Michael H. Parsons

Familiarity Breeds Contempt: Kangaroos Persistently Avoid Areas with Experimentally Deployed Dingo Scents

Background Whether or not animals habituate to repeated exposure to predator scents may depend upon whether there are predators associated with the cues. Understanding the contexts of habituation is theoretically important and has profound implication for the application of predator-based herbivore deterrents. We repeatedly exposed a mixed mob of macropod marsupials to olfactory scents (urine, feces) from a sympatric predator (Canis lupus dingo), along with a control (water). If these predator cues were alarming, we expected that over time, some red kangaroos (Macropus rufous), western grey kangaroos (Macropus fuliginosus) and agile wallabies (Macropus agilis) would elect to not participate in cafeteria trials because the scents provided information about the riskiness of the area. Methodology/Principal Findings We evaluated the effects of urine and feces independently and expected that urine would elicit a stronger reaction because it contains a broader class of infochemicals (pheromones, kairomones). Finally, we scored non-invasive indicators (flight and alarm stomps) to determine whether fear or altered palatability was responsible for the response. Repeated exposure reduced macropodid foraging on food associated with 40 ml of dingo urine, X = 986.75±3.97 g food remained as compared to the tap water control, X = 209.0±107.0 g (P<0.001). Macropodids fled more when encountering a urine treatment, X = 4.50±2.08 flights, as compared to the control, X = 0 flights (P<0.001). There was no difference in effect between urine or feces treatments (P>0.5). Macropodids did not habituate to repeated exposure to predator scents, rather they avoided the entire experimental area after 10 days of trials (R 2 = 83.8; P<0.001). Conclusions/Significance Responses to urine and feces were indistinguishable; both elicited fear-based responses and deterred foraging. Despite repeated exposure to predator-related cues in the absence of a predator, macropodids persistently avoided an area of highly palatable food. Area avoidance is consistent with that observed from other species following repeated anti-predator conditioning, However, this is the first time this response has been experimentally observed among medium or large vertebrates − where a local response is observed spatially and an area effect is revealed over time.

Sounds Scary? Lack of Habituation following the Presentation of Novel Sounds

Background Animals typically show less habituation to biologically meaningful sounds than to novel signals. We might therefore expect that acoustic deterrents should be based on natural sounds. Methodology We investigated responses by western grey kangaroos (Macropus fulignosus) towards playback of natural sounds (alarm foot stomps and Australian raven (Corvus coronoides) calls) and artificial sounds (faux snake hiss and bull whip crack). We then increased rate of presentation to examine whether animals would habituate. Finally, we varied frequency of playback to investigate optimal rates of delivery. Principal Findings Nine behaviors clustered into five Principal Components. PC factors 1 and 2 (animals alert or looking, or hopping and moving out of area) accounted for 36% of variance. PC factor 3 (eating cessation, taking flight, movement out of area) accounted for 13% of variance. Factors 4 and 5 (relaxing, grooming and walking; 12 and 11% of variation, respectively) discontinued upon playback. The whip crack was most evocative; eating was reduced from 75% of time spent prior to playback to 6% following playback (post alarm stomp: 32%, raven call: 49%, hiss: 75%). Additionally, 24% of individuals took flight and moved out of area (50 m radius) in response to the whip crack (foot stomp: 0%, raven call: 8% and 4%, hiss: 6%). Increasing rate of presentation (12x/min ×2 min) caused 71% of animals to move out of the area. Conclusions/Significance The bull whip crack, an artificial sound, was as effective as the alarm stomp at eliciting aversive behaviors. Kangaroos did not fully habituate despite hearing the signal up to 20x/min. Highest rates of playback did not elicit the greatest responses, suggesting that ‘more is not always better’. Ultimately, by utilizing both artificial and biological sounds, predictability may be masked or offset, so that habituation is delayed and more effective deterrents may be produced.

Effects of Novel and Historic Predator Urines on Semi-Wild Western Grey Kangaroos

Abstract Classic studies in fear ecology have been inconclusive regarding whether predator waste products repel herbivores and whether the deterrent effect, if any, is based on repulsion or fear. Other studies imply that the predator must have co-evolved with prey to maximize the efficacy of response. We used chemosensory cues from the urine of native and nonnative canines to manipulate the behavior of the western grey kangaroo (Macropus fuliginosus). One-choice feeding trials were located along a distance gradient, and administered to 28 free-ranging, semi-wild, western grey kangaroos. Foods closer to the chemical source (within 12 m) were less likely to be eaten than those further from the source when the urine came from a native predator, the dingo (Canis dingo). Flight behavior was more likely to be observed on occasions when the dingo urine had been presented. A lesser effect occurred (to within 6 m) when urine was presented from the nonnative canid (coyote [Canis latrans]), while the flight behavior occurred once. Neither human urine, nor tap-water control, had any effect. We offer the first evidence that native predator-based chemical cues affect patch selection, while increasing fear, for this herbivore.

