Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study

Top‐order predators often have positive effects on biological diversity owing to their key functional roles in regulating trophic cascades and other ecological processes. Their loss has been identified as a major factor contributing to the decline of biodiversity in both aquatic and terrestrial systems. Consequently, restoring and maintaining the ecological function of top predators is a critical global imperative. Here we review studies of the ecological effects of the dingo Canis lupus dingo, Australia's largest land predator, using this as a case study to explore the influence of a top predator on biodiversity at a continental scale. The dingo was introduced to Australia by people at least 3500 years ago and has an ambiguous status owing to its brief history on the continent, its adverse impacts on livestock production and its role as an ecosystem architect. A large body of research now indicates that dingoes regulate ecological cascades, particularly in arid Australia, and that the removal of dingoes results in an increase in the abundances and impacts of herbivores and invasive mesopredators, most notably the red fox Vulpes vulpes. The loss of dingoes has been linked to widespread losses of small and medium‐sized native mammals, the depletion of plant biomass due to the effects of irrupting herbivore populations and increased predation rates by red foxes. We outline a suite of conceptual models to describe the effects of dingoes on vertebrate populations across different Australian environments. Finally, we discuss key issues that require consideration or warrant research before the ecological effects of dingoes can be incorporated formally into biodiversity conservation programs.     

Keystone effects of an alien top-predator stem extinctions of native mammals

Alien predators can have catastrophic effects on ecosystems and are thought to be much more harmful to biodiversity than their native counterparts. However, trophic cascade theory and the mesopredator release hypothesis predict that the removal of top predators will result in the reorganization of trophic webs and loss of biodiversity. Using field data collected throughout arid Australia, we provide evidence that removal of an alien top-predator, the dingo, has cascading effects through lower trophic levels. Dingo removal was linked to increased activity of herbivores and an invasive mesopredator, the red fox (Vulpes vulpes), and to the loss of grass cover and native species of small mammals. Using species distribution data, we predict that reintroducing or maintaining dingo populations would produce a net benefit for the conservation of threatened native mammals across greater than 2.42 × 10⁶ km² of Australia. Our study provides evidence that an alien top predator can assume a keystone role and be beneficial for biodiversity conservation, and also that mammalian carnivores more generally can generate strong trophic cascades in terrestrial ecosystems.     

Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management

Mammalian carnivore populations are often intensively managed, either because the carnivore in question is endangered, or because it is viewed as a pest and is subjected to control measures, or both. Most management programmes treat carnivore species in isolation. However, there is a large and emerging body of evidence to demonstrate that populations of different carnivores interact with each other in a variety of complex ways. Thus, the removal or introduction of predators to or from a system can often affect other species in ways that are difficult to predict. Wildlife managers must consider such interactions when planning predator control programmes. Integrated predator control will require a greater understanding of the complex relationships between species. In many parts of the world, sympatric species of carnivores have coexisted over an evolutionary time scale so that niche differentiation has occurred, and competition is difficult to observe. Australia has experienced numerous introductions during the past 200 years, including those of the red fox (Vulpes vulpes) and the feral cat (Felis catus). These species now exist in sympatry with native mammalian predators, providing ecologists with the opportunity to study their interactions without the confounding effects of coevolution. Despite an increasing body of observational evidence for complex interactions among native and introduced predators in Australia, few studies have attempted to clarify these relationships experimentally, and the interactions remain largely unacknowledged. A greater understanding of these interactions would provide ecologists and wildlife managers world-wide with the ability to construct robust predictive models of carnivore communities, and to identify their broader effects on ecosystem functioning. We suggest that future research should focus on controlled and replicated predator removal or addition experiments. The dingo (Canis lupus dingo), as a likely keystone species, should be a particular focus of attention.     

Top-predator control-induced trophic cascades: an alternative hypothesis to the conclusion of Colman et al.

Colman et al. (2014 Proc. R. Soc. B 281, 20133094. (doi:10.1098/rspb.2013.3094)) recently argued that observed positive relationships between dingoes and small mammals were a result of top-down processes whereby lethal dingo control reduced dingoes and increased mesopredators and herbivores, which then suppressed small mammals. Here, I show that the prerequisite negative effects of dingo control on dingoes were not shown, and that the same positive relationships observed may simply represent well-known bottom-up processes whereby more generalist predators are found in places with more of their preferred prey. Identification of top-predator control-induced trophic cascades first requires demonstration of some actual effect of control on predators, typically possible only through manipulative experiments with the ability to identify cause and effect.     

