to excessive hunting pressure; this for . and .%, respectively. Mortalities caused by gun- trend is evident from the fact that most gunshot mortalities shots were responsible for .% of disbandment as a result occur during the autumn and winter hunting season ( of anthropogenic causes, and .% of all disbandment. In October– December; Bartel & Rabon, ). Since  comparison to red wolf breeding pairs, congeneric breeding there has been a significant increase in the break-up of red pairs were disrupted more by management actions (. vs wolf breeding pairs as a result of anthropogenic mortalities, .%) and less by natural (. vs .%) and anthropogenic in which gunshot mortalities were a primary reason for dis-     x2   ,   causes ( . vs . %; 3 = . ,P . ). Anthropogenic bandment, prevented long-term pairings and facilitated the and unknown causes of Canis breeding pair break-ups were increase in congeneric breeding pairs observed during  x2   ,   – highest in Phase III (Fig. ; 6 = . ,P . ). Assessing . Replacement by coyotes in red wolf breeding only red wolf breeding pairs across all Phases, anthropogenic pairs disbanded as a result of gunshot mortalities has in- causes of break-ups increased (., . and .%during creased significantly since the early s. This pattern x2   ,   Phase I, II and III, respectively; 6 = . ,P . ). has profound effects on red wolf demography and popula- Similarly, anthropogenic causes in congeneric pair disband- tion increase because each breeding pair disbanded repre- ment increased across all Phases (, . and .% during sents a lost reproductive opportunity. This loss is x2     Phase I, II and III, respectively; 6 = . ,P=. ). compounded by an increase in coyotes replacing disbanded Overall, red wolves were more likely to replace Canis breed- pairs, further reducing the ability of surviving wolves to find ing pairs when disbandment was caused by natural causes conspecific mates. Similarly to red wolf breeding pairs, con-  x2     and management actions (Table ; 4 = . ,P= . ). generic breeding pairs containing sterile placeholders were Overall, the percentage of red wolf breeding pairs vs con- also disbanded at higher rates as a result of anthropogenic generic breeding pairs did not change among phases (., mortality. This trend is problematic for controlling hybrid-     x2   . and . % for Phase I, II and III, respectively; 2 = . , ization if sterile coyotes and hybrids paired with red wolves P=.). However, the percentage of congeneric breeding are killed and replaced by fertile coyotes. pairs including coyotes was highest during Phase III (., Rutledge et al. () reported that intense harvest out-     x2   . and . % for Phase I, II and III, respectively; 2 = . , side Algonquin Provincial Park disrupted pack structure P , .). Congeneric pairs typically contained more fe- and social patterns in which culling of eastern wolves during     x2    male than male red wolves ( . vs . %; 1 = . , the s was linked to past introgression from coyotes P , .). There was no variation observed in the duration within the Park (Rutledge et al., ). Benson et al. () of red wolf breeding pairs over time (x = . ± SE ., . ± SE also suggested that levels of harvest in areas adjacent to . and . ± SE . years in Phases I, II and III, respectively; Algonquin Provincial Park may influence hybridization

TABLE 2 Cause of break-up of Canis breeding pairs, with the number of break-ups attributed to each cause, and the percentage of pairs replaced by red wolves or coyotes/hybrids, or not replaced ,  months after breeding pairs disbanded in eastern North Carolina during –.

Cause of No. of % replaced % replaced % not replaced break-up break-ups by red wolves by coyotes within , 12 months Phase I (1991–1998) Anthropogenic 3 33.3 33.3 33.3 Management 5 60.0 0.0 40.0 Natural 17 37.5 12.5 50.0 Unknown 0 0.0 0.0 0.0 Phase II (1999–2005) Anthropogenic 12 41.7 41.7 16.6 Management 17 76.5 11.8 11.8 Natural 29 55.2 31.0 13.8 Unknown 3 33.3 33.3 33.3 Phase III (2006–2013) Anthropogenic 37 52.8 47.2 0.0 Management 11 72.7 27.3 0.0 Natural 28 71.4 25.0 3.6 Unknown 12 28.1 40.7 1.2