Are single odorous components of a predator sufficient to elicit defensive behaviors in prey species

When exposed to the odor of a sympatric predator, prey animals typically display escape or defensive responses. These phenomena have been well-documented, especially in rodents, when exposed to the odor of a cat, ferret, or fox. As a result of these experiments new discussions center on the following questions: (1) is a single volatile compound such as a major or a minor mixture constituent in urine or feces, emitted by the predator sufficient to cause defensive reactions in a potential prey species or (2) is a whole array of odors required to elicit a response and (3) will the relative size or escapability of the prey as compared to the predator influence responsiveness. Most predator-prey studies on this topic have been performed in the laboratory or under semi-natural conditions. Field studies could help to find answers to these questions. Australian mammals are completely naïve toward the introduced placental carnivores. That offers ideal opportunities to analyze in the field the responses of potential prey species to unknown predator odors. During the last decades researchers have accumulated an enormous amount of data exploring the effects of eutherian predator odors on native marsupial mammals. In this review, we will give a survey about the development of olfactory research, chemical signals and their influence on the behavior and—in some cases—physiology of prey species. In addition, we report on the effects of predator odor experiments performed under natural conditions in Australia. When studying all these literature we learned that data gained under controlled laboratory conditions elucidate the role of individual odors on brain structures and ultimately on a comparatively narrow range behaviors. In contrast to single odors odor arrays mimic much more the situation prey animals are confronted to in nature. Therefore, a broad range of methodology—from chemistry to ecology including anatomy, physiology, and behavior—is needed to understand all the different (relevant) stimuli that govern and guide the interactions between a predator and its potential prey.

Biologically meaningful scents: a framework for understanding predator–prey research across disciplines

Fear of predation is a universal motivator. Because predators hunt using stealth and surprise, there is a widespread ability among prey to assess risk from chemical information – scents – in their environment. Consequently, scents often act as particularly strong modulators of memory and emotions. Recent advances in ecological research and analytical technology are leading to novel ways to use this chemical information to create effective attractants, repellents and anti‐anxiolytic compounds for wildlife managers, conservation biologists and health practitioners. However, there is extensive variation in the design, results, and interpretation of studies of olfactory‐based risk discrimination. To understand the highly variable literature in this area, we adopt a multi‐disciplinary approach and synthesize the latest findings from neurobiology, chemical ecology, and ethology to propose a contemporary framework that accounts for such disparate factors as the time‐limited stability of chemicals, highly canalized mechanisms that influence prey responses, and the context within which these scents are detected (e.g. availability of alternative resources, perceived shelter, and ambient physical parameters). This framework helps to account for the wide range of reported responses by prey to predator scents, and explains, paradoxically, how the same individual predator scent can be interpreted as either safe or dangerous to a prey animal depending on how, when and where the cue was deposited. We provide a hypothetical example to illustrate the most common factors that influence how a predator scent (from dingoes, Canis dingo) may both attract and repel the same target organism (kangaroos, Macropus spp.). This framework identifies the catalysts that enable dynamic scents, odours or odorants to be used as attractants as well as deterrents. Because effective scent tools often relate to traumatic memories (fear and/or anxiety) that cause future avoidance, this information may also guide the development of appeasement, enrichment and anti‐anxiolytic compounds, and help explain the observed variation in post‐traumatic‐related behaviours (including post‐traumatic stress disorder, PTSD) among diverse terrestrial taxa, including humans.

A Nose for Death: Integrating Trophic and Informational Networks for Conservation and Management

Non-lethal management of wildlife, both ‘problem wildlife’ and pest species, to protect crops and threatened species is becoming increasingly important as non-human animals and humans come into closer proximity. A particularly promising approach is to apply predator scents to manipulate the cost/benefit ratio that influences the behavioral decisions made by prey and other predators about where to forage or rest. However, such olfactory manipulations are not always successful. Using insights from size-structured food webs, we develop a novel integrative model of the information that animals acquire from eavesdropping on predator and conspecific scents. We show how animals can use the information content in predator scents to derive knowledge of other predators and competitors and thus influence their decision to stay in or leave an area. This model framework clarifies how predator scents can influence all trophic levels, from interference competition directed at smaller predators, to predation and herbivory, and exploits direct and indirect pathways to promote landscapes of fear that influence spatial and temporal patch use in target animals. We illustrate how the application of this conceptual model can focus future research to enhance the use of predator scent-based deterrents in conservation and management. This integrated model shows great promise for addressing wildlife management concerns and for eventually improving the success and efficacy of traditional management techniques.

Relative effects of mammal herbivory and plant spacing on seedling recruitment following fire and mining