Demographic and functional responses of wild dogs to poison baiting

Lethal control of wild dogs – that is Dingo (Canis lupus dingo) and Dingo/Dog (Canis lupus familiaris) hybrids – to reduce livestock predation in Australian rangelands is claimed to cause continental‐scale impacts on biodiversity. Although top predator populations may recover numerically after baiting, they are predicted to be functionally different and incapable of fulfilling critical ecological roles. This study reports the impact of baiting programmes on wild dog abundance, age structures and the prey of wild dogs during large‐scale manipulative experiments. Wild dog relative abundance almost always decreased after baiting, but reductions were variable and short‐lived unless the prior baiting programme was particularly effective or there were follow‐up baiting programmes within a few months. However, age structures of wild dogs in baited and nil‐treatment areas were demonstrably different, and prey populations did diverge relative to nil‐treatment areas. Re‐analysed observations of wild dogs preying on kangaroos from a separate study show that successful chases that result in attacks of kangaroos by wild dogs occurred when mean wild dog ages were higher and mean group size was larger. It is likely that the impact of lethal control on wild dog numbers, group sizes and age structures compromise their ability to handle large difficult‐to‐catch prey. Under certain circumstances, these changes sometimes lead to increased calf loss (Bos indicus/B. taurus genotypes) and kangaroo numbers. Rangeland beef producers could consider controlling wild dogs in high‐risk periods when predation is more likely and avoid baiting at other times.     

Fox‐baiting in agricultural landscapes in south‐eastern Australia: a case‐study appraisal and suggestions for improvement

Summary In south‐eastern Australia, the introduced Red Fox (Vulpes vulpes) is a major predator of native wildlife and livestock. Fox control in agricultural landscapes is heavily reliant on the laying of poisoned baits by private landholders, yet there have been few assessments of the application or success of landholder‐baiting practices. We evaluated a community‐based fox‐baiting campaign, typical of programs employed throughout the agricultural regions of south‐eastern Australia to control foxes. We recorded the spatial coverage of 1080 baits deployed by landholders, assessed baiting procedures, monitored the survival of six radio‐collared foxes during and after baiting, and compared the spatial coverage and likely effectiveness of the baiting program with two alternative (theoretical) baiting strategies. Relative to other baiting programs, coordination among neighbours was reasonably high, with 37.5% of baited properties (n = 40) adjoining ≥3 neighbouring properties that also contained baits. Nevertheless, the maximum distance from the centre of a baited property to the nearest edge of an unbaited property was <750 m (mean = 380 m ± 147 m SD). On average, 33% (±17% SD) of each fox’s home range overlapped with baited properties, but only two foxes died during the baiting program. The remaining four foxes were still alive 10 weeks after baiting ceased. Modelling of simulated fox home ranges showed that 13.5% contained no bait stations based on the community baiting program, whereas alternative roadside‐ and grid‐baiting strategies (theoretically) delivered baits to all simulated home ranges. Some landholders employed practices that could reduce the effectiveness of baiting programs such as not removing decayed baits before deploying new ones or placing bait stations too close together. Our research illustrates the difficulties of managing a coordinated baiting program on private land that effectively controls foxes. Alternative baiting strategies such as roadside baiting need to be considered to improve fox control in agricultural landscapes.     

BIODIVERSITY RESEARCH: Diversity and distribution of macroinvertebrates in lentic habitats in massively altered landscapes in south‐eastern Australia

