Invader immunology: invasion history alters immune system function in cane toads (Rhinella marina) in tropical Australia

Because an individual's investment into the immune system may modify its dispersal rate, immune function may evolve rapidly in an invader. We collected cane toads (Rhinella marina) from sites spanning their 75‐year invasion history in Australia, bred them, and raised their progeny in standard conditions. Evolved shifts in immune function should manifest as differences in immune responses among the progeny of parents collected in different locations. Parental location did not affect the offspring's cell‐mediated immune response or stress response, but blood from the offspring of invasion‐front toads had more neutrophils, and was more effective at phagocytosis and killing bacteria. These latter measures of immune function are negatively correlated with rate of dispersal in free‐ranging toads. Our results suggest that the invasion of tropical Australia by cane toads has resulted in rapid genetically based compensatory shifts in the aspects of immune responses that are most compromised by the rigours of long‐distance dispersal.     

Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone

Invasive species often encounter environmental conditions well outside those found in their native geographic ranges, and thus provide ideal model systems with which to explore responses to novel abiotic challenges. Within Australia, the invasive cane toad Rhinella marina has colonized areas that are considerably more arid than those found within its native range. Has the colonization of these novel environments been accompanied by shifts in physiology and/or locomotor performance? We measured rates of evaporative water loss, water gain, and effects of desiccation on locomotor performance of cane toads from two invasion fronts: one mesic (the wet‐dry tropics) and one arid (the semi‐desert). The two populations diverged substantially. Contrary to intuition (but consistent with intra‐specific comparisons between other toad populations from mesic vs arid areas), rates of evaporative water loss were lower (not higher) in toads from the mesic population. However, arid‐zone toads gained water more rapidly through their ventral surfaces, and rates of water loss and gain were highly correlated within individual toads from the arid‐zone population. Rates of water exchange in laboratory‐acclimated toads from the semi‐arid zone did not differ from those of free‐ranging conspecifics from the same population, suggesting that divergences between mesic and semi‐arid toads reflect genetic changes that have occurred during the species’ Australian invasion. Mesic and semi‐arid toads showed similar locomotor performance (endurance, distance per hop) when fully hydrated, but locomotor performance declined much more rapidly with desiccation in the mesic toads. Thus, within the short (decades‐long) timespan of the cane toad's Australian invasion, there has been substantial population divergence in the ability to withstand desiccating conditions. If we are to accurately predict the distributions (and hence impacts) of invading organisms, we will need to include adaptation potential in risk assessment schemes.     

The accelerating anuran: evolution of locomotor performance in cane toads (Rhinella marina,Bufonidae) at an invasion front

As is common in biological invasions, the rate at which cane toads (Rhinella marina) have spread across tropical Australia has accelerated through time. Individuals at the invasion front travel further than range-core conspecifics and exhibit distinctive morphologies that may facilitate rapid dispersal. However, the links between these morphological changes and locomotor performance have not been clearly documented. We used raceway trials and high-speed videography to document locomotor traits (e.g. hop distances, heights, velocities, and angles of take-off and landing) of toads from range-core and invasion-front populations. Locomotor performance varied geographically, and this variation in performance was linked to morphological features that have evolved during the toads'' Australian invasion. Geographical variation in morphology and locomotor ability was evident not only in wild-caught animals, but also in individuals that had been raised under standardized conditions in captivity. Our data thus support the hypothesis that the cane toad''s invasion across Australia has generated rapid evolutionary shifts in dispersal-relevant performance traits, and that these differences in performance are linked to concurrent shifts in morphological traits.     

