Patterns in the abundance of kangaroo populations in arid Australia are consistent with the exploitation ecosystems hypothesis

The exploitation ecosystems hypothesis (EEH) makes predictions about trophic interactions along gradients of primary productivity. The EEH has been shown to apply to a wide range of terrestrial environments but its applicability to arid environments has received little attention. One reason for this is that arid environments may not satisfy the assumptions of the EEH because dearth of water may limit biological activity in both temporal and spatial contexts. The EEH predicts that herbivore biomass should increase linearly with primary productivity in the absence of predators; but when predators are present herbivore biomass will remain relatively constant due to top down regulation. We tested this prediction in an arid environment using rainfall as a proxy of primary productivity and an index of the abundance of the dominant herbivores (kangaroos Macropus spp.). We compared an index of kangaroo abundance at 18 areas situated along a gradient of mean annual rainfall in areas where a top predator (the dingo Canis lupus dingo) was rare and common. We also explored the relationship between the density of artificial water points (AWPs) and kangaroo abundance to investigate if the resource subsidy provided by AWPs allows kangaroos to persist in high numbers. Consistent with the EEH, kangaroo abundance showed a weak relationship with mean annual rainfall in the presence of dingoes but increased with increasing annual rainfall in the absence of dingoes. The density of AWPs was a poor predictor of kangaroo abundance. Our analysis of macro‐ecological patterns suggests that kangaroo populations are primarily top down regulated in the presence of dingoes, but are bottom up regulated in the absence of dingoes. Our findings provide evidence that top down regulation can prevail over bottom up regulation of herbivore populations in arid ecosystems and highlights the usefulness of the EEH as a predictor of macro‐ecological patterns of species abundance.     

Strength of a Trophic Cascade Between an Apex Predator,Mammalian Herbivore and Grasses in a Desert Ecosystem Does Not Vary with Temporal Fluctuations in Primary Productivity

There has long been debate regarding the primacy of bottom-up and top-down effects as factors shaping ecosystems. The exploitation ecosystems hypothesis (EEH) predicts that predators indirectly benefit plants because their top-down effects limit herbivores’ consumption of plants, and that the strength of trophic cascade increases with increasing primary productivity. However, in arid environments, pulses of primary productivity produced by irregular rainfall events could decouple herbivore–plant and predator–prey dynamics if high conversion efficiency from seed biomass to consumers allows the rapid build-up of consumer populations. Here, we test predictions of the EEH in an arid environment. We measured activity/abundances of dingoes, red kangaroos and grasses, and diet of dingoes, in landscapes where dingoes were culled or not culled over 3 years. Dingo activity was correlated with rainfall, and their tracks were less frequent at culled sites. Kangaroo abundance was greater at sites where dingoes were culled and increased with rainfall in the previous 6 months. Grass cover was greater at sites where dingoes were not culled and increased with rainfall in the previous 3 months. During a period of average rainfall, dingoes primarily consumed rodents and increased their consumption of kangaroos during a period of drier conditions. Our results are consistent with the hypothesis that suppression of an apex predator triggers a trophic cascade, but are at odds with the EEH’s prediction that the magnitude of trophic cascades should increase with primary productivity. Our study demonstrates that temporal fluctuations in primary productivity can have effects on biomasses of plants and consumers which are in many ways analogous to those observed along spatial gradients of primary productivity.     

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.     

Spatial patterns and dynamic responses of arctic food webs corroborate the exploitation ecosystems hypothesis (EEH)

