Integration of ecosystem science into radioecology: A consensus perspective.

In the Fall of 2016 a workshop was held which brought together over 50 scientists from the ecological and radiological fields to discuss feasibility and challenges of reintegrating ecosystem science into radioecology. There is a growing desire to incorporate attributes of ecosystem science into radiological risk assessment and radioecological research more generally, fueled by recent advances in quantification of emergent ecosystem attributes and the desire to accurately reflect impacts of radiological stressors upon ecosystem function. This paper is a synthesis of the discussions and consensus of the workshop participant's responses to three primary questions, which were: 1) How can ecosystem science support radiological risk assessment? 2) What ecosystem level endpoints potentially could be used for radiological risk assessment? and 3) What inference strategies and associated methods would be most appropriate to assess the effects of radionuclides on ecosystem structure and function? The consensus of the participants was that ecosystem science can and should support radiological risk assessment through the incorporation of quantitative metrics that reflect ecosystem functions which are sensitive to radiological contaminants. The participants also agreed that many such endpoints exit or are thought to exit and while many are used in ecological risk assessment currently, additional data need to be collected that link the causal mechanisms of radiological exposure to these endpoints. Finally, the participants agreed that radiological risk assessments must be designed and informed by rigorous statistical frameworks capable of revealing the causal inference tying radiological exposure to the endpoints selected for measurement.

Atrazine exposure shifts activity but has minimal effects on courtship in an agrobiont spider.

The behavior of many animals relies upon the input of chemical signals throughout the environment. Those animals that live in close proximity to humans may then be at risk, as the input of anthropogenic chemicals can have significant sublethal effects by masking or altering these naturally occurring signals. While the herbicide atrazine has been found to have the potential to alter such chemical information, research is lacking on how it may impact agrobiont arthropods which are the first and most direct line of exposure. Here we investigated the sublethal effects atrazine may be playing on an agrobiont wolf spider that makes up a major component of agricultural spider communities in the Eastern United States. We exposed spiders to ecologically relevant doses of atrazine and monitored general activity patterns as well as mating behaviors. We found that while sex determined a large portion of activity variation in these predators, both males and females spent more time mobile but at lower speeds in the presence of atrazine. We did not find any evidence for info-disruption based on male courtship rate and mating success, but with increasing dosage of atrazine came shortened bouts of courtship leading to copulation. These results suggest that atrazine changed activity patterns of a wolf spider, which may result in altered foraging, survival, and reproduction.

Impact of an atrazine-based herbicide on an agrobiont wolf spider.

For animals that live in association with humans, a key ecological question is how anthropogenic factors influence their life history. While major negative effects are obvious, subtle non-lethal responses to anthropogenic stimuli may provide insight into the features that lead to the success of species that thrive in habitats heavily impacted by humans. Here we explored the influence of the herbicide atrazine on various life history traits of a wolf spider that thrives in agroecosystems where it is commonly applied. We found that exposure delayed maturation and increased the probability of having molting errors. Atrazine also decreased the probability of producing an egg sac after mating, but increased the average mass of the initial egg sacs that were produced while not impacting the average number of eggs inside. The total number of eggs produced from a single mating on the other hand, was increased in the presence of atrazine through the production of multiple egg sacs. Finally, adult lifespan was shortened with exposure to atrazine. These results suggest that the atrazine based herbicides that are routinely applied to agricultural fields result in altered life history traits, potentially through endocrine disruption, that may counteract one another to allow persistence.

Contact with a glyphosate-based herbicide has long-term effects on the activity and foraging of an agrobiont wolf spider.

Animals that live in conventional agroecosystems must cope with a variety of anthropogenic chemicals. Most of the focus of toxicology is on lethality, deformities, or short-term shifts in behavior. However, for animals that succeed in spite of their exposure, it is important to determine if long-term changes are brought on by their experience. We tested the hypothesis that contact with a commercial formulation of a glyphosate-based herbicide would affect the behavior of subsequent instars in the wolf spider, Pardosa milvina, a species that thrives in the agroecosystems of eastern United States. In one experiment, we housed females carrying egg sacs on a surface treated with the herbicide for 7 h. Then we monitored their activity and foraging of the offspring 4 weeks after emergence. We repeated the same tests on adults that had been housed with herbicide during their penultimate stage. In both studies, exposed spiders displayed higher levels of activity and greater capture success than their unexposed counterparts. Exposure of penultimate instar to herbicide had larger effects on the behavior of adult males than adult females. These results suggest that herbicides have the potential to adjust the behavior of individuals in the predator community. Thus, impact on the food web and their positive or negative potential for biological control may extend beyond their role in controlling weeds.