The impact of invasive cane toads on native wildlife in southern Australia

Commonly, invaders have different impacts in different places. The spread of cane toads (Rhinella marina: Bufonidae) has been devastating for native fauna in tropical Australia, but the toads' impact remains unstudied in temperate‐zone Australia. We surveyed habitat characteristics and fauna in campgrounds along the central eastern coast of Australia, in eight sites that have been colonized by cane toads and another eight that have not. The presence of cane toads was associated with lower faunal abundance and species richness, and a difference in species composition. Populations of three species of large lizards (land mullets Bellatorias major, eastern water dragons Intellagama lesueurii, and lace monitors Varanus varius) and a snake (red‐bellied blacksnake Pseudechis porphyriacus) were lower (by 84 to 100%) in areas with toads. The scarcity of scavenging lace monitors in toad‐invaded areas translated into a 52% decrease in rates of carrion removal (based on camera traps at bait stations) and an increase (by 61%) in numbers of brush turkeys (Alectura lathami). The invasion of cane toads through temperate‐zone Australia appears to have reduced populations of at least four anurophagous predators, facilitated other taxa, and decreased rates of scavenging. Our data identify a paradox: The impacts of cane toads are at least as devastating in southern Australia as in the tropics, yet we know far more about toad invasion in the sparsely populated wilderness areas of tropical Australia than in the densely populated southeastern seaboard.     

The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front

At the edge of a biological invasion, evolutionary processes (spatial sorting, natural selection) often drive increases in dispersal. Although numerous traits influence an individual''s displacement (e.g. speed, stamina), one of the most important is path straightness. A straight (i.e. highly correlated) path strongly enhances overall dispersal rate relative to time and energetic cost. Thus, we predict that, if path straightness has a genetic basis, organisms in the invasion vanguard will exhibit straighter paths than those following behind. Our studies on invasive cane toads (Rhinella marina) in tropical Australia clearly support this prediction. Radio-tracking of field-collected toads at a single site showed that path straightness steadily decreased over the first 10 years post-invasion. Consistent with an evolved (genetic) basis to that behavioural shift, path straightness of toads reared under common garden conditions varied according to the location of their parents'' origin. Offspring produced by toads from the invasion vanguard followed straighter paths than did those produced by parents from long-established populations. At the individual level, offspring exhibited similar path straightness to their parents. The dramatic acceleration of the cane toad invasion through tropical Australia has been driven, in part, by the evolution of a behavioural tendency towards dispersing in a straight line.     

Athletic anurans: the impact of morphology,ecology and evolution on climbing ability in invasive cane toads

Although primarily terrestrial, cane toads (Rhinella marina) sometimes climb near‐vertical surfaces (tree‐trunks, cliffs, fences) during foraging or dispersal activities. We scored climbing ability (in laboratory trials) of 288 cane toads from four regions in Australia, plus two sites on the island of Hawai'i. We found strong divergence in climbing ability associated not only with sex and relative limb length, but also population of origin. Within each population, longer‐limbed individuals (and hence, males rather than females) were better climbers, although the geographical divergence in climbing ability remained significant even when sex and limb length were included in multivariate regression models. The geographical difference in climbing ability (but not morphology) disappeared when the progeny were raised in captivity under identical conditions, without climbing opportunities. Although influenced by morphology, climbing ability in wild‐caught cane toads appears to be driven primarily by local environmental conditions that facilitate and/or reward arboreal activity.     

Behavioural tactics used by invasive cane toads (Rhinella marina) to exploit apiaries in Australia

Behavioural flexibility plays a key role in facilitating the ability of invasive species to exploit anthropogenically‐created resources. In Australia, invasive cane toads (Rhinella marina) often gather around commercial beehives (apiaries), whereas native frogs do not. To document how toads use this resource, we spool‐tracked cane toads in areas containing beehives and in adjacent natural habitat without beehives, conducted standardized observations of toad feeding behaviour, and ran prey‐manipulation trials to compare the responses of cane toads versus native frogs to honeybees as potential prey. Toads feeding around beehives travelled shorter distances per night, and hence used different microhabitats, than did toads from nearby control sites without beehives. The toads consumed live bees from the hive entrance (rather than dead bees from the ground), often climbing on top of one another to gain access to the hive entrance. Prey manipulation trials confirm that bee movement is the critical stimulus that elicits the toads’ feeding response; and in standardized trials, native frogs consumed bees less frequently than did toads. In summary, cane toads flexibly modify their movements, foraging behaviour and dietary composition to exploit the nutritional opportunities created by commercial beehives, whereas native anurans do not.     