According to the exploitation ecosystems hypothesis (EEH), productive terrestrial ecosystems are characterized by community-level trophic cascades, whereas unproductive ecosystems harbor food-limited grazers, which regulate community-level plant biomass. We tested this hypothesis along arctic-alpine productivity gradients at the Joatka field base, Finnmark, Norway. In unproductive habitats, mammalian predators were absent and plant biomass was constant, whereas herbivore biomass varied, reflecting the productivity of the habitat. In productive habitats, predatory mammals were persistently present and plant biomass varied in space, but herbivore biomass did not. Plant biomass of productive tundra scrublands declined by 40% when vegetation blocks were transferred to predation-free islands. Corresponding transfer to herbivore-free islands triggered an increase in plant biomass. Fertilization of an unproductive tundra heath resulted in a fourfold increase in rodent density and a corresponding increase in winter grazing activity, whereas the total aboveground plant biomass remained unchanged. These results corroborate the predictions of the EEH, implying that the endotherm community and the vegetation of the North European tundra behaves dynamically as if each trophic level consisted of a single population, in spite of local co-occurrence of >20 plant species representing different major taxonomic groups, growth forms, and defensive strategies.     

Apex predator suppression is linked to restructuring of ecosystems via multiple ecological pathways

Removal of apex predators can drive ecological regime shifts owing to compensatory positive and negative population level responses by organisms at lower trophic levels. Despite evidence that apex predators can influence ecosystems though multiple ecological pathways, most studies investigating apex predators’ effects on ecosystems have considered just one pathway in isolation. Here, we provide evidence that lethal control of an apex predator, the dingo Canis dingo, drives shifts in the structure of Australia's tropical‐savannah ecosystems. We compared mammal assemblages and understorey structure at seven paired‐sites. Each site comprised an area where people poisoned dingoes and an area without dingo control. The effects of dingo control on mammals scaled with body size. Where dingoes were poisoned, we found greater activity of herbivorous macropods and feral cats, a mesopredator, but sparser understorey vegetation and lower abundances of native rodents. Our study suggests that ecological cascades arising from apex predators’ suppressive effects on herbivores and mesopredators occur simultaneously. Concordant effects of dingo removal across tropical‐savannah, forest and desert biomes suggest that dingoes once exerted ubiquitous top–down effects across Australia and provides support for calls that top–down forcing should be considered a fundamental process governing ecosystem structure.     

From bottom-up to top-down control of invertebrate herbivores in a retrogressive chronosequence

In the long-term absence of disturbance, ecosystems often enter a decline or retrogressive phase which leads to reductions in primary productivity, plant biomass, nutrient cycling and foliar quality. However, the consequences of ecosystem retrogression for higher trophic levels such as herbivores and predators, are less clear. Using a post-fire forested island-chronosequence across which retrogression occurs, we provide evidence that nutrient availability strongly controls invertebrate herbivore biomass when predators are few, but that there is a switch from bottom-up to top-down control when predators are common. This trophic flip in herbivore control probably arises because invertebrate predators respond to alternative energy channels from the adjacent aquatic matrix, which were independent of terrestrial plant biomass. Our results suggest that effects of nutrient limitation resulting from ecosystem retrogression on trophic cascades are modified by nutrient-independent variation in predator abundance, and this calls for a more holistic approach to trophic ecology to better understand herbivore effects on plant communities.     

Are dingoes a trophic regulator in arid Australia? A comparison of mammal communities on either side of the dingo fence

The direct and indirect interactions that large mammalian carnivores have with other species can have far‐reaching effects on ecosystems. In recent years there has been growing interest in the role that Australia's largest terrestrial predator, the dingo, may have in structuring ecosystems. In this study we investigate the effect of dingo exclusion on mammal communities, by comparing mammal assemblages where dingoes were present and absent. The study was replicated at three locations spanning 300 km in the Strzelecki Desert. We hypothesized that larger species of mammal subject to direct interactions with dingoes should increase in abundance in the absence of dingoes while smaller species subject to predation by mesopredators should decrease in abundance because of increased mesopredator impact. There were stark differences in mammal assemblages on either side of the dingo fence and the effect of dingoes appeared to scale with body size. Kangaroos and red foxes were more abundant in the absence of dingoes while Rabbits and the Dusky Hopping‐mouse Notomys fuscus were less abundant where dingoes were absent, suggesting that they may benefit from lower red fox numbers in the presence of dingoes. Feral cats and dunnarts (Sminthopsis spp.) did not respond to dingo exclusion. Our study provides evidence that dingoes do structure mammal communities in arid Australia; however, dingo exclusion is also associated with a suite of land use factors, including sheep grazing and kangaroo harvesting that may also be expected to influence kangaroo and red fox populations. Maintaining or restoring populations of dingoes may be useful strategies to mitigate the impacts of mesopredators and overgrazing by herbivores.     

Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades

Single trophic‐level studies of the relationship between biodiversity and ecosystem functioning highlight the importance of mechanisms such as resource partitioning, facilitation, and sampling effect. In a multi‐trophic context, trophic interactions such as intraguild predation may also be an important mediator of this relationship. Using a salt‐marsh food web, we investigated the interactive effects of predator species richness (one to three species) and trophic composition (strict predators, intraguild predators, or a mixture of the two) on ecosystem functions such as prey suppression and primary production via trophic cascades. We found that the trophic composition of the predator assemblage determined the impact of increasing predator species richness on the occurrence of trophic cascades. In addition, increasing the proportion of intraguild predator species present diminished herbivore suppression and reduced primary productivity. Therefore, trophic composition of the predator assemblage can play an important role in determining the nature of the relationship between predator diversity and ecosystem function.     

Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades

The ability of predators to elicit a trophic cascade with positive impacts on primary productivity may depend on the complexity of the habitat where the players interact. In structurally-simple habitats, trophic interactions among predators, such as intraguild predation, can diminish the cascading effects of a predator community on herbivore suppression and plant biomass. However, complex habitats may provide a spatial refuge for predators from intraguild predation, enhance the collective ability of multiple predator species to limit herbivore populations, and thus increase the overall strength of a trophic cascade on plant productivity. Using the community of terrestrial arthropods inhabiting Atlantic coastal salt marshes, this study examined the impact of predation by an assemblage of predators containing Pardosa wolf spiders, Grammonota web-building spiders, and Tytthus mirid bugs on herbivore populations (Prokelisia planthoppers) and on the biomass of Spartina cordgrass in simple (thatch-free) and complex (thatch-rich) vegetation. We found that complex-structured habitats enhanced planthopper suppression by the predator assemblage because habitats with thatch provided a refuge for predators from intraguild predation including cannibalism. The ultimate result of reduced antagonistic interactions among predator species and increased prey suppression was enhanced conductance of predator effects through the food web to positively impact primary producers. Behavioral observations in the laboratory confirmed that intraguild predation occurred in the simple, thatch-free habitat, and that the encounter and capture rates of intraguild prey by intraguild predators was diminished in the presence of thatch. On the other hand, there was no effect of thatch on the encounter and capture rates of herbivores by predators. The differential impact of thatch on the susceptibility of intraguild and herbivorous prey resulted in enhanced top-down effects in the thatch-rich habitat. Therefore, changes in habitat complexity can enhance trophic cascades by predator communities and positively impact productivity by moderating negative interactions among predators.     

Functional responses of an apex predator and a mesopredator to an invading ungulate: Dingoes,red foxes and sambar deer in south‐east Australia

Biological invasions by large herbivores involve the establishment of novel interactions with the receiving mammalian carnivore community, but understanding these interactions is difficult due to the large spatiotemporal scales at which such dynamics would occur. We quantified the functional responses of a native apex predator (the dingo (Canis familiaris), which includes wild dogs and their hybrids) and a non‐native mesopredator (red fox; Vulpes vulpes) to an invading non‐native ungulate (sambar deer; Cervus unicolor) in Australia. We predicted that the apex predator would exhibit a stronger functional response to increasing sambar deer abundance than the mesopredator. We used a state–space model to link two 30‐year time series: (i) sambar deer abundance (hunter catch‐per‐unit‐effort); and (ii) percentages of sambar deer in dingo (N = 4531) and fox (N = 5002) scats. Sambar deer abundance increased over fourfold during 1984?2013. The percentages of sambar deer in dingo and fox scats increased during this 30‐year period, from nil in both species in 1984 to 8.2% in dingoes and 0.5% in foxes in 2013. Dingoes exhibited a much stronger functional response to increasing sambar deer abundance than foxes. The prediction that invading deer would be utilized more by the apex predator than by the mesopredator was therefore supported. The increasing abundance of sambar deer during the period 1984?2013 provided an increasingly important food source for dingoes. In contrast, the smaller red fox utilized sambar deer much less. Our study demonstrates that prey enrichment can be an important consequence of large herbivore invasions and that the effect varies predictably with the trophic position of the mammalian carnivores in the receiving community.     