Aim We investigated whether faunas of lentic macroinvertebrates differed among two landscape types: (1) those that are largely covered in forests (presumed to be in a more pre‐human‐impact condition) and (2) those that are completely cleared for agricultural exploitation (massively altered). Location Five pairs of landscapes (each pair referred to as a region) – one of each landscape type – across a 30,000 km² region of north‐central Victoria, Australia. Methods Each individual waterbody was surveyed three times (austral spring 2006, autumn 2007, and spring 2007) for invertebrates. Waterbodies were characterized by measurements of static (e.g. abutting vegetation cover) and labile (e.g. pH) variables. Data were analysed using hierarchical Bayesian models of species richness, α‐ and β‐diversities and functional feeding groups. Assemblage composition was related to landscape and in‐waterbody characteristics. Results Neither measured, nor asymptotic estimates of, species richness differed among landscape types, notwithstanding consistent differences in in‐waterbody habitat characteristics among waterbodies in the two landscape types. There were no discernible differences in patterns of α‐ and β‐diversities at landscape scales relating to landscape type. Habitat diversity of waterbodies at the landscape scale did not affect β‐diversity, although distinct waterbodies within landscapes tended to have more distinct faunas. Main conclusions The lentic macroinvertebrate faunas are relatively homogeneous over the entire region, with little differentiation between wooded and cleared landscapes. The regional fauna may be a homogenized subset of native species, possibly arising from the huge numerical predominance of lentic habitats in agricultural landscapes producing ‘spill‐over’ effects into forested landscapes. Of taxa more frequently found in one or other landscape type, trophic group diversity was greater in forested landscapes.     

Changes in understorey plant species richness following logging and prescribed burning in shrubby dry sclerophyll forests of south‐eastern Australia

Abstract The impacts of prescribed burning and timber harvesting on species diversity have been the subject of considerable debate. The temporal and spatial scale of these disturbances often presents major limitations to many studies. Here we present the medium‐term results of a planned long‐term study examining the impacts of logging and prescribed burning on the understorey floristic richness in shrubby dry sclerophyll forest in the south‐east of New South Wales, Australia. Generalized estimating equations were used to model the effect of environmental factors and disturbance variables on species richness at the coupe (～30 ha) and plot (～0.01 ha) scale. At the plot scale, fire effects on separate components of the vegetation were broadly consistent with other studies, with frequent fire resulting in a relative increase of species richness for species less than 1 m in height and a decline of larger species taller than this height. At the coupe scale, there was no decline in richness of larger shrub species, possibly owing to the spatial heterogeneity of fire frequency at this scale. Logging resulted in significantly greater species richness in the shrub layer, but had no significant effect on species richness in the ground layer. During the study period, there was a general decline in plant species richness at both coupe and plot scales which occurred independently of imposed management regimes. This is thought to be related to a natural succession following wildfire, and may be due to the absence of high‐intensity fire in the study area since 1973, or to an effect related to season of burning.     

Revegetation,restoration and reptiles in rural landscapes: Insights from long‐term monitoring programmes in the temperate eucalypt woodlands of south‐eastern Australia

Over the past decade, there has been a concerted effort to better understand the distribution and abundance of reptiles in agricultural landscapes and to specifically evaluate their response to revegetation (tree and shrub plantings) and habitat restoration in the wheat‐sheep belt of south‐eastern Australia. This article reviews the response of reptiles to revegetation and woodland management and provides ten insights and lessons that can be applied to help improve reptile conservation in temperate eucalypt woodlands and fragmented agricultural landscapes in Australia. The review focuses primarily on revegetation programmes conducted by Landcare and Greening Australia, and management interventions funded by Local Land Services in NSW and Catchment Management Authorities in Victoria.     

Nestedness in fragmented landscapes: birds of the box‐ironbark forests of south‐eastern Australia

Nestedness in biota as a function of species richness – biota of depauperate assemblages being non‐random subsets of richer biotas – has been widely documented in recent years (see Wright et al. 1998 , Oecologia 113: 1–20). Ordering sites by richness maximizes nestedness indices; however, ordering by other criteria such as area or isolation may be more ecologically interpretable. We surveyed birds in true fragments (35 in all), and in “reference areas” in large extant forest blocks (30 locations), of the same range of areas (10, 20, 40, 80 ha). The avifauna was divided into “bush birds”– species dependent on forest and woodland, and “open country” species. We looked at nestedness in four data sets: “bush birds” in fragments and reference areas, and “all birds” in fragments and in reference areas. All data sets were significantly nested. Ordering by area in all cases was not significantly less nested than ordering by richness. Ordering by area in fragments was significantly greater than in reference areas, but the differences in standardized nestedness indices were small (<15%). We identified those birds that had distributions among fragments that conformed strongly with area, those that were more randomly distributed and some species that were more likely to occupy the smallest fragments. Among the latter was a hyperaggressive, invasive, colonial native species (noisy miner Manorina melanocephala). A suite of small, insectivorous birds were more likely to strongly conform with expected distributions in relation to area, which was consistent with observations of their vulnerability to the effects of the noisy miner in smaller fragments.     