Sublethal costs associated with the consumption of toxic prey by snakes

Costs of plant defences to herbivores have been extensively studied, but costs of chemical defences to carnivores are less well understood. We examine the costs to Australian keelback snakes (Tropidonophis mairii, Gray 1841) of consuming cane toads (Bufo[Rhinella]marinus Linnaeus 1758). Cane toads (an invasive species in Australia) are highly toxic. Although keelbacks can consume toads without dying (unlike most Australian snakes), we show that cane toads are poor quality prey for keelbacks. Toads are of low net nutritional value, take longer to consume than do native frogs and reduce the snake's locomotor performance for up to 6 h after ingestion of a meal. These latter effects may increase a snake's vulnerability to predation. Nutritional content of vertebrate prey is not the only factor driving the evolution of foraging behaviour; other more subtle costs, such as risk of predation, may be widespread.     

Differences in developmental strategies between long‐settled and invasion‐front populations of the cane toad in Australia

Phenotypic plasticity can enhance a species’ ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long‐colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion‐vanguard populations to exhibit less phenotypic plasticity than range‐core populations. Compared to clutches from long‐colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade‐off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet‐hedging) or instead are driven by geographic variation in genetic quality or parental effects.     

Moving south: effects of water temperatures on the larval development of invasive cane toads (Rhinella marina) in cool‐temperate Australia

The distributional limits of many ectothermic species are set by thermal tolerances of early‐developmental stages in the life history; embryos and larvae often are less able to buffer environmental variation than are conspecific adults. In pond‐breeding amphibians, for example, cold water may constrain viability of eggs and larvae, even if adults can find suitable thermal conditions in terrestrial niches. Invasive species provide robust model systems for exploring these questions, because we can quantify thermal challenges at the expanding range edge (from field surveys) and larval responses to thermal conditions (in the laboratory). Our studies on invasive cane toads (Rhinella marina) at the southern (cool‐climate) edge of their expanding range in Australia show that available ponds often average around 20°C during the breeding period, 10°C lower than in many areas of the toads’ native range, or in the Australian tropics. Our laboratory experiments showed that cane toad eggs and larvae cannot develop successfully at 16°C, but hatching success and larval survival rates were higher at 20°C than in warmer conditions. Lower temperatures slowed growth rates, increasing the duration of tadpole life, but also increased metamorph body mass. Water temperature also influenced metamorph body shape (high temperatures reduced relative limb length, head width, and body mass) and locomotor performance (increased speed from intermediate temperatures, longer hops from high temperatures). In combination with previous studies, our data suggest that lower water temperatures may enhance rather than reduce recruitment of cane toads, at least in areas where pond temperatures reach or exceed 20°C. That condition is fulfilled over a wide area of southern Australia, suggesting that the continuing expansion of this invasive species is unlikely to be curtailed by the impacts of relatively low water temperatures on the viability of early life‐history stages.     

Far from home: responses of an American predator species to an American prey species in a jointly invaded area of Australia

Far from their native ranges in the Americas, two invasive species come into contact in Australian waterbodies. Cane toads (Rhinella marina) fatally poison many anurophagous predators, whereas eastern mosquito fish (Gambusia holbrooki) voraciously consume anuran larvae. As cane toads spread south along Australia’s east coast, they are colonizing areas where mosquito fish are abundant. What happens when these two American invaders encounter each other in Australia? We tested the responses to toad tadpoles of mosquito fish from populations that were sympatric versus allopatric with cane toads. Toad-sympatric fish generally ignored toad tadpoles. Toad-allopatric fish initially consumed a few tadpoles, but rapidly developed an aversion to these toxic prey items. The laboratory-reared progeny of toad-allopatric fishes were more likely to approach toad tadpoles than were the offspring of toad-sympatric fishes, but the two groups learned toad-avoidance at similar rates. Thus, mosquito fish show an innate aversion to cane toad tadpoles (perhaps reflecting coevolution with North American bufonid taxa), as well as an ability to rapidly learn taste-aversion. Our comparisons among populations suggest that several decades of toad-free existence in Australia caused a decline in the fishes’ innate (heritable) aversion to toads, but did not affect the fishes’ capacity to learn toad-avoidance after an initial exposure. Any impact of mosquito fish on cane toads thus is likely to be transitory. The rapid (<100-year) time frame of these shifts (the initial weakening of the fishes’ response during toad-allopatry, and its recovery after secondary contact) emphasizes the dynamic nature of faunal responses during biological invasions, and the interplay between adaptation and phenotypic plasticity.     