Predator–prey interactions in a grassland food chain vary with temperature and food quality

Because species interactions are often context‐dependent, abiotic factors such as temperature and biotic factors such as food quality may alter species interactions with potential consequences to ecosystem structure and function. For example, altered predator–prey interactions may influence the dynamics of trophic cascades, affecting net primary production. In a three‐year field experiment, we manipulated a plant–grasshopper–spider food chain in mesic tallgrass prairie to investigate the effects of temperature and food quality on grasshopper performance, and to understand the direct and indirect tritrophic interactions that contribute to trophic cascades. Because spiders are active at cooler temperatures than grasshoppers in our system, we hypothesized that predator effects would be strongest in cooled treatments, and weakest in warmed treatments. Grasshopper spider interactions were highly context‐dependent and varied significantly with food quality, temperature treatment and year. Spiders most often reduced grasshopper survival in the cooled and ambient temperature treatments, but had little to no effect on grasshopper survival in the warmed treatments, as hypothesized. In some years, plants compensated for grasshopper herbivory and trophic cascades were not observed despite significant effects of predators on grasshopper survival. However, in the year they were observed, trophic cascades only occurred in cooled treatments where predator effects on grasshoppers were strongest. Predicting ecosystem responses to climate change will require an understanding of how temperature influences species interactions. Our results demonstrate that changes in daily temperature regimes can alter predator–prey interactions among arthropods with consequences for ecosystem processes such as primary production and the relative importance of top–down and bottom–up processes.     

Terrestrial trophic cascades: how much do they trickle?

Although more consensus is now emerging on the magnitude and frequency of cascading trophic effects in aquatic communities, the debate over their terrestrial counterparts continues. We used meta-analysis to analyze field experiments on trophic cascades in terrestrial arthropod-dominated food webs to evaluate the overall magnitude of trophic cascades and conditions affecting their occurrence and strength. We found extensive support for the presence of trophic cascades in terrestrial communities. In the majority of experiments, predator removal led to increased densities of herbivorous insects and higher levels of plant damage. Cascades in which removing predators led to decreased herbivory also were detected but were less frequent and weaker, suggesting a predominantly three-trophic-level behavior of arthropod-dominated terrestrial food webs. Despite the clear evidence that cascades often decreased plant damage, residual effects of predation produced either no or only minimal changes in overall plant biomass. Agricultural systems and natural communities exhibited similarly strong effects of predation on herbivore abundance. However, resulting effects on plant damage and community-wide effects of trophic cascades on plant biomass usually were highly variable, and only in the managed agricultural systems did predators occasionally have strong indirect effects on plant biomass. Our meta-analysis suggests that the effects of trophic cascades on the biomass of primary producers are weaker in terrestrial than aquatic food webs.     

