Bioacoustics of Canis aureus

ECOLOGY Population characteristics. —In Tanzania , densities up to 2 adults per km 2 may occur ( Moehlman 1983 , 1986 , 1989 ). In northern Dalmatia, Croatia , territory density was 0.61–1.15 groups per 10 km 2 ( Krofel 2008 ), whereas in southern Dalmatia density was 6–7 groups per 10 km 2 ( Krofel 2007 ). In Kenya , juveniles comprised 47% of captured Canis aureus ( Fuller et al. 1989 ) . In the Serengeti, maximum longevity is about 14 years (Moehlman and Hofer 1997). In captivity, individuals have lived up to 18 years 10 months (Weigl 2005). Sex ratio at approximately 3 weeks when pups emerge from the den is 1:0.8 ( n = 33), surviving at age 14 weeks (1:0.8, n = 44), helping as juveniles at approximately 52 weeks (1:1, n = 16), and reproductive adults (1:1, n = 46— Moehlman 1986 ). The sex ratio is equal for all age groups and sex ratio is equal for helpers. Space use. —Tolerance of dry habitats and an omnivorous diet allow Canis aureus access to a wide variety of habitats (Jhala and Moehlman 2008). They normally live in open grassland habitat but also occur in deserts, woodlands, mangroves, and agricultural and rural habitats in India and Bangladesh (Jhala and Moehlman 2008) In the Serengeti, C . aureus maintains year-round exclusive territories of 0.5–7.0 km 2 ( Moehlman 1983 ) and 2–5 km 2 in Ngorongoro (van Lawick and van Lawick-Goodall 1970), but will make excursions beyond these territorial boundaries to gain access to fresh carcasses. In Algeria , seasonal territories as may be as small as 0.39 km 2 ( Khidas 1990 ). Territories are within larger home ranges. Home range size of radiocollared individuals in some locales can vary according to habitat and age. An adult pair in Acacia woodland in Kenya had a home range of 2.4 km 2 and 2 juvenile females had home ranges of 5.6 and 21.7 km 2 ( Fuller et al. 1989 ), although range size over a 16-month period in the Bale Mountains of Ethiopia varied from 7.9 to 48.2 km 2 for adults and from 24.2 to 64.8 km 2 for subadults ( Admasu et al. 2004 ). Subadults may have larger home ranges as they explore and search for a mate and a territory. Home ranges of individuals within a social group tend to overlap (van Lawick and van Lawick-Goodall 1970; Khidas 1990 ; Admasu et al. 2004 ). In Bangladesh , breeding pairs defend an average of 37.3 ha of cover but not the peripheral foraging areas ( Jaeger et al. 1996 , 2007 ) and a male and female had home ranges of 1.1 and 0.6 km 2 , respectively ( Poché et al. 1987 ). In Israel , home and core ranges (km 2 ) of C. aureus near villages were about one-third of those in more natural areas (mean, SD ): home, 6.6 (4.5) versus 21.2 (9.3); core, 1.2 (0.9) versus 3.5 (1.6— Rotem et al. 2011 ). In the Serengeti, territories are maintained for up to 8 years albeit with changes in boundaries and size through time. Both members of the pair mark and defend the territory ( Moehlman 1986 ). Diet. —In Bangladesh , rodents are the most common food ( Jaeger et al. 2007 ). Similarly, in Bulgaria , rodents comprise 59.3% of the diet with brown hares ( Lepus europaeus , 20.1%) and plants (primarily fruit, 19.7%) as the next most common components (Markov and Lanszki 2012). In Rajasthan , India , rodents make up 45% of the diet ( Mukherjee et al. 2004 ). In Algeria , mammals comprise about a one-third of the diet with 17–24% poultry and 12–27% insects depending on location ( Amroun et al. 2006 ). In Israel , domestic carrion may form a significant component of the diet along with fruit, birds, small mammals, and invertebrates ( Borkowski et al. 2011 ). In Bangladesh , 12 stomachs contained primarily carrion, poultry, and vegetation but no rodents ( Poché et al. 1987 ). Single C . aureus typically hunt smaller prey like rodents and birds, using their hearing to locate rodents in the grass and then pouncing on them by leaping through the air, or digging out rodents from their burrows. However, single animals will also hunt Thomson’s gazelle ( Eudorcas tomsonii ) fawns. They have been observed to hunt young, old, and infirm ungulates that are sometimes 4–5 times their body weight (van Lawick and van Lawick-Goodall 1970; Eisenberg and