Habitat and introduced predators influence the occupancy of small threatened macropods in subtropical Australia

Australia has had the highest rate of mammal extinctions in the past two centuries when compared to other continents. Frequently cited threats include habitat loss and fragmentation, changed fire regimes and the impact of introduced predators, namely the red fox (Vulpes vulpes) and the feral cat (Felis catus). Recent studies suggest that Australia's top predator, the dingo (Canis dingo), may have a suppressive effect on fox populations but not on cat populations. The landscape of fear hypothesis proposes that habitat used by prey species comprises high to low risk patches for foraging as determined by the presence and ubiquity of predators within the ecosystem. This results in a landscape of risky versus safe areas for prey species. We investigated the influence of habitat and its interaction with predatory mammals on the occupancy of medium‐sized mammals with a focus on threatened macropodid marsupials (the long‐nosed potoroo [Potorous tridactylous] and red‐legged pademelon [Thylogale stigmatica]). We assumed that differential use of habitats would reflect trade‐offs between food and safety. We predicted that medium‐sized mammals would prefer habitats for foraging that reduce the risk of predation but that predators would have a positive relationship with medium‐sized mammals. We variously used data from 298 camera trap sites across nine conservation reserves in subtropical Australia. Both dingoes and feral cats were broadly distributed, whilst the red fox was rare. Long‐nosed potoroos had a strong positive association with dense ground cover, consistent with using habitat complexity to escape predation. Red‐legged pademelons showed a preference for open ground cover, consistent with a reliance on rapid bounding to escape predation. Dingoes preferred areas of open ground cover whereas feral cats showed no specific habitat preference. Dingoes were positively associated with long‐nosed potoroos whilst feral cats were positively associated with red‐legged pademelons. Our study highlights the importance of habitat structure to these threatened mammals and also the need for more detailed study of their interactions with their predators.     

Habitat selection by feral cats and dingoes in a semi‐arid woodland environment in central Australia

Habitat use by feral cats and dingoes was examined within a heterogeneous semi‐arid woodland site in central Australia over 2 years. Density estimates of feral cats based on tracks were higher in mulga habitat than in open habitat. Isodar analysis implied that this pattern of habitat use by feral cats was consistent with the consumer‐resource model of density‐dependent habitat selection, which is an ideal free solution. The reason why mulga supported higher densities of feral cats was unclear. Foraging success of feral cats may be higher in the mulga because the stalk and ambush hunting tactics typically employed by felids are well suited to dense cover. Mulga may also have offered feral cats more protection from dingo predation. Dingo activity was distributed uniformly across habitats. The dingo isodar was statistically non‐significant, suggesting that habitat selection by dingoes was independent of density.     

Heavy metal pollution negatively correlates with anuran species richness and distribution in south‐eastern Australia

Heavy metal pollution has likely played an important role in global biodiversity decline, but there remains a paucity of information concerning the effects of metals on amphibian diversity. This study assessed anuran species richness and distribution in relation to sediment metal content and water chemistry in wetlands located along the Merri Creek corridor in Victoria, south‐eastern Australia. Anurans were present in 60% (21/35) of study sites, with a total of six species detected: the eastern common froglet (Crinia signifera), the eastern sign‐bearing froglet (Crinia parinsignifera), the southern brown tree frog (Litoria ewingii), the growling grass frog (Litoria raniformis), the eastern banjo frog (Limnodynastes dumerilii) and the spotted marsh frog (Limnodynastes tasmaniensis). Mean species richness was 1.77 ± 0.32 per site, and species richness ranged from zero to six species per site. Across sites, species richness correlated negatively with sediment concentrations of six heavy metals: copper, nickel, lead, zinc, cadmium and mercury. Species richness also correlated negatively with wetland water electrical conductivity (a proxy for salinity) and concentrations of orthophosphate. Distributions of the three most commonly observed frog species (C. signifera, L. tasmaniensis and L. ewingii) were significantly negatively associated with the total level of metal contamination at individual sites. The study is the first to provide evidence for an association between metal contamination and anuran species richness and distribution in the southern hemisphere, adding to a small but growing body of evidence that heavy metal pollution has contributed to global amphibian decline.     