Information from familiar and related conspecifics affects foraging in a solitary wolf spider.

As neighbours become familiar with one another, they can divert attention away from one another and focus on other activities. Since familiarity is a likely mechanism by which animals recognise relatives, both kinship and prior association with conspecifics should allow individuals to increase foraging. We attempted to determine if the interference observed among conspecific foragers could be mitigated by familiarity and/or kinship. Because Pardosa milvina wolf spiders are sensitive to chemotactile cues deposited on substrates by other spiders, we used cues to manipulate the information available to focal spiders. We first verified that animals could use these cues to differentiate relatives and familiar conspecifics. We then documented foraging in the presence of all combinations of related and familiar animal cues. Test spiders were slower foragers, less likely to capture prey, and consumed less of each prey item when on cues from unfamiliar kin, but were faster and more effective foragers on cues from familiar non-kin. Their reactions to familiar kin and unfamiliar non-kin were intermediate. High foraging intensity on familiar cues is consistent with the idea that animals pay less attention to neighbours after some prior association. Lower foraging effort in the presence of cues from relatives may be an attempt to reduce kin competition by shifting attention toward dispersal or to provide increased access to prey for hungry relatives nearby. These findings reveal that information from conspecifics mediates social interactions among individuals and affects foraging in ways that can influence their role in the food web.

Nonconsumptive Predator-Prey Interactions: Sensitivity of the Detritivore Sinella curviseta (Collembola: Entomobryidae) to Cues of Predation Risk From the Spider Pardosa milvina (Araneae: Lycosidae).

Predators can affect prey indirectly when prey respond to cues indicating a risk of predation by altering activity levels. Changes in prey behavior may cascade through the food web to influence ecosystem function. The response of the collembolan Sinella curviseta Brook (Collembola: Entomobryidae) to cues indicating predation risk (necromones and cues from the wolf spider Pardosa milvina (Hentz) (Araneae: Lycosidae)) was tested. Additionally, necromones and predator cues were paired in a conditioning experiment to determine whether the collembolan could form learned associations. Although collembolans did not alter activity levels in response to predator cues, numerous aspects of behavior differed in the presence of necromones. There was no detectable conditioned response to predator cues after pairing with necromones. These results provide insight into how collembolans perceive and respond to predation threats that vary in information content. Previously detected indirect impacts of predator cues on ecosystem function are likely due to changes in prey other than activity level.

Fear of predation alters soil carbon dioxide flux and nitrogen content.

Predators are known to have both consumptive and non-consumptive effects (NCEs) on their prey that can cascade to affect lower trophic levels. Non-consumptive interactions often drive these effects, though the majority of studies have been conducted in aquatic- or herbivory-based systems. Here, we use a laboratory study to examine how linkages between an above-ground predator and a detritivore influence below-ground properties. We demonstrate that predators can depress soil metabolism (i.e. CO2 flux) and soil nutrient content via both consumptive and non-consumptive interactions with detritivores, and that the strength of isolated NCEs is comparable to changes resulting from predation. Changes in detritivore abundance and activity in response to predators and the fear of predation likely mediate interactions with the soil microbe community. Our results underscore the need to explore these mechanisms at large scales, considering the disproportionate extinction risk faced by predators and the importance of soils in the global carbon cycle.

Predator interference alters foraging behavior of a generalist predatory arthropod.

Interactions between predators foraging in the same patch may strongly influence patch use and functional response. In particular, there is continued interest in how the magnitude of mutual interference shapes predator-prey interactions. Studies commonly focus on either patch use or the functional response without attempting to link these important components of the foraging puzzle. Predictions from both theoretical frameworks suggest that predators should modify foraging efforts in response to changes in feeding rate, but this prediction has received little empirical attention. We study the linkage between patch departure rates and food consumption by the hunting spider, Pardosa milvina, using field enclosures in which prey and predator densities were manipulated. Additionally, the most appropriate functional response model was identified by fitting alternative functional response models to laboratory foraging data. Our results show that although prey availability was the most important determinant of patch departure rates, a greater proportion of predators left enclosures containing elevated predator abundance. Functional response parameter estimation revealed significant levels of interference among predators leading to lower feeding rates even when the area allocated for each predator was kept constant. These results suggest that feeding rates determine patch movement dynamics, where interference induces predators to search for foraging sites that balance the frequency of agonistic interactions with prey encounter rates.

