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Dogs Are Charming and Cute, Professor John L. Hoogland But They Are Also Serial Killers

Adult Utah , which weighs about 800 grams. CREDIT: Elaine Miller Bond (www.elainemillerbond.com) Two Utah prairie dogs kissing early in the morning while scanning for predators. CREDIT: Elaine Miller Bond (www.elainemillerbond.com) ‘Long term research and careful analyses are crucial and decisive for understanding the and social behaviour of as complex as prairie dogs. I have been fortunate to spend a lifetime studying these captivating . Consequently, I have been able to make several riveting discoveries that have led to novel, far-reaching conclusions.’

PRAIRIE DOGS ARE CHARMING AND CUTE, BUT THEY ARE ALSO SERIAL KILLERS

When John Hoogland first visited a prairie dog colony as a young graduate student, he said aloud to himself, ‘I could study these animals for the next 10 years.’ Forty-four years later, John is still studying prairie dogs, and he still marvels about the sometimes bizarre, often provocative, and always fascinating lives of his favourite animals. He is the undisputed world’s CREDIT: Mariana Rivera Rodriguez expert on these remarkable social . John Hoogland reading the eartags of one of his Gunnison’s prairie dogs; note the canvas CREDIT: Elaine Miller Bond (www.elainemillerbond.com) bag used for handling. male attacking another male during the mating season.

Behavioural ecologist Professor John discovered that, contrary to popular belief parks in Arizona, Colorado, New Mexico, The alarm call in response to predators is finding and inseminating receptive females, several hours on a single day. And finally, Hoogland’s research career began with a at the time, Wyoming ground do , and Utah. And yet John still a pivotal reason for this increased safety. with little of predators. And for the 3rd most copulations occur underground! By deceptively simple question: Why do animals not actually live in discrete colonies. One says at every one of his lectures, ‘The more I But alarm calling is puzzling. Why should an and 4th weeks after they mate, females in watching marked individuals from dawn to live in colonies? To pursue the answer, he night John broke down and sobbed to his learn about prairie dogs, the less I know.’ individual draw a predator’s attention to itself late pregnancy are especially vulnerable – dusk every day, by watching for diagnostic turned to prairie dogs, which are diurnal, new bride (Judy) about his calamity. Judy by calling in order to save other prairie dogs because they are overweight with as many as aboveground behaviours just before and herbivorous, -like rodents that live instantly responded, ‘Why not study prairie John’s initial research focused on trying to with whom it competes? The payoff is that 8 large foetuses, and therefore unable to run just after an underground copulation, and in large colonies throughout the dogs? Everybody knows that prairie dogs figure out why prairie dogs live in colonies. alarm calls warn genetic relatives of danger. as fast as other prairie dogs. by collecting DNA-samples from all juveniles of western . These gregarious live in colonies.’ John listened, and visited a When compared with solitary prairie dogs, These calls warn nearby offspring for three of and all potential parents, John and his rodents, whom John frequently calls his colony of prairie dogs the next day. Within colony residents face higher competition for the prairie dog species that John has studied. Family Matters students are able to specify who mates ‘little people’, have afforded him unique a few minutes of his arrival, John was food, mates, and other resources, and they For the fourth species, individuals call not with whom for over 95% of females at their opportunities for his research over the last mesmerised by the nonstop vocalisations, also incur a higher risk for contracting nasty only for offspring, but also for more distant Family dynamics can be complicated when study-colony each year. By following parents four decades, with sweeping conclusions and by the chases, fights, and kisses that he diseases and parasites. kin such as nieces, nephews, and cousins. your entire extended family lives in a small and their offspring – for a minimum of 10 for not only prairie dogs, but also other was seeing everywhere. area, as occurs for all four species of prairie years for each of four species – John has social animals. But what are the compensating advantages of prairie dogs is rare, as just dogs that John has studied. One of his documented that prairie dogs consistently John quickly developed the simple protocol that over-ride these serious costs? John’s noted. When it occurs, John was expecting early objectives after graduate school was avoid incestuous matings with close kin Life in the Colony of ‘Catch ’em. Mark ’em. Watch ’em.’ He and early research showed that the major benefit that the old, the weak, and the sickly to figure out if prairie dogs are concerned such as parents, offspring, and siblings, even his students – usually 4–5 per year, with a to living in a colony for prairie dogs is the would be the most common victims. But about incest. The solution did not come though these genetic relatives frequently In April 1974, while working on a PhD at the grand total over 200 – took this protocol lower risk of being captured by a predator. the prairie dogs surprised him. He learned easily, because the mating season lasts for live in the same or adjacent territories. Such University of Michigan, John found himself in to a new level over the next 44 years: an ‘With so many individuals within a colony that the largest, most aggressive, and most only 3 weeks in late winter and early spring avoidance reduces the problem of inbreeding a devastating situation for a young graduate inconceivable >200,000 man-hours of watching for enemies, the probability that a successful males in one species are the most at high altitudes, where temperatures are depression (the reduction of survivorship of student. While attempting to study colony research with four different species of prairie bobcat, , or will be able susceptible to predation during the mating low and arctic winds are relentless. Further, inbred offspring). But prairie dogs frequently dynamics of Wyoming ground squirrels, he dogs under natural conditions at national to capture a prairie dog is low,’ John says. season – because they are so obsessed with each female is sexually receptive for only mate with more distant kin such as aunts