Lockhart 1972). C . aureus in Bale, Ethiopia , may be more solitary than elsewhere in the range, with individuals having been observed foraging alone on 87% of occasions ( Admasu et al. 2004 ). This is likely because food resources were widely dispersed and rarely concentrated enough for jackals to forage in groups ( Admasu et al. 2004 ). In the Serengeti, mated pairs will hunt cooperatively and regularly kill Thomson Gazelle fawns and occasionally adults; pairs have a higher kill rate than individuals (Wyman 1967; Kruuk 1972 ; Rosevear 1974 ). Cooperative hunting permits them to harvest much larger prey in areas where they are available Temu et al. 2017. In the Ngorongoro Crater, C. aureus pairs cooperatively killed Thomson’s gazelle fawns and occasionally killed adult Thomson’s gazelle. Individuals successfully hunted Abdim’s storks ( Ciconia abdimii ) and during Wildebeest calving season consumed the abundantly available placentas. There was one observation of C. aureus cooperatively killing and eating a bat-eared fox ( Otocyon megalotis ) (Temu et al. 2017). Golden jackals consumed significantly more grams of food per hour of foraging when compared with sympatric Silver-backed jackals (Temu et al. 2016). In some areas, particularly where food resources are clumped, aggregations of C . aureus may occur, such as 14 jackals on a carcass in Ngorongoro (van Lawick and van Lawick-Goodall 1970) and aggregations of 5–18 jackals scavenging on carcasses of large ungulates in India (Y. V. Jhala, in litt.). C. aureus will cache excess food (van Lawick and van Lawick-Goodall 1970). In India , they will kill poultry as well as young and weak sheep and goats (Jhala and Moehlman 2004), and will venture into human habitation at night to feed on garbage ( Poché et al. 1987 ). In the Golan Heights, 1.5–1.9% of domestic calves are killed by predators, primarily C . aureus (Yom-Tov et al. 1995) . In the Serengeti, C . aureus scavenges the kills of spotted hyenas ( Crocuta crocuta ) and lions ( Panthera leo ) and leopards ( Panthera pardus —van Lawick and van Lawick-Goodall 1970; Moehlman 1986 ). In the Serengeti during the dry season, C . aureus does not have access to free standing water and can tolerate dry habitats (Moehlman and Jhala 2013). Diseases and parasites. —In the Serengeti, blood of 2 Canis aureus males was negative for leptospirosis, canine distemper, canine brucellosis, rabies, rinderpest, African horse sickness, and rift valley fever. Both individuals had titers for canine adenovirus and canine coronavirus. The older male was positive for canine parvovirus (Karesh 1990 in litt.). In 1994 during an outbreak of distemper, one C . aureus tested positive for canine distemper virus (Roelke- Parker et al. 1996 ). In 2011, samples collected from C . aureus pups were positive for canine distemper virus, but only 1 death was observed (Olarte-Castillo et al. 2015). In Kenya (1987–1988) testing for canine parvovirus (CPV-2), canine distemper virus, Ehrlichia canis , and rabies indicated that 9 of 16 individuals were positive for CPV-2; all were negative for canine distemper virus, E. canis , and rabies ( Alexander et al. 1994 ). In Israel , a serological survey indicated the presence of canine distemper virus, E. canis , and Leshimania infantum. Blood smears in one individual revealed Hepatazoon canis ( Shamir et al. 2001 ) . Leshimania tropica is also known from Israeli jackals (Talmi-Frank et al. 2010). Six of 8 C . aureus were positive for Toxoplasmosis gondii in the United Arab Emirates ( Dubey et al. 2010 ). Canis aureus in Serbia had an infection rate of 46 out of 447 jackals (10.3%) of at least one helminth species and in total 12 species were identified: 2 trematodes, Alaria alata and Pseudamphistomum truncatum , 3 nematodes, Toxocara canis , Ancylostoma caninum , and Gongylonema , and 7 cestodes, Taenia pisiformis , Taenia hydatigena , Multiceps multiceps , Multiceps serialis , Mesocestoides lineatus , Macrocanthorynchus hirudinaceus , and Onicola canis ( Ćirović et al. 2015 ) . In Israel , fecal samples had A. caninum and Dipylidium caninum ( Shamir et al. 2001 ) . In Tanzania , fecal samples from C . aureus had Coccida , Ancyclostoma , Psoroptes , and T. canis (W. B. Karesh, in litt.). In Rumania , the roundworm, Trichinella britovi occurs in C . aureus ( Blaga et al. 2008 ) . In Uzbekistan and Turkmenistan , the Ministries of Health ( Berdyeva 1998 ; L. M. Isaev Institute of Medical Parasitology 1998 ) reported that C . aureus may be infected with the guinea worm, Dracunculiasis medinensis ; thus, C . aureus potentially can infect water sources. In Italy , a subadult male had 2 ectoparasitic species, Dermacentor reticulatus , Isodes ricinus , and 1 endoparasitic species, Metagonimus yokogawai ( Lapini et al. 2009 ) . One C . aureus from Tunisia had 72 tapeworms, Echinococcus granulosus while 4 others had fecal evidence of the species ( Lahmar et al. 2009 ). The protozoan, Babesia gibsoni , may use C. aureus as a host ( Patton 1910 ). Interspecific interactions. —In East Africa, Canis aureus is sympatric with C. mesomelas and C. adustus . Skull characters indicate that C . aureus are more carnivorous than C. adustus and less carnivorous than C. mesomelas (van Valkenburgh and Wayne 1994) . In Hungary , dietary overlap between sympatric C . aureus and red foxes ( Vulpes vulpes ) is high at 73% as both primarily eat small mammals < 50 g ( Lanszki et al. 2006 ). In East Africa, spotted hyenas will kill and feed on C . aureus ( Kruuk 1972 ; Kingdon 1977 ). In the Serengeti, C . aureus give a “warning yowl” when spotted hyenas approach their dens. The adult jackals then chase the hyenas and bite them on the rump or genitals. Honey badgers ( Mellivora capensis ) have been observed near C . aureus dens, but have always been chased away by the parents and helpers. In India , striped hyenas ( Hyaena hyaena ) may prey on C . aureus (Y. V. Jhala, in litt.) and pythons ( Python molurus ) can be major predators ( Singh 1983 ). In India , when C . aureus approaches human habitation it may be killed by feral domestic dogs and death due to road kills increased during its breeding season (Y. V. Jhala, in litt.). C . aureus may be killed as a side effect of predator control programs when it scavenges poisoned carcasses (Moehlman and Jhala 2013). Miscellaneous. —Capture methods include rubber-padded, steel, foot-hold traps, cage-type live traps, large box traps, and Victor steel traps with off-set jaws ( Poché et al. 1987 ; Fuller et al. 1989 ; Admasu et al. 2004 ; Rotem et al. 2011 ). Differences in white markings on throat and chest may allow individual identification ( Macdonald 1979 ). Unique facial scars and naturally notched ears can be used to identify individuals ( Moehlman 1983 , 1986 ). HUSBANDRY As of March 2000 , approximately 193 Canis aureus were in Indian zoos (Jhala and Moehlman 2004). C . aureus have been raised in captivity for behavioral studies ( Seitz 1959 ; Wandry 1975). Individuals were housed in a kennel of 225 m 2 which included 5 separate and interconnected areas/cages. Each cage had a large box with a tunnel-like entrance (Wandry 1975). BEHAVIOR Grouping behavior. — Canis aureus are typically monogamous but can potentially be socially flexible depending on demography and food resources ( Macdonald 1979 ; Moehlman 1983, 1986 , 1989 ; Fuller et al. 1989 ; Moehlman and Hofer 1997; Admasu et al. 2004 ). The basic social unit is the breeding pair and some offspring from the previous year’s litter may remain with the parents and help to raise the current littler of pups ( Moehlman 1983 , 1986 , 1989 ). In Tanzania , C . aureus usually form long-term pair bonds which can last for up to 6 years. The bonded pair is territorial and both male and female mark within and on the boundaries of their territory and defend their territories against intruders. Same sex aggression is the norm with the territorial male attacking intruding males and females attacking intruding females. The pair hunt together, share food, and cooperatively rear their young ( Moehlman 1983 , 1986 , 1989 ). Moehlman and Hofer (1997) give average group size as 2.5 (Serengeti, Tanzania ), similar to average group size (3; n = 7) in Velavadar N. P., India (Y. V. Jhala, in litt.). Reproductive behavior. — Canis aureus has a strong pair bond which normally lasts for its lifetime ( Moehlman 1983 , 1986 , 1989 ). Mating involves a copulatory tie that lasts for several minutes (Golani and Mendelssohn 1971; Golani and Keller 1975). Pups are born in an underground den and normally emerge at about 3 weeks of age. Once pups emerge from the den they are fed solid food by adults regurgitating to them in addition to nursing. The origin of the dens can vary. Some authors (e.g., Rosevear 1974 ) report the use of existing aardvark Oryceropus afer or warthog Phacochoerus burrows, but in the Serengeti this is unlikely as C . aureus den openings are too small for either of these species (Jhala and Moehlman 2004). Earthen dens may have 1–3 openings and are typically about 2–3 m long and 0.5–1 m deep (Jhala and Moehlman 2004). Pups may be moved to different dens 2–4 times during their first 14 weeks of development ( Moehlman 1983 , 1986 , 1989 ). In Tanzania , C . aureus typically produces litters once a year during the wet season (December to February) when the large migratory herds of wildebeest ( Connochaetes taurinus ), zebra ( Equus burchelli ), and Thomson’s gazelles are present on the short-grass plains ( Maddock 1979 ). Thus, when C . aureus has pups, food items ranging in size from dung beetles to Thomson’s gazelle fawns are abundant. C . aureus also scavenges at carcasses of wildebeest and zebra that are killed by larger predators, mainly spotted hyenas (van Lawick and van Lawick-Goodall 1970; Moehlman 1983 , 1986 ). In the Serengeti since mated pairs are monogamous with long-term bonds, sequential litters are full siblings as confirmed by genetic analysis of microsatellite DNA (P. D. Moehlman, in litt.). The male provisions the female while she is pregnant and both the male and the helpers (the previous years pups) provide the female with food while she is lactating ( Moehlman 1983 , 1986 , 1989 ; Moehlman and Hofer 1997). The presence of helpers correlates significantly with a higher pup survival (Macdonald and Moehlman 1983 ; Moehlman 1986 , 1989 ). Communication. —Territories are maintained indirectly by scent marking and vocalizations. Both members of a pair use a raised-leg urination posture to scent mark grass tufts, bushes, and trees at nose height. Urination with a raised rear leg instead of squatting is considered to be a ‘marking posture’ and indicates that the individual is a territory holder and on its territory. Marking, for example “raised-leg” urinations indicate that an individual is a territory holder and on its territory. When a territorial male or female leaves their area they do not “mark.” Both the boundary and the area within a territory are “marked.” When foraging with their mate, territorial individuals mark at twice the frequency as when they are foraging alone. When travelling together they mark the same spot in tandem ( Moehlman 1983 , 1986 ). The presence of scent from both members of the pair may advertise to potential intruders that they are both actively in residence ( Moehlman 1983 ). Such scent marks are considered to play an important role in territorial defense ( Rosevear 1974 ). Affiliative behaviors like greeting ceremonies, grooming, and group vocalizations are common in C . aureus social interactions (Van Lawick and van Lawick-Goodall 1970; Golani and Keller 1975). Vocalization consists of a complex howl repertoire beginning with 2–3 simple low-pitch howls and culminating in a high-pitched staccato of calls. In the Serengeti, individuals give reciprocal howls to locate their mates and family members. Families also occasionally group howl in response to neighboring family howls ( Moehlman 1983 ). Similar functions accrue to howling in Bangladesh , for territory maintenance and advertisement of dominance ( Jaeger et al. 1996 ). C . aureus has a “rumble growl” and “predator bark” when potential predators like spotted hyenas approach a den with pups. Pups respond to these vocalizations by running into the den ( Moehlman 1983 ). Miscellaneous behavior. —In Kenya , Canis aureus was active during the day, as well as at dawn and dusk but not in the middle of the night ( Fuller et al. 1989 ). In Bangladesh , it preferred the cover of sugarcane during the day ( Jaeger et al. 2007 ).