Not such silly sausages: Evidence suggests northern quolls exhibit aversion to toads after training with toad sausages

The invasion of toxic cane toads (Rhinella marina) is a major threat to northern quolls (Dasyurus hallucatus) which are poisoned when they attack this novel prey item. Quolls are now endangered as a consequence of the toad invasion. Conditioned taste aversion can be used to train individual quolls to avoid toads, but we currently lack a training technique that can be used at a landscape scale to buffer entire populations from toad impact. Broad‐scale deployment requires a bait that can be used for training, but there is no guarantee that such a bait will ultimately elicit aversion to toads. Here, we test a manufactured bait – a ‘toad sausage’ – in a small captive trial, for its ability to elicit aversion to toads in northern quolls. To do this, we exposed one group of quolls to a toad sausage and another to a control sausage and compared the quolls' predatory responses when presented with a dead adult toad. Captive quolls that consumed a single toad sausage showed a reduced interest in cane toads, interacting with them for less than half the time of their untrained counterparts and showing reduced Attack behaviour. We also quantified bait uptake in the field, by both quolls and non‐target species. These field trials showed that wild quolls were the most frequent species attracted to the baits, and that approx. 61% of quolls consumed toad‐aversion baits when first encountered. Between 40% and 68% of these animals developed aversion to further bait consumption. Our results suggest that toad‐aversion sausages may be used to train wild quolls to avoid cane toads. This opens the possibility for broad‐scale quoll training with toad aversion sausages: a technique that may allow wildlife managers to prevent quoll extinctions at a landscape scale.     

Does intraspecific niche partitioning in a native predator influence its response to an invasion by a toxic prey species?

Abstract The introduced and highly toxic cane toad (Bufo marinus) is rapidly spreading across northern Australia where it may affect populations of large terrestrial vertebrate predators. The ecological impact of cane toads will depend upon the diets, foraging modes and habitat use of native predators, and their feeding responses to cane toads. However, intraspecific niche partitioning may influence the degree of vulnerability of predators to toxic prey, as well as the time course of the impact of alien invaders on native species. We studied the diet of the northern death adder Acanthophis praelongus and their feeding responses to cane toads. In the laboratory, death adders from all size classes and sexes readily consumed frogs and cane toads. Diets of free ranging A. praelongus from the Adelaide River floodplain were more heterogeneous. Juvenile snakes ate mainly frogs (39% of prey items) and small scincid lizards (43%). Both sexes displayed an ontogenetic dietary shift from lizards to mammals, but adult males fed on frogs (49%) and mammals (39%) whereas adult females (which grew larger than males) fed mainly on mammals (91%) and occasionally, frogs (9%). Feeding rates and body condition of adult snakes varied temporally and tracked fluctuations in prey availability. These results suggest that cane toads may negatively affect populations of northern death adders in the Darwin region. However, we predict that different size and sex classes of A. praelongus will experience differential mortality rates over different timescales. The initial invasion of large toads may affect adult males, but juveniles may be unaffected until juvenile toads appear the following year, and major affects on adult female death adders may be delayed until annual rainfall fluctuations reduce the availability of alternative (rodent) prey.     

Excluding access to invasion hubs can contain the spread of an invasive vertebrate

Many biological invasions do not occur as a gradual expansion along a continuous front, but result from the expansion of satellite populations that become established at 'invasion hubs'. Although theoretical studies indicate that targeting control efforts at invasion hubs can effectively contain the spread of invasions, few studies have demonstrated this in practice. In arid landscapes worldwide, humans have increased the availability of surface water by creating artificial water points (AWPs) such as troughs and dams for livestock. By experimentally excluding invasive cane toads (Bufo marinus) from AWP, we show that AWP provide a resource subsidy for non-arid-adapted toads and serve as dry season refuges and thus invasion hubs for cane toads in arid Australia. Using data on the distribution of permanent water in arid Australia and the dispersal potential of toads, we predict that systematically excluding toads from AWP would reduce the area of arid Australia across which toads are predicted to disperse and colonize under average climatic conditions by 38 per cent from 2,242,000 to 1,385,000 km(2). Our study shows how human modification of hydrological regimes can create a network of invasion hubs that facilitates a biological invasion, and confirms that targeted control at invasion hubs can reduce landscape connectivity to contain the spread of an invasive vertebrate.     