Herbivore species richness, composition and community structure mediate predator richness effects and top-down control of herbivore biomass

Changes in predator species richness can have important consequences for ecosystem functioning at multiple trophic levels, but these effects are variable and depend on the ecological context in addition to the properties of predators themselves. Here, we report an experimental study to test how species identity, community attributes, and community structure at the herbivore level moderate the effects of predator richness on ecosystem functioning. Using mesocosms containing predatory insects and aphid prey, we independently manipulated species richness at both predator and herbivore trophic levels. Community structure was also manipulated by changing the distribution of herbivore species across two plant species. Predator species richness and herbivore species richness were found to negatively interact to influence predator biomass accumulation, an effect which is hypothesised to be due to the breakdown of functional complementarity among predators in species-rich herbivore assemblages. The strength of predator suppression of herbivore biomass decreased as herbivore species richness and distribution across host plants increased, and positive predator richness effects on herbivore biomass suppression were only observed in herbivore assemblages of relatively low productivity. In summary, the study shows that the species richness, productivity and host plant distribution of prey communities can all moderate the general influence of predators and the emergence of predator species richness effects on ecosystem functioning.     

Temporal and spatial trends in the abundances of an apex predator,introduced mesopredator and ground-nesting bird are consistent with the mesopredator release hypothesis

Apex predator extirpation has been identified as a key driver of biodiversity losses. The mesopredator release hypothesis (MRH) predicts that reduced abundance of apex predators results in an increase in the abundance and predatory impact of mesopredators. Here we test predictions made according to the MRH that an apex predator, the dingo (Canis dingo), benefits a small ground-nesting bird, the little button-quail (Turnix velox), by reducing the abundance of introduced mesopredators, the red fox (Vulpes vulpes) and feral cat (Felis catus). We also examined an alternative hypothesis that herbivore grazing negatively affects little button-quail abundance by reducing ground cover. To test our predictions we compared dingo, mesopredator, quail, herbivore and ground cover abundances and predator diets over a 25 month period and across a 10,000 km² region encompassing areas where dingoes were common and rare, pastoral properties, and conservation reserves. Little button-quails were primarily observed where dingoes were common and foxes rare. Cats were detected at low numbers throughout the sample area irrespective of the index abundance of little button-quails, dingoes or foxes. Birds occurred less frequently in dingo than fox or cat scats. Ground cover and herbivore grazing activity were poor correlates of little button-quail abundance. Our results are consistent with the hypothesis that apex predators’ mesopredator-suppressive effects translate to population-level benefits for a ground-nesting bird. Positive associations between the abundances of dingoes and small-prey species suggests that positive management of dingoes could be incorporated into broad-scale biodiversity conservation programs as a strategy to alleviate the predatory impacts of foxes.     

Spatial variation in vegetation damage relative to primary productivity,small rodent abundance and predation

The relative importance of top‐down and bottom‐up mechanisms in shaping community structure is still a highly controversial topic in ecology. Predatory top‐down control of herbivores is thought to relax herbivore impact on the vegetation through trophic cascades. However, trophic cascades may be weak in terrestrial systems as the complexity of food webs makes responses harder to predict. Alternatively, top‐down control prevails, but the top‐level (predator or herbivore) changes according to productivity levels. Here we show how spatial variation in the occurrence of herbivores (lemmings and voles) and their predators (mustelids and foxes) relates with grazing damage in landscapes with different net primary productivity, generating two and three trophic level communities, during the 2007 rodent peak in northern Norway. Lemmings were most abundant on the unproductive high‐altitude tundra, where few predators were present and the impact of herbivores on vegetation was strong. Voles were most common on a productive, south facing slope, where numerous predators were present, and the impacts of herbivores on vegetation were weak. The impact of herbivores on the vegetation was strong only when predators were not present, and this cannot be explained by between‐habitat differences in the abundance of plant functional groups. We thus conclude that predators influence the plant community via a trophic cascade in a spatial pattern that support the exploitation ecosystems hypothesis. The responses to grazing also differed between plant functional groups, with implications for short and long‐term consequences for plant communities.     

A cross-ecosystem comparison of the strength of trophic cascades

Although trophic cascades (indirect effects of predators on plants via herbivores) occur in a wide variety of food webs, the magnitudes of their effects are often quite variable. We compared the responses of herbivore and plant communities to predator manipulations in 102 field experiments in six different ecosystems: lentic (lake and pond), marine, and stream benthos, lentic and marine plankton, and terrestrial (grasslands and agricultural fields). Predator effects varied considerably among systems and were strongest in lentic and marine benthos and weakest in marine plankton and terrestrial food webs. Predator effects on herbivores were generally larger and more variable than on plants, suggesting that cascades often become attenuated at the plant–herbivore interface. Top‐down control of plant biomass was stronger in water than on land; however, the differences among the five aquatic food webs were as great as those between wet and dry systems.     

