Humans are increasingly subsidizing and altering natural food webs via changes to nutrient cycling and productivity. Where human trophic subsidies are concentrated and persistent within natural environments, their consumption could have complex consequences for wild animals through altering habitat preferences, phenotypes and fitness attributes that influence population dynamics. Human trophic subsidies conceptually create both costs and benefits for animals that receive increased calorific and altered nutritional inputs. Here, we evaluated the effects of a common terrestrial human trophic subsidies, human food refuse, on population and phenotypic (comprising morphological and physiological health indices) parameters of a large predatory lizard (∼2 m length), the lace monitor (Varanus varius), in southern Australia by comparison with individuals not receiving human trophic subsidies. At human trophic subsidies sites, lizards were significantly more abundant and their sex ratio highly male biased compared to control sites in natural forest. Human trophic subsidies recipient lizards were significantly longer, heavier and in much greater body condition. Blood parasites were significantly lower in human trophic subsidies lizards. Collectively, our results imply that human trophic subsidized sites were especially attractive to adult male lace monitors and had large phenotypic effects. However, we cannot rule out that the male-biased aggregations of large monitors at human trophic subsidized sites could lead to reductions in reproductive fitness, through mate competition and offspring survival, and through greater exposure of eggs and juveniles to predation. These possibilities could have negative population consequences. Aggregations of these large predators may also have flow on effects to surrounding food web dynamics through elevated predation levels. Given that flux of energy and nutrients into food webs is central to the regulation of populations and their communities, we advocate further studies of human trophic subsidies be undertaken to evaluate the potentially large ecological implications of this significant human environmental alteration.

Funding: Funding for research was provided by Zoos Victoria as part of the “forest for life” project. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2012 Jessop et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

Humans exert an incredible array of ecological and evolutionary influences on wild animals and their ecosystems [1]. For example, production and loss (e.g. waste) of human food resources in urban, periurban, agricultural and natural landscapes represents an emergent and growing trophic subsidy for associated food webs [2]. Human trophic subsidies include any direct provision of food (i.e. energy) or associated nutrient alteration which modifies the nutritional landscape of animals [2]. For example, the aesthetic enjoyment of feeding birds leads to the introduction of a massive food subsidy to wild animals; 43 and 75% of households in the US and UK, respectively, feed birds [3], [4]. Given that the flux of energy and nutrients into food webs is a central process underpinning the regulation of animal populations and ecological communities [5], [6], human trophic subsidies may drive changes at the individual level which have community level consequences [7], [8], [9].

At the heart of nutrient and energy flows in food webs are the immediate functional consequences for individual consumers. Native animals that consume human trophic subsidies receive nutrition that may differ markedly in energy, nutrient composition and quality from their natural diet. Thus, via nutrition alone, human trophic subsidies could cause novel, complex and even antagonistic fitness effects for native animals [10] (Figure 1). Modified macro- (i.e. protein, fat, carbohydrates) or micro-nutrient intake might alter phenotypic traits that improve fitness, such as increasing growth rates, fat stores, reproductive effort and immunocompetence [9], [11]. Such responses could lead to higher fitness phenotypes and dramatic shifts in localized population parameters (e.g. survival, reproductive output) and in turn positively influence population growth rates. Hence, human trophic subsidies modified habitats could act as population sources [9], [12], [13].