Interacting biocontrol programmes: invasive cane toads reduce rates of breakdown of cowpats by dung beetles

Ecological interactions among invasive species can affect not only the success of the invaders, but also their impact on ecosystems in the invaded range. In Australia, both dung beetles (subfamily Scarabaeinae) and cane toads (Rhinella marina) were introduced for biocontrol: the beetles to break down bovine faeces piles (cowpats) that otherwise accumulate and reduce pasture productivity, and the cane toad to consume scarab beetles that eat sugarcane and thus reduce sugar production. The dung beetles have been a success, whereas the toads have been a failure. Our experimental studies show that as well as impacting native fauna directly, cane toads reduce the rate of cowpat breakdown by consuming dung beetles. In the laboratory, dehydrated toads actively sought out cowpats based on scent cues, and in field enclosures, the presence of a cane toad significantly reduced rates of cowpat decomposition. Although toads have benefited from agricultural activities, their spread across Australia likely has reduced the effectiveness of one of the most successful biocontrol programmes ever conducted in that continent.     

Skin resistance to water gain and loss has changed in cane toads (Rhinella marina) during their Australian invasion

The water‐permeable skin of amphibians renders them highly sensitive to climatic conditions, and interspecific correlations between environmental moisture levels and rates of water exchange across the skin suggest that natural selection adapts hydroregulatory mechanisms to local challenges. How quickly can such mechanisms shift when a species encounters novel moisture regimes? Cutaneous resistance to water loss and gain in wild‐caught cane toads (Rhinella marina) from Brazil, USA (Hawai''i) and Australia exhibited strong geographic variation. Cutaneous resistance was low in native‐range (Brazilian) toads and in Hawai''ian populations (where toads were introduced in 1932) but significantly higher in toads from eastern Australia (where toads were introduced in 1935). Toads from recently invaded areas in western Australia exhibited cutaneous resistance to water loss similar to the native‐range populations, possibly because toads are restricted to moist sites within this highly arid landscape. Rates of rehydration exhibited significant but less extreme geographic variation, being higher in the native range than in invaded regions. Thus, in less than a century, cane toads invading areas that impose different climatic challenges have diverged in the capacity for hydroregulation.     

Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations

At an invasion front, energetic and physiological trade‐offs may differ from those at the range‐core as a result of selection for enhanced dispersal, combined with a low density of conspecifics (which reduces pathogen transmission and competition for food). We measured traits related to energy stores and immunity in wild cane toads (Rhinella marina) across a 750‐km transect from their invasion front in tropical Australia, back into sites colonized 21 years earlier. Several traits were found to vary with population age; some linearly and others in a curvilinear manner. The relative size of spleens and fat bodies was highest in the oldest and newest populations, where rates of lungworm infection were lowest. Toads from older populations produced more corticosterone in response to a standardized stressor, and had higher lymphocyte counts (but lower basophil counts). The amount of skin swelling elicited by phytohaemagglutinin injection did not vary geographically, although recruitment of leukocytes to the injected tissue was higher in toads from long‐colonized areas. Because this was a field‐based study, we cannot differentiate the effects of population age, toad density or pathogen pressure on our measures of stress and immune responses, nor can we distinguish whether the causation involves hard‐wired adaptive processes or phenotypically plastic responses. Nonetheless, our data demonstrate substantial variation in immune systems among toads at varying distances from an invasion front, showing that a biological invasion imposes strong pressures on physiological systems of the invader.     

Toads in the backyard: why do invasive cane toads (Rhinella marina) prefer buildings to bushland?