BackgroundThere is much debate concerning which ecological constraints are the most limiting factors to seedling recruitment in disturbed communities. We provide the first comparison between selective herbivory and plant competition effects among two post-mined forest ecosystems (primary succession) and one post-fire woodland ecosystem (secondary succession). Animal exclosure assessments of nine common species across eight sites were performed for comparison within three locations separated by up to 200 km. Additionally, we asked whether pre-browsed plants differed in nutrient content between or within species in the separate systems.ResultsAmong the nine common species, seven of these were affected by mammal herbivory while five shared a similar vulnerability to predation regardless of system. One species was limited by competition (planting density). There was a strong linear correlation between herbivore selectivity (% browsed) and impact (biomass loss) on the fertilized minesites, but not post-fire sites. Phosphorus and potassium were higher for most species in the post-mined system. Principal components analyses revealed that nutrients in shortest supply may be the most likely components of selection within each system. Among all locations, species with highest levels of phosphorus, ADF and leaf water content were often favoured, while high tannins and nitrogen content were generally selected against.ConclusionHerbivory, rather than seedling competition, was the limiting factor for plant performance among post-fire and post-mined reclamation areas. The post-fire seedlings were smaller and more water and nutrient limited, nevertheless browsing prevalence was equivalent at all locations with nearly all seedlings predated. Kangaroo density in the post-fire community declined from the beginning of the experiment, while numbers in the post-mined revegetation increased fourfold within one year. Differences in water and nutrient availability may explain why herbivores are more likely to be attracted to post-mined communities.

Novel use for a predator scent: preliminary data suggest that wombats avoid recolonising collapsed burrows following application of dingo scent

Abstract. Southern hairy-nosed wombats (Lasiorhinus latifrons) are fossorial marsupials that live in large burrow systems where their digging behaviour brings them into conflict with agriculture. In the absence of any available control options, non-selective culling is the primary mode of wombat management. This approach is contentious and has unknown implications for long-term wombat conservation. Predator scents, however, have been effective in altering behaviours of some herbivores and may offer a non-lethal alternative to culling if they discourage wombats from burrowing in perceived problem areas. Therefore, we trialled two dingo scents (faeces, urine) over 75 days to determine whether these scents would deter wombats from repopulating collapsed burrows. Ten inhabited single-entrance burrows were excavated over three days (to allow time for inhabitants to exit), collapsed and then filled in. Five burrows, separated by at least 200 m, were used for dingo scent treatments (three urine; two faeces) and three burrows, separated by the same distance, served as negative controls (unscented), along with two ‘farmer-monitored’ active controls (dog urine and a dingo carcass). We used a rank-sum score to assess wombat activity: scratching was scored with a value of (1), digging (2), and recolonisation (5), with each value reflecting total energy and time spent in the vicinity of the treatment. We fitted Generalised Estimating Equations (repeated-measures, Fisher Method) to explain variation within, and across, treatment and control burrows. Within 20 days, all 10 sites had signs of wombat activity that ranged from fresh digging, to fully functional burrows. Among the five treatment sites, scratching and tracks identified wombats as being present, but they did not dig. After 75 days, the five sites treated with dingo scents had minimal activity and no new burrows, while wombats recolonised all control burrows. Though we used only 10 burrows for this preliminary study, our findings suggest the need for further testing of dingo scents as a tool for dissuading wombats from digging and recolonisation of collapsed burrows. This represents a novel use for a predator scent, in that prey may remain in the vicinity near the deterrent, but curb problematic behaviours of economic consequence.

Jump-Starting Urban Rat Research: Conspecific Pheromones Recruit Wild Rats into a Behavioral and Pathogen-Monitoring Assay

Wild rats, Rattus spp, have adapted so well to urbanization that humans may be obligatory to their survival. Consequently, rats foul human food sources, predate threatened fauna and serve as reservoirs for disease, costing the US economy

A Detailed Protocol to Enable Safe-Handling, Preemptive Detection, and Systematic Surveillance of Rat-Vectored Pathogens in the Urban Environment

19 billion in losses year -1. Urban rat ecology however, remains vastly unexplored because these animals are cryptic, crepuscular, difficult to identify, and hazardous to handle. Additionally, the high-rise buildings that block satellite link-ups, underground sewers and subway tunnels, and rebar enforced concrete covered landscape make it difficult—if not impossible— to track urban animals using traditional radio telemetry. Consequently, there are few ecological studies with free-ranging urban rats. Therefore, we set out to monitor the behaviors and health of free-ranging rats in metropolitan New York. Recognizing that wild rats are attracted to live laboratory-reared conspecifics and that they are sensitive to pheromones, we used soiled rat bedding to repeatedly attract animals to a Remote Frequency Identification (RFID)- based antenna with camera-trap and load cell (scale) for collecting weights. We captured and micro-chipped 13 rats within 50, 30 and 10 m from our antenna and followed their movements. Seven of the 8 animals released within 10 m of the antenna, visited the RFID antenna lure 398 times over 41 standardized days. Males (2.7 visits day-1) visited the antenna at the same frequency as females (2.7 visits day-1; P>0.5), and both sexes spent similar time dwelling at the pheromones (M, 2.9±0.9 sec; F, 2.4.±0.4 sec; P>0.05). The passive integrated transponder (PIT)-tag worked free on the lone individual that did not participate. Within our population, female activity peaked between 6am and 7pm, while males visited throughout the day. Our results demonstrate the potential to safely overcome the primary barriers that have impeded urban rat ecological studies. We used pheromone-based lures to attract micro-chipped rats, irrespective of sex or age-class, where their individual identities, behaviors and pathogen loads could be consistently recorded. We discuss the potential for similar assays to help address several longstanding knowledge gaps in the literature regarding pathogen monitoring over time and space, rat dispersal patterns, population parameters and seasonal migrations through corridors.