Alternately, and analogous to the human obesity epidemic, costs may arise if human trophic subsidies provides excessive calorific intake and imbalanced nutrition causing metabolic syndromes and nutritional disorders [10], [14]. Additionally ingestion of detrimental food additives (e.g. chemicals/hormones) and exposure to novel pathogens harboured in food [15] could further increase costs to animal recipients of human trophic subsidies. Human trophic subsidies -mediated phenotypic responses are likely to be further influenced by population density dependent effects. As many sources of human trophic subsidies are spatially discreet, they serve as high density population aggregation areas, relative to low density populations inhabiting adjacent natural environs [13], [16]. human trophic subsidies induced aggregation could exacerbate social conflict and territoriality [17], skew sex ratios [18], increase parasite/disease transmission [11], elevate stress levels, decrease immunocompetence and ultimately lead to reduced individual fitness, either through decreased reproductive success or elevated mortality rates through higher predation risk. Thus, spatially discrete human trophic subsidies in natural environments could drive ecological traps, resulting in fitness costs to individuals and demographic changes in populations [19]. Robertson and Hutto [20] propose that ecological traps arise from habitat alteration that operates in by increasing the attractiveness of an environment by enhancing the set of cues that animals recognise as beneficial and concurrently decreasing the suitability of a habitat. Conceivably, animals could prefer human trophic subsidized - habitats over natural habitats as they mimic a strong ecological cue (i.e. high food availability) which typically signals the presence of a good quality natural habitat [13]. Human trophic subsidies -modified habitats have the potential to modify other ecological processes and reduce the fitness of resident animals. Under such circumstances, human trophic subsidies -modified habitats would acts as ecological traps, with consequences at the individual level ultimately leading to reduced local fitness and in the absence of sufficient recruitment from outside immigration cause negative population growth. A good example of an ecological trap is that of red necked grebes (Podiceps grisegena) foraging in a large scale carp (Cyprinus carpio) aquaculture venture [21]. Here adult grebes pending their choice of carp size within particular fish rearing ponds, where fish are raised in discreet size classes, can impact offspring survival. If adult birds choose to forage at ponds containing medium sized carp which grow to become too large during the course of egg development and incubation, it denies young birds a food supply causing high chick mortality, even though the adult condition and survival is high [21].Human trophic subsidies are common in natural landscapes, but their effects on individuals are poorly understood [16], [19]–[21]. Here, we evaluated the effects of human trophic subsidies on a common Australian predator, the Lace Monitor (Varanus varius). These large lizards (∼2 m length) exploit multiple sources of human trophic subsidies from agriculture (carrion from live stock or introduced prey foraging on pasture e.g. rabbits) and human food waste deposited in refuse tips or accessible in recreational wilderness areas (e.g. food from campers and hikers) (Figure 1A). Further, given that human trophic subsidies are accessible at spatially confined point-sources nested within natural landscapes, they provide good natural experiments to examine the effects of human modified nutritional input which are not confounded by other major landscape changes that could influence this predator’s ecology.

Human trophic subsidies could influence these large predatory lizards via two key pathways that ultimately influence their population abundance via changes in demographic processes (Figure 2). The first pathway considers phenotypic responses of lizards to human trophic subsidies. Pending the quantity and quality of macro- and mirco-nutrients ingested, we would expect diverse changes in multiple morphological and physiological parameters. For example, spatial variation in ungulate prey resources in Komodo dragons (Varanus komodoensis) is associated with ∼ fourfold differences in maximum body mass [22], [23]. Hence, greater protein availability in human trophic subsidies -modified habitats may enable lizards to grow faster and larger relative to lizards in natural habitats. Similarly, for many animals, variation in body condition is often associated with large individual differences in immunocompetence, which underpins parasite resistance and regulates both basal and maximal endocrine stress levels [24]–[26].

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larger image TIFF original image Download: Figure 1. Figure (A) depicts potential sources of human mediated trophic subsides available to Lace Monitors in the general vicinity of the study site (rectangle) in southern Australia (inset). These include refuse tips and farms where domesticated animals and introduced prey (eg. rabbits) could increase food availability to lizards above, and with differenct consequences, than that sourced in natural forests. Figure (B) depicts the two refuse tips (black squares) and corresponding control sites (black polygons with green dots representing individual lizard capture locations) that were evaluated to assess the population and phenotypic consequences of human trophic subsidies on Lace Monitor lizards in southern Australia. Symbols purely represent location and not scale. https://doi.org/10.1371/journal.pone.0034069.g001

The second pathway through which human trophic subsidies could affect Lace Monitors is via altering realized or perceived habitat quality cues. Increased availability of protein-rich food is likely to attract Lace Monitors, who routinely consume both live prey and scavenge for carrion. Thus, human trophic subsidies sites could continuously recruit lizards from adjacent habitats. However, the net consequence of human trophic subsidies recruitment could be either positive or negative for the local demography pending how individual lizards interact with conspecifics. For example, prolonged focal supplementary feeding of Komodo dragons to enhance tourism (i.e. ease of viewing of this large predator) increased local population densities of lizards by nearly sixfold relative to adjacent natural areas [27]. However, such aggregations were dominated by large male lizards (the larger sex) that skewed the operational sex ratio relative to natural areas. A strong body of research and theory indicate that increased competition for mates leads to skewed or reduced reproductive success for males [28]–[30]. A habitat-related cost of supplementary feeding via human trophic subsidies to lace monitors could also result in shifts to operational sex ratios.

To evaluate these potential effects of human trophic subsidies, via human food refuse, on Lace Monitors in Southern Australia, we used integrative methods to assess both population (counts and sex ratio) and phenotypic effects (morphology, metabolic enzymes, endocrine stress state, plasma biochemistry and parasite load).