Like many invasive species, cane toads (Rhinella marina) in Australia concentrate in the disturbed habitats created by human activity, rather than in pristine areas. We surveyed cane toads in the wet–dry tropics of the Northern Territory to assess the abundances, body sizes, sexes, behaviour, hydration state and feeding rates of toads around buildings compared to those in areas remote from buildings, and conducted experimental trials to assess the effects of building-related variables (lights and increased toad densities) on the foraging success of toads. Toads around buildings were smaller than bushland conspecifics, and adult sex-ratios were female-biased. Toads were more sedentary around buildings than in the bush, but their feeding rates (based on direct observations and faeces production post-capture) were similar. That similarity, despite twofold-higher densities of competing toads around building, reflected the strong enhancement of feeding rates due to artificial lights attracting insects (in our experimental trials, a threefold increase regardless of the number of competing toads). Toads collected from around buildings were apparently in better hydric condition. Thus, access to water also may attract toads to buildings. The relative scarcity of adult male toads around buildings likely reflects waterbody-centred reproductive activities, whereas the concentration of females and juveniles around buildings is driven largely by access to the insects attracted by artificial light. We conclude that buildings enhance the persistence of cane toad populations and may facilitate their spread.     

After the crash: How do predators adjust following the invasion of a novel toxic prey type?

The ability of a native predator to adjust to a dangerously toxic invasive species is key to avoiding an ongoing suppression of the predator's population and the trophic cascade of effects that can result. Many species of anurophagous predators have suffered population declines due to the cane toad's (Rhinella marina: Bufonidae) invasion of Australia; these predators can be fatally poisoned from attempting to consume the toxic toad. We studied one such toad‐vulnerable predator, the yellow‐spotted monitor (Varanus panoptes: Varanidae), testing whether changes to the predator's feeding behaviour could explain how the species persists following toad invasion. Wild, free‐roaming lizards from (1) toad‐naïve and (2) toad‐exposed populations were offered non‐toxic native frogs and slightly toxic cane toads (with parotoid glands removed) in standardized feeding trials. Toad‐naïve lizards readily consumed both frogs and toads, with some lizards displaying overt signs of illness after consuming toads. In contrast, lizards from toad‐exposed populations consumed frogs but avoided toads. Repeated encounters with toads did not modify feeding responses by lizards from the toad‐naïve populations, suggesting that aversion learning is limited (but may nonetheless occur). Our results suggest that this vulnerable predator can adjust to toad invasion by developing an aversion to feeding on the toxic invader, but it remains unclear as to whether the lizard's toad‐aversion arises via adaptation or learning.     

A trophic cascade initiated by an invasive vertebrate alters the structure of native reptile communities

Invasive vertebrates are frequently reported to have catastrophic effects on the populations of species which they directly impact. It follows then, that if invaders exert strong suppressive effects on some species then other species will indirectly benefit due to ecological release from interactions with directly impacted species. However, evidence that invasive vertebrates trigger such trophic cascades and alter community structure in terrestrial ecosystems remains rare. Here, we ask how the cane toad, a vertebrate invader that is toxic to many of Australia's vertebrate predators, influences lizard assemblages in a semi‐arid rangeland. In our study area, the density of cane toads is influenced by the availability of water accessible to toads. We compared an index of the abundance of sand goannas, a large predatory lizard that is susceptible to poisoning by cane toads and the abundances of four lizard families preyed upon by goannas (skinks, pygopods, agamid lizards and geckos) in areas where cane toads were common or rare. Consistent with the idea that suppression of sand goannas by cane toads initiates a trophic cascade, goanna activity was lower and small lizards were more abundant where toads were common. The hypothesis that suppression of sand goannas by cane toads triggers a trophic cascade was further supported by our findings that small terrestrial lizards that are frequently preyed upon by goannas were more affected by toad abundance than arboreal geckos, which are rarely consumed by goannas. Furthermore, the abundance of at least one genus of terrestrial skinks benefitted from allogenic ecosystem engineering by goannas where toads were rare. Overall, our study provides evidence that the invasion of ecosystems by non‐native species can have important effects on the structure and integrity of native communities extending beyond their often most obvious and frequently documented direct ecological effects.