WWW.SCIENTIA.GLOBAL WWW.SCIENTIA.GLOBAL in the natal territory with other family for , and Swainson’s hawks. In a typical their entire lives. But why do a few females IK, the prairie dog repeatedly bites the disperse? John ignored this question for in the neck or thorax over a over 35 years, until Judy wanted to know period of 1–3 minutes until death, and then more about dispersing females. ‘It’s so rare, walks away with no consumption. Most it’s not worth further investigation,’ John killers (N = 28) slew a single ground squirrel, replied to his wife. But Judy would not let it but 19 serial killers slew two or more ground go. When John agreed, begrudgingly, to do squirrels. One female killed six ground an analysis for one species, he immediately squirrels over 5 years, another female killed realised that Judy’s persistent curiosity had nine over 4 years, and a third female killed led him to a stunning discovery: Females seven juveniles from the same litter in a only disperse when they have no surviving single day. John’s large sample size (N = 163 close kin in the home territory. When John IKs, over 6 years) allowed him to demonstrate did the same analysis for the other three that females that kill ground squirrels have prairie dog species, he found the same significantly higher annual and lifetime unexpected pattern. Indeed, females are reproductive success than nonkillers. These 12.5 times more likely to disperse in the differences in Darwinian fitness probably CREDIT: Elaine Miller Bond (www.elainemillerbond.com) CREDIT: Elaine Miller Bond (www.elainemillerbond.com) absence of mother and siblings for one result from lower interspecific competition species, and 5.5 times more likely for another with ground squirrels for vegetation following John Hoogland releasing a Utah prairie dog uniquely marked with three vertical stripes for Two Utah prairie dogs on the first day they appear aboveground at weaning, when they are about species. This striking pattern of dispersal IKs – so that killers and their offspring identification from as far away as 100 m. 5.5 weeks old and weigh about 200 grams. has previously been detected in only one consequently have more food. other species – even though dispersal is probably should be on that list as well. and uncles, nieces and nephews, and first offspring, for example, and this one of the most intensively studied topics Because IKs were so quick, subtle, and and second cousins. So they avoid extreme is the main cause of juvenile mortality in in all of ecology. For female prairie dogs, the unanticipated, John and his students John has documented that prairie dogs inbreeding (incest), but prairie dogs regularly most years. Lactating black-tailed prairie benefits of cooperating with family members studied white-tailed prairie dogs for 4 have a profound impact on their engage in moderate inbreeding. dog females are especially likely to kill, and (e.g. alarm calling, communal nursing) years before they detected the first case. , and are therefore keystone murdered most or all of the juveniles for evidently outweigh the costs of competing Their compelling results should help other species. For example, their change John’s careful observations of the prairie a whopping 65 of 294 litters (22%) under with the same family members (e.g. fighting, ecologists to realise that IKs might be the landscape and soil chemistry, affect the dog mating system have provided insights surveillance by John and his students over infanticide). So females stay home and happening frequently but surreptitiously, and cycling of water and nutrients, alter floral for another conundrum first recognised several years. These 65 mass killings involved rarely disperse. And for John, the benefits of with significant consequences for Darwinian species composition, and provide shelter and by Charles Darwin almost 150 years ago: 38 different females, and, incredibly, the listening to his wife are enormous, with no fitness, for animals they have been studying nesting for many other organisms polyandry (i.e. mating with more than one victims were the offspring of close kin in the costs. for many years. such as burrowing owls, tiger salamanders, male). ‘Females of almost every sexual killer’s home territory in 62 of the 65 killings and hundreds of species of and species that has been carefully studied – from (95%). The most common victims were the The Latest Outlandish Discovery The Future of the Prairie Dog spiders. Further, prairie dogs serve as plants and slime moulds through humans offspring of the killer’s mother (the killer’s prey for numerous predators – American and other primates – commonly solicit siblings), the offspring of the killer’s daughter Individuals of different species commonly Prairie dogs have faced many serious badgers, bobcats, and coyotes to name a few sperm from two or more males,’ he explains. (the killer’s grandoffspring), and the offspring compete with each other. African lions challenges over time, mostly from humans. mammalian enemies, and golden eagles, ‘But this is a paradox, because a female can of the killer’s sister (the killer’s nieces and and spotted hyenas compete for the same Because prairie dogs are that northern goshawks, and prairie falcons almost always obtain all the sperm she needs nephews). Some lactating females were prey, for example. To reduce interspecific commonly live in grasslands used for raising to name a few avian enemies. Escaping to fertilise all her eggs from a single mating, more likely to kill than others. One serial competition, natural selection commonly cattle, ranchers have worried that they will extinction for at least one species, the black- and additional matings increase the risk of killer, for example, slew all juveniles in eight favors divergence in ecology, morphology, or consume vegetation necessary to fatten footed ferret, is dependent on the long-term One-year-old female white-tailed prairie dog diseases, parasites, and predation.’ John has litters over 3 years, and another serial killer physiology. But natural selection has favored their livestock. Such competition does survival of prairie dogs, because ferrets feed that has just killed a juvenile via a series of bites to the neck. documented three clear benefits for female dispatched juveniles in six litters over 3 years. a different, unusual strategy for one species sometimes occur, but cattle nevertheless almost exclusively on prairie dogs. If prairie Photo by John Hoogland. prairie dogs that mate with more than one But now consider this: When juveniles are of prairie dog that John has studied: White- often prefer to forage at colony-sites because dogs disappear, grassland ecosystems as we male: polyandrous females are more likely to about 6 weeks old and appear aboveground tailed prairie dogs kill, but do not consume, the plants there can be more nutritious. know them will vanish as well. conceive, they wean larger litters, and their from their nursery burrows for the first time, Wyoming ground squirrels encountered in Ranchers also fret that their cattle will incur John has just begun to write his ‘magnum offspring have higher survivorship in the females commonly suckle the offspring of the prairie dog’s home territory. Like prairie broken legs from stepping into burrows, but John hopes that his research will help to opus’ – a book in which he will attempt first year after weaning. Win, Win, and Win close kin such as sisters, daughters, and dogs but smaller, ground squirrels are such fractures are exceedingly rare. These conserve prairie dogs. One of his key findings to summarise and explain all 44 years of again. For prairie dogs, at least, polyandry is nieces living in the home territory – the colonial, diurnal, burrowing rodents that overrated concerns have led ranchers to is helping to dispel a century-old myth his research with prairie dogs. He reflects, no longer a mystery – with the implication same offspring they had been trying to kill inhabit western North America and eat the shoot and poison billions of prairie dogs over perpetuated by farmers and ranchers: that ‘If we want to save prairie dogs and their that these same benefits might apply to the for the previous several weeks. Say what?!? same plants that prairie dogs also consume. the last 150 years, often with assistance from prairie dogs are fast-breeding like mice and ecosystems, knowledge is power, and thousands of other less-studied species for ‘Life for prairie dogs is all about balancing federal and state agencies. In recent years, rats, and will take over grasslands unless they my research is providing information on which females frequently mate with more competition with cooperation,’ says John, In collaboration with Charles Brown, disease has been another problem for prairie are exterminated. By contrast, John’s tracking every aspect of the biology of prairie dogs. than one male. ‘but this sudden transition from the killing of John discovered that interspecific killing dogs: Millions have died from epidemics of of thousands of prairie dogs first captured as Unfortunately, I will not live long enough to the offspring of close kin to the communal (IK) of ground squirrels by prairie dogs bubonic plague, an introduced disease to juveniles demonstrates that prairie dogs do answer all the questions I still have. Beyond the dynamics of choosing mates, nursing of the offspring of close kin is was common, involving a preposterous which prairie dogs have no good defence. not live long (usually only 1 or 2 years), that I especially want to better understand the prairie dog mothers face other formidable nonetheless extraordinary. 47 different killers of both sexes. In 3 of 6 Further, housing communities and shopping many females do not reproduce every year, serial killing of juveniles of close kin by challenges associated with raising offspring years, the number of IKs was higher that the malls have destroyed much of their natural and that successful females can only wean a female black-tailed prairie dogs, and the in a crowded colony. Both invading adult Though this balance of competition versus number of ground squirrels killed by the habitat. As a result, two species of prairie small number of offspring (usually three or serial killing of Wyoming ground squirrels by males and lactating females commonly cooperation can be difficult to maintain, combined efforts of fifteen mammalian and dogs are now on the list of threatened and four, with a maximum of eight) per year. white-tailed prairie dogs.’ kill and cannibalise a mother’s unweaned John has found that females usually remain avian predators such as American badgers, endangered species, and the other species