Land use legacy effects on woody vegetation in agricultural landscapes of south‐western Ethiopia

Aim

Past land use legacy effects—extinction debts and immigration credits—might be particularly pronounced in regions characterized by complex and dynamic landscape change. The aim of this study was to evaluate how current woody plant species distribution, composition and richness related to historical and present land uses.

Location

A smallholder farming landscape in south‐western Ethiopia.

Methods

We surveyed woody plants in 72 randomly selected 1‐ha sites in farmland and grouped them into forest specialist, generalist and pioneer species. First, we investigated woody plant composition and distribution using non‐metric multidimensional scaling. Second, we modelled species richness in response to historical and current distance from the forest edge. Third, we examined diameter class distributions of trees in recently converted vs. permanent farmland.

Results

Historical distance was a primary driver of woody plant composition and distribution. Generalist and pioneer species richness increased with historical distance. Forest specialists, however, did not respond to historical distance. Only few old individuals of forest specialist species remained in both recently converted and permanent farmlands.

Main conclusions

Our findings suggest that any possible extinction debt for forest specialist species in farmland at the landscape scale was rapidly paid off, possibly because farmers cleared large remnant trees. In contrast, we found substantial evidence of immigration credits in farmland for generalist and pioneer species. This suggests that long‐established farmland may have unrecognized conservation values, although apparently not for forest specialist species. We suggest that conservation policies in south‐western Ethiopia should recognize not only forests, but also the complementary value of the agricultural mosaic—similar to the case of European cultural landscapes. A possible future priority could be to better reintegrate forest species in the farmland mosaic.

     

Avian top predator and the landscape of fear: responses of mammalian mesopredators to risk imposed by the golden eagle

Top predators may induce extensive cascading effects on lower trophic levels, for example, through intraguild predation (IGP). The impacts of both mammalian and avian top predators on species of the same class have been extensively studied, but the effects of the latter upon mammalian mesopredators are not yet as well known. We examined the impact of the predation risk imposed by a large avian predator, the golden eagle (Aquila chrysaetos, L.), on its potential mammalian mesopredator prey, the red fox (Vulpes vulpes, L.), and the pine marten (Martes martes, L.). The study combined 23 years of countrywide data from nesting records of eagles and wildlife track counts of mesopredators in Finland, northern Europe. The predation risk of the golden eagle was modeled as a function of territory density, density of fledglings produced, and distance to nearest active eagle territory, with the expectation that a high predation risk would reduce the abundances of smaller sized pine martens in particular. Red foxes appeared not to suffer from eagle predation, being in fact most numerous close to eagle nests and in areas with more eagle territories. This is likely due to similar prey preferences of the two predators and the larger size of foxes enabling them to escape eagle predation risk. Somewhat contrary to our prediction, the abundance of pine martens increased from low to intermediate territory density and at close proximity to eagle nests, possibly because of similar habitat preferences of martens and eagles. We found a slightly decreasing trend of marten abundance at high territory density, which could indicate that the response in marten populations is dependent on eagle density. However, more research is needed to better establish whether mesopredators are intimidated or predated by golden eagles, and whether such effects could in turn cascade to lower trophic levels, benefitting herbivorous species.     

The functional role of biodiversity in ecosystems: incorporating trophic complexity

Understanding how biodiversity affects functioning of ecosystems requires integrating diversity within trophic levels (horizontal diversity) and across trophic levels (vertical diversity, including food chain length and omnivory). We review theoretical and experimental progress toward this goal. Generally, experiments show that biomass and resource use increase similarly with horizontal diversity of either producers or consumers. Among prey, higher diversity often increases resistance to predation, due to increased probability of including inedible species and reduced efficiency of specialist predators confronted with diverse prey. Among predators, changing diversity can cascade to affect plant biomass, but the strength and sign of this effect depend on the degree of omnivory and prey behaviour. Horizontal and vertical diversity also interact: adding a trophic level can qualitatively change diversity effects at adjacent levels. Multitrophic interactions produce a richer variety of diversity-functioning relationships than the monotonic changes predicted for single trophic levels. This complexity depends on the degree of consumer dietary generalism, trade-offs between competitive ability and resistance to predation, intraguild predation and openness to migration. Although complementarity and selection effects occur in both animals and plants, few studies have conclusively documented the mechanisms mediating diversity effects. Understanding how biodiversity affects functioning of complex ecosystems will benefit from integrating theory and experiments with simulations and network-based approaches.     