unpubl. data) and our findings indicate that the mean duration of red wolf breeding pairs is  years. The short duration of breeding pairs is a consequence of low life expectancy and prevents the long-term pairing required for developing the social structure and stability necessary to maintain pack dynamics. The average time for red wolves to replace lost mates is unknown, but selecting a new mate may occur over a period of several days to several months, as in other canids (Asa & Valdespino, ; Bekoff & Gese, ; Borg et al., ). When resident red wolves lose mates they permit transients of the opposite sex into their territories to facilitate selection of a new mate. The excessive turnover of Canis breeding pairs resulting from anthropo- FIG. 4 Percentage of Canis breeding pairs that were disbanded as a result of anthropogenic causes, management actions, natural genic mortality is likely to erode strong territorial behaviour causes, and unknown causes in eastern North Carolina (Fig. ) in both wolves and coyotes, and increases mate-selection be- during –. Phases represent changes in conservation haviours. This promotes coyote encroachment into areas strategies to mitigate environmental factors that affected red wolf where red wolf breeding pairs have been disbanded by an- recovery efforts in the wild population. The total number of thropogenic causes, facilitating an increase in congeneric    Canis breeding pairs was in Phase I, in Phase II, and in pairing between red wolves and coyotes. It may also create Phase III. opportunities for coyotes to outnumber red wolves and usurp their territories. dynamics between eastern wolves and coyotes. Similarly, Bohling & Waits () reported a strong bias of female Bohling & Waits () found that most hybridization red wolves producing hybrid litters but asserted that hybrid events in the Recovery Area occurred after red wolves lost litters were easier to find when they involved radio-collared mates to gunshots, and suggested that the disruption to female wolves rather than female coyotes and hybrids with- the wolves’ social structure and stability facilitated hybrid- out radio collars. Similarly, our results show that c. %of ization. Our results complement the findings of these stud- all congeneric breeding pairs included a female red wolf, and ies and offer unique insights regarding how Canis breeding we believe the greater occurrence of female wolves produ- pairs are affected by the anthropogenic factors responsible cing hybrid litters reported by Bohling & Waits ()was for disbandment. In addition to negatively affecting red not a result of monitoring bias. It appears female red wolves wolf survival, anthropogenic mortality disrupts pack dy- are more likely than males to form congeneric pairs and, as namics by reducing the mean life expectancy. The mean life- red wolf pairs and packs are disrupted by excessive an- span of a red wolf in the wild is . years (J.W. Hinton et al., thropogenic mortality, surviving female wolves pair-bond

http://journals.cambridge.org Downloaded: 14 Oct 2015 IP address: 70.193.133.148 Anthropogenic mortality of the red wolf 7 with encroaching coyotes when compatible wolf mates are Program, specifically A. Beyer, M. Butts, R. Harrison, unavailable. The loss of female red wolves to encroaching C. Lucash, F. Mauney, M. Morse and R. Nordsven. We coyotes is problematic because it disrupts wolf natality also thank J. Benson for comments on the manuscript. that is necessary to buffer the effects of mortality. Natality The findings and conclusions in this article are those of has the greatest influence on a population’s ability to in- the authors and do not necessarily represent the views crease (Vandermeer & Goldberg, ), and congeneric of the U.S. Fish and Wildlife Service. Any use of trade, prod- pairing disrupts the red wolf’s potential to compensate for uct or firm names is for descriptive purposes only and does the loss of breeders through reproduction. not imply endorsement. Current approaches to coyote management often focus on demographic consequences of population control methods, with little consideration of accidental or intentional killing of other Canis species. Previous hunting regulations References (no closed season, artificial lights permitted, and no bag lim-  its) increased the likelihood of red wolves being mistaken for ASA, C.S. & VALDESPINO,C.( ) Canid reproductive biology: an  integration of proximate mechanisms and ultimate causes. coyotes and shot by hunters. In a court-approved American Zoologist, , –. settlement between several conservation groups and the BARTEL, R.A. & RABON, D.R. () Re-introduction and recovery of North Carolina Wildlife Resources Commission banned the red wolf in the southeastern USA. In Global Re-introduction night-time hunting of coyotes, and permitting and report- Perspectives: . Further Case Studies from Around the Globe (ed. – ing are now required for coyote hunting during the day in P.S. Soorae), pp. . IUCN/SSC Reintroduction Specialist Group, Gland, Switzerland, and Environment Agency Abu Dhabi, the Recovery Area (Boyle, ). Regulating the take of coy- Abu Dhabi, UAE. otes will have considerable potential for reducing the effects BECK, K.B., LUCASH, C.F. & STOSKOPF, M.K. () Lack of impact of of incidental killing of red wolves. Nevertheless, the USFWS den interference on neonatal red wolves. Southeastern Naturalist, , is responsible for developing recovery plans to address key –. threats to the survival of threatened and endangered species BEKOFF,M.&GESE, E.M. () Coyote (Canis latrans). In Wild  (Hoekstra et al., ). Anthropogenic mortality and hy- Mammals of North America, nd edition (eds G.A. Feldhamer, B.C. Thompson & J.A. Chapman), pp. –. 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D AVID R ABON Chicago, USA. is a conservation biologist interested in the restoration and manage- PURVIS, A., GITTLEMAN, J.L., COWLISHAW,G.&MACE, G.M. () ment of threatened species, particularly wild canids and other carni- Predicting extinction risk in declining species. Proceedings of the vores. M ICHAEL C HAMBERLAIN conducts research on a variety of Royal Society B, , –. wildlife species, with a keen focus on canids.

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