Glyphosate-based herbicide has contrasting effects on prey capture by two co-occurring wolf spider species.

Anthropogenic substances have the potential to affect animal behavior either because they present a novel stimulus or because they interfere with natural chemical communication pathways. Such shifts can alter the dynamic between predators and potential prey, which might affect population success as well as the strength of food web linkages. We examined the foraging of two wolf spiders, Tigrosa helluo and Pardosa milvina (Araneae, Lycosidae), that are abundant in agroecosystems where they are routinely exposed to herbicides. We tested the hypothesis that the presence of a commercial formulation of a glyphosate-based herbicide would affect the prey capture behavior of these two wolf spiders. We tested the larger Tigrosa foraging on Pardosa or crickets (Acheta domesticus) and the smaller Pardosa foraging on crickets. Tigrosa subdued crickets more quickly and with fewer lunges than it took them to capture Pardosa. The presence of herbicide allowed Tigrosa to orient toward and capture both prey species more quickly but it did not affect the number of lunges required to subdue either prey. Herbicide did not affect the timing of prey capture for Pardosa but it did cause them to use more lunges in the process. Thus, herbicide had contrasting effects on foraging behavior of these two agrobiont predators, which means that it could shift the direction and strength of food web linkages in complex ways.

Spider silk reduces insect herbivory.

The role of predators in food webs extends beyond their ability to kill and consume prey. Such trait-mediated effects occur when signals of the predator influence the behaviour of other animals. Because all spiders are silk-producing carnivores, we hypothesized that silk alone would signal other arthropods and enhance non-lethal effects of spiders. We quantified the herbivory inflicted by two beetle species on green bean plants (Phaseolus vulgaris) in the presence of silkworm silk and spider silk along with no silk controls. Single leaflets were treated and enclosed with herbivores in the laboratory and field. Another set of leaflets were treated and left to experience natural herbivory in the field. Entire plants in the field were treated with silk and enclosed with herbivores or left exposed to herbivory. In all cases, the lowest levels of herbivory occurred with spider silk treatments and, in general, silkworm silk produced intermediate levels of leaf damage. These results suggest that silk may be a mechanism for the trait-mediated impacts of spiders and that it might contribute to integrated pest management programmes.

The nutritional content of prey affects the foraging of a generalist arthropod predator.

While foraging theory predicts that predatory responses should be determined by the energy content and size of prey, it is becoming increasingly clear that carnivores regulate their intake of specific nutrients. We tested the hypothesis that prey nutrient composition and predator nutritional history affects foraging intensity, consumption, and prey selection by the wolf spider, Pardosa milvina. By altering the rearing environment for fruit flies, Drosophila melanogaster, we produced high quality flies containing more nitrogen and protein and less lipid than low quality fruit flies. In one experiment, we quantified the proportion of flies taken and consumption across a range of densities of either high or low quality flies and, in a second experiment, we determined the prey capture and consumption of spiders that had been maintained on contrasting diets prior to testing. In both cases, the proportion of prey captured declined with increasing prey density, which characterizes the Type II functional response that is typical of wolf spiders. Spiders with similar nutritional histories killed similar numbers of each prey type but consumed more of the low quality prey. Spiders provided high quality prey in the weeks prior to testing killed more prey than those on the low quality diet but there was no effect of prior diet on consumption. In the third experiment, spiders were maintained on contrasting diets for three weeks and then allowed to select from a mixture of high and low quality prey. Interestingly, feeding history affected prey preferences: spiders that had been on a low quality diet showed no preference but those on the high quality diet selected high quality flies from the mixture. Our results suggest that, even when prey size and species identity are controlled, the nutritional experience of the predator as well as the specific content of the prey shapes predator-prey interactions.

Predator cues and an herbicide affect activity and emigration in an agrobiont wolf spider.

Animals use chemical cues for signaling between species. However, anthropogenic chemicals might interrupt this natural chemical information flow, with potential impacts on predator-prey interactions. Our goal was to explore how Buccaneer® Plus, a common herbicide similar to Round-up® (active ingredient glyphosate), affected the interactions between intraguild predators. The wolf spider Pardosa milvina (Hentz, 1844) is numerically dominant in agricultural systems across the eastern United States, and often falls prey to or competes with the larger wolf spider, Hogna helluo (Walckenaer, 1837) and/or the carabid beetle, Scarites quadriceps (Chaudoir, 1843). We tested the effects of chemical cues from these intraguild predators and exposure to herbicide on the activity, emigration, and survival of P. milvina using a full-factorial laboratory experiment. Both predator cues and herbicide led to a decrease in movement by P. milvina. However, although H. helluo cues alone decreased movement, S. quadriceps cues only decreased movement when combined with herbicide. These results indicate that predation risk and herbicide application likely interact in complex ways to affect the movement of a major arthropod predator in agricultural systems, and thus may have complex effects on the food web.