The impact of fire regimes on populations of an endangered lizard in montane south‐eastern Australia

The Blue Mountains water skink (Eulamprus leuraensis; Scincidae) is restricted to less than 40 fragmented swamp sites, all within the Blue Mountains and Newnes Plateau areas of New South Wales, Australia. Climate change is expected to increase fire frequency in the area, potentially degrading habitat quality for this endangered reptile. We quantified lizard abundances in 12 swamps using standardized surveys, and constructed a Global Information System (GIS) database to determine fire‐histories for each swamp since 1967. The abundance of Blue Mountains water skinks was negatively correlated with fire frequency, but not with time since fire. Indirect impacts of fire (mediated via shifts in vegetation density, moisture levels, prey availability and post‐fire predation) may be more important than direct effects in these cool, moist habitats. Although lizards were less common in swamps close to urban areas, and less common in frequently burnt areas, viable populations of this endangered reptile still persist even in anthropogenically disturbed swamps and in swamps that have experienced up to four fires in 20 years. Future research could usefully extend these analyses to other swamps in the locality, and explore the broader impacts of fire regimes on the distinctive flora and fauna of this threatened ecological community.     

Environmental gradients and the evolution of tri‐trophic interactions

Long‐standing theory predicts herbivores and predators should drive selection for increased plant defences, such as the specific production of volatile organic compounds for attracting predators near the site of damage. Along elevation gradients, a general pattern is that herbivores and predators are abundant at low elevation and progressively diminish at higher elevations. To determine whether plant adaptation along such a gradient influences top‐down control of herbivores, we manipulated soil predatory nematodes, root herbivore pressure and plant ecotypes in a reciprocal transplant experiment. Plant survival was significantly higher for low‐elevation plants, but only when in the presence of predatory nematodes. Using olfactometer bioassays, we showed correlated differential nematode attraction and plant ecotype‐specific variation in volatile production. This study not only provides an assessment of how elevation gradients modulate the strength of trophic cascades, but also demonstrates how habitat specialisation drives variation in the expression of indirect plant defences.     

Microhabitat relationships among five lizard species associated with granite outcrops in fragmented agricultural landscapes of south‐eastern Australia

A fundamental part of developing effective biodiversity conservation is to understand what factors affect the distribution and abundance of particular species. However, there is a paucity of data on ecological requirements and habitat relationships for many species, especially for groups such as reptiles. Furthermore, it is not clear whether habitat relationships for particular species in a given environment are transferable to other environments within their geographical range. This has implications for the type of ‘landscape model’ used to guide management decisions in different environments worldwide. To test the hypothesis that species‐specific habitat relationships are transferable to other environments, we present microhabitat models for five common lizard species from a poorly studied habitat – insular granite outcrops, and then compared these relationships with studies from other environments in south‐eastern Australia. We recorded twelve species from five families, representing 699 individuals, from 44 outcrops in the south‐west slopes of New South Wales. Five lizard species were abundant and accounted for 95% of all observations: Egernia striolata, Ctenotus robustus, Cryptoblepharus carnabyi, Morethia boulengeri and Carlia tetradactyla (Scincidae). Linear regression modelling revealed suites of different variables related to the abundance patterns of individual species, some of which were broadly congruent with those measured for each species in other environments. However, additional variables, particular to rocky environments, were found to relate to reptile abundance in this environment. This finding means that species' habitat relationships in one habitat may not be readily transferable to other environments, even those relatively close by. Based on these data, management decisions targeting reptile conservation in agricultural landscapes, which contain rocky outcrops, will be best guided by landscape models that not only recognize gradients in habitat suitability, but are also flexible enough to incorporate intraspecies habitat variability.