WWW.SCIENTIA.GLOBAL WWW.SCIENTIA.GLOBAL Meet the researcher Professor John L. Hoogland Professor of Wildlife Ecology Appalachian Laboratory The University of Maryland Center for Environmental Science Frostburg, Maryland, USA

Professor John Hoogland completed his BSc (1971) and PhD (1977) at KEY COLLABORATORS the University of Michigan. After completing a postdoc at the University of Minnesota in 1979 and serving as an Assistant Professor at Princeton Professor Charles Brown, University of Tulsa University for several years, John joined the Appalachian Laboratory Professor David Eads, United States Geological Survey of the University of Maryland Center for Environmental Science in 1985, where he is currently a Professor of Wildlife Ecology. Since he FUNDING first saw them when he was a graduate student in 1974, prairie dogs have fascinated John. Over the last 44 years, he has devoted his career Since he started studying prairie dogs in 1974, 22 different organisations to finding answers to questions about the conservation, ecology, have funded John’s research. Recent sources of funding include and social behaviour of these amazing grassland rodents. As John Colorado Parks and Wildlife, Denver Zoological Foundation, National frequently says: ‘Gotta love those prairie dogs.’ Science Foundation, and New Mexico Department of Game and Fish.

Awards during John’s career include the Peter Okkelberg Award for REFERENCES outstanding achievement in biology (1971), the American Society of Mammalogists Alma Shadle Award (1976), the Harry Frank Guggenheim JL Hoogland, CR Brown, Prairie dogs increase fitness by killing Career Development Award (1986), and the Prairie Dog Protector of interspecific competitors, Proceedings of the Royal Society B, 2016, 283, the Year Award (2015). Citations to John’s research number >5,000, and 1–7. span >120 journals. His discoveries have been reported in hundreds JL Hoogland, Prairie dogs disperse when all close kin have of newspapers around the world, 10 textbooks, 9 radio programs, 11 disappeared, Science, 2013, 339, 1205–1207. television programs, and also >50 popular magazines such as Atlantic, Audubon, National Geographic, National Wildlife, New Scientist, Ranger JL Hoogland, Why do female prairie dogs copulate with more than one Rick, Science News, and Smithsonian. male?—Insights from long-term research, Journal of Mammalogy, 2013, 94, 731–744. CONTACT JL Hoogland, editor, Conservation of the black-tailed prairie Dog, Island Press, Washington, District of Columbia, 2006. E: [email protected] T: (+1) 301 689 7130 JL Hoogland, The black-tailed prairie dog: Social life of a burrowing W: http://www.umces.edu/al/people/jhoogland , University of Chicago Press, 1995.

JL Hoogland, Levels of inbreeding among prairie dogs, American Naturalist, 1992, 139, 591–602.

JL Hoogland, Infanticide in prairie dogs: Lactating females kill offspring of close kin, Science, 1985, 230, 1037–1040.

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