Effects of a glyphosate-based herbicide on mate location in a wolf spider that inhabits agroecosystems.

Chemical communication is important to many arthropod species but the potential exists for anthropogenic chemicals to disrupt information flow. Although glyphosate-based herbicides are not acutely toxic to arthropods, little is known regarding their effects on natural chemical communication pathways. The wolf spider, Pardosamilvina, is abundant in agroecosystems where herbicides are regularly applied and uses air- and substrate-borne chemical signals extensively during mating. The aim of this study was to examine effects of a commercial formulation of a glyphosate-based herbicide on the ability of males to find females. In the field, virgin females, when hidden inside pitfall traps with herbicide, attracted fewer males than females with water. Likewise females in traps with a ring of herbicide surrounding the opening were less likely to attract males than those in traps surrounded by water. We explored the reaction of males to any airborne component of the herbicide in a laboratory two-choice olfactometer experiment. When no female pheromones were present, males were equally likely to select herbicide or water treated corridors and they all moved through the apparatus at similar speeds. When female pheromones were present, the males that selected control corridors moved more slowly than those that selected herbicide and, if we control for the initial decision time, more males selected the control corridors over the herbicide. These data suggest that glyphosate-based herbicides are "info-disruptors" that alter the ability of males to detect and/or react fully to female signals.

Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters.

Structural features of habitat are known to affect the density of predators and prey, and it is generally accepted that complexity provides some protection from the environment and predators but may also reduce foraging success. A next step in understanding these interactions is to decouple the impacts of both spatial and trophic ingredients of complexity to explicitly explore the trade-offs between the habitat, its effects on foraging success, and the competition that ensues as predator densities increase. We quantified the accumulation of spiders and their prey in habitat islands with different habitat complexities created in the field using natural plants, plant debris and plastic plant mimics. Spiders were observed at higher densities in the complex habitat structure composed of both live plants and thatch. However, the numerically dominant predator in the system, the wolf spider Pardosa milvina, was observed at high densities in habitat islands containing plastic mimics of plants and thatch. In a laboratory experiment, we examined the interactive effects of conspecific density and habitat on the prey capture of P. milvina. Thatch, with or without vertical plant structure, reduced prey capture, but the plastic fiber did not. Pairwise interactions among spiders reduced prey capture, but this effect was moderated by thatch. Taken together, these experiments highlight the flexibility of one important predator in the food web, where multiple environmental cues intersect to explain the role of habitat complexity in determining generalist predator accumulation.

Exposure to a glyphosate-based herbicide affects agrobiont predatory arthropod behaviour and long-term survival.

Humans commonly apply chemicals to manage agroecosystems. If those chemicals influence the behaviour or survival of non-target arthropods, the food web could be altered in unintended ways. Glyphosate-based herbicides are among the most ubiquitous pesticides used around the world, yet little is known about if and how they might affect the success of terrestrial predatory arthropods in agroecosystems. In this study, we quantified the effects of a commercial formulation of a glyphosate-based herbicide on the activity of three predatory arthropod species that inhabit agricultural fields in the eastern United States. We also measured the survival of the most common species. We tested the reactions of the wolf spider, Pardosa milvina, to either direct application (topical) or contact with a treated substrate (residual). We quantified the reactions of a larger wolf spider, Hogna helluo, and a ground beetle, Scarites quadriceps, to a compound (topical plus residual) exposure. Pardosa milvina reduced locomotion time and distance under topical herbicide exposure, but increased speed and non-locomotory activity time on exposed substrate. Both H. helluo and S. quadriceps increased non-locomotory activity time under compound herbicide exposure. Over a period of 60 days post-exposure, residually exposed P. milvina exhibited lower survivorship compared to topically exposed and control groups. Thus, exposure of terrestrial arthropods to glyphosate-based herbicides affects their behaviour and long-term survival. These results suggest that herbicides can affect arthropod community dynamics separate from their impact on the plant community and may influence biological control in agroecosystems.

Males make poor meals: a comparison of nutrient extraction during sexual cannibalism and predation.