Death by sex in an Australian icon: a continent‐wide survey reveals extensive hybridization between dingoes and domestic dogs

Hybridization between domesticated animals and their wild counterparts can disrupt adaptive gene combinations, reduce genetic diversity, extinguish wild populations and change ecosystem function. The dingo is a free‐ranging dog that is an iconic apex predator and distributed throughout most of mainland Australia. Dingoes readily hybridize with domestic dogs, and in many Australian jurisdictions, distinct management strategies are dictated by hybrid status. Yet, the magnitude and spatial extent of domestic dog–dingo hybridization is poorly characterized. To address this, we performed a continent‐wide analysis of hybridization throughout Australia based on 24 locus microsatellite DNA genotypes from 3637 free‐ranging dogs. Although 46% of all free‐ranging dogs were classified as pure dingoes, all regions exhibited some hybridization, and the magnitude varied substantially. The southeast of Australia was highly admixed, with 99% of animals being hybrids or feral domestic dogs, whereas only 13% of the animals from remote central Australia were hybrids. Almost all free‐ranging dogs had some dingo ancestry, indicating that domestic dogs could have poor survivorship in nonurban Australian environments. Overall, wild pure dingoes remain the dominant predator over most of Australia, but the speed and extent to which hybridization has occurred in the approximately 220 years since the first introduction of domestic dogs indicate that the process may soon threaten the persistence of pure dingoes.     

The distribution of deer biomass in North America supports the hypothesis of exploitation ecosystems

The hypothesis of exploitation ecosystems (EEH) predicts that, along a productivity gradient in terrestrial environments, predators will regulate herbivores at a relatively constant density whenever primary productivity exceeds 700 g m⁻² y⁻¹; under this threshold, or if predators are absent, forage production determines herbivore density. I tested EEH using the pattern of deer biomass distribution over North America, the dominant family of large herbivores. Deer biomass increased from the High Arctic to the north of the boreal forest and remained in the same range southward within the gray wolf range; for the same latitude, deer biomass increased by a factor of 5 in the absence of wolves. South of the wolf range, there existed a clear relationship between actual evapotranspiration, a proxy of primary productivity, and deer biomass. Highest deer densities occurred in the south-east of the continent where only white-tailed deer are present. The observed pattern lends support to EEH and suggests that the removal of large predators in southern North America may have imposed an unprecedented pressure on plants eaten by deer.     

Variation of prey responses to cues from a mesopredator and an apex predator

Detection and avoidance of predator cues can be costly, so it is important for prey to balance the benefits of gaining food against the costs of avoiding predators. Balancing these factors becomes more complicated when prey are threatened by more than one type of predator. Hence, the ability to recognize species‐specific predator odours and prioritize behaviours according to the level of risk is essential for survival. We investigated how rock rats, Zyzomys spp. modify their foraging behaviour and giving‐up density (GUD) in the presence of an apex predator, the dingo Canis dingo, a mesopredator, the northern quoll Dasyurus hallucatus, a herbivore, the rock wallaby Petrogale brachyotis as a pungency control and water as a procedural control. Both dingoes and quolls consume rock rats, but because quolls can enter small crevices inhabited by rock rats, they pose a greater threat to rock rats than dingoes. Rock rats demonstrated a stronger avoidance to quoll odour than dingo odour, and no avoidance of the pungency control (rock wallaby) and the procedural control (water). GUD values declined significantly over the duration of the study, but did not differ between odour treatments. Our results support the hypothesis that prey vary behaviour according to perceived predator threat, and show stronger responses to potentially more dangerous predators.