Cannibalism is hypothesized to have evolved as a way to obtain a high-quality meal. We examined the extraction of lipid and protein by female wolf spiders, Hogna helluo, during sexual cannibalism of males and predation of crickets. Most food-limited females did not cannibalize males but immediately consumed a size-matched cricket. When consuming male H. helluo and crickets, female H. helluo only consumed 51% of the male body while they consumed 72% of the cricket body. While males had higher protein content in their bodies than crickets and other insects, female H. helluo ingested similar amounts of protein from male H. helluo and crickets. Female H. helluo extracted 47% of the protein present in male H. helluo and 67% of the protein present in crickets. Females were able to extract nearly all of the lipid present in male H. helluo and crickets. However, crickets and other insects had almost 4 times higher lipid content than male H. helluo. The ratio of lipid to protein consumed from crickets appeared more similar to the nutritional requirements of egg production than that of males. Taken together, female hesitancy to engage in cannibalism, low extraction of nutrients from males and a low ratio of lipid to protein in the food extracted from males suggest that males may be poor-quality prey items compared to common insects such as crickets.

Sexual size dimorphism predicts the frequency of sexual cannibalism within and among species of spiders.

Sexual cannibalism varies widely among spiders, but no general evolutionary hypothesis has emerged to explain its distribution across taxa. Sexual size dimorphism (SSD) also varies widely among spiders and could affect the vulnerability of males to cannibalistic attacks by females. We tested for a relationship between SSD and sexual cannibalism within and among species of spiders, using a broad taxonomic data set. For most species, cannibalism was more likely when males were much smaller than females. In addition, using phylogenetically controlled and uncontrolled analyses, there was a strong positive relationship between average SSD of a species and the frequency of sexual cannibalism. This is the first evidence that the degree of size difference between males and females is related to the phylogenetic distribution of sexual cannibalism among a broad range of spiders.

Field evidence of an airborne enemy-avoidance kairomone in wolf spiders.

Hogna helluo, Pardosa milvina, and Trochosa ruricola are co-occurring species of wolf spiders within agricultural fields in the eastern USA. The largest species, H. helluo, is a common predator of the two smaller species, P. milvina and T. ruricola. H. helluo frequently resides within soil fissures where P. milvina and T. ruricola may be attacked when they enter or walk near these fissures. We tested the ability of P. milvina and T. ruricola to avoid H. helluo-containing burrows by detecting airborne enemy-avoidance kairomones associated with H. helluo. To simulate soil fissures and control for visual and vibratory means of predator detection, we baited funneled pitfall traps with one of the following (N = 20 traps/treatment): (1) blank (empty trap); (2) one house cricket (Acheta domesticus); (3) one adult female H. helluo; and (4) one adult male H. helluo. Over two separate 3-d periods, we measured pitfall capture rates of P. milvina and T. ruricola as well as other incidentally captured ground-dwelling arthropods. During the day, male P. milvina showed significant avoidance of pitfall traps baited with H. helluo of either sex but showed no avoidance of empty traps or those containing crickets. At night, male T. ruricola showed a qualitatively similar pattern of avoiding H. helluo-baited traps, but the differences were not statistically significant. We found no evidence that other ground-dwelling arthropods either avoided or were attracted to H. helluo-baited traps. This study suggests that an airborne enemy-avoidance kairomone may mediate behavior among male P. milvina in the field.

Prey size, prey perishability and group foraging in a social spider.

Selection might favor group foraging and social feeding when prey are distributed in patches that do not last long enough for a solitary individual to consume more than a small fraction of them (Pulliam and Millikan 1982; Pulliam and Caraco 1984). Here we considered the foraging behavior of a social spider, Anelosimus eximius, in light of this ephemeral resource hypothesis. This species builds large webs in which members cooperate to capture a wide variety of different sizes and types of prey, many of which are very large. The capture success of this species was very high across all prey sizes, presumably due to the fact that they foraged in groups. Group consumption times in natural colonies for all prey larger than five mm were less than the time that dead insects remained on the plastic sheets that we used as artificial webs. Solitary consumption estimates, calculated from the rate at which laboratory individuals extracted insect biomass while feeding, were the same as the residence times of insects on artificial webs in the field for insects between 6 and 15 mm in length and were significantly longer than the persistence of insects on plastic sheets for all larger insects. Large prey, that contribute substantially to colony energy supplies, appeared to be ephemeral resources for these spiders that could not be consumed by a single spider in the time they were available. These factors made the food intake of one spider in a group less sensitive to scavenging by others and could act to reinforce the social system of this species.