William E. Snyder

Organic agriculture promotes evenness and natural pest control

Human activity can degrade ecosystem function by reducing species number (richness) and by skewing the relative abundance of species (evenness). Conservation efforts often focus on restoring or maintaining species number, reflecting the well-known impacts of richness on many ecological processes. In contrast, the ecological effects of disrupted evenness have received far less attention, and developing strategies for restoring evenness remains a conceptual challenge. In farmlands, agricultural pest-management practices often lead to altered food web structure and communities dominated by a few common species, which together contribute to pest outbreaks. Here we show that organic farming methods mitigate this ecological damage by promoting evenness among natural enemies. In field enclosures, very even communities of predator and pathogen biological control agents, typical of organic farms, exerted the strongest pest control and yielded the largest plants. In contrast, pest densities were high and plant biomass was low when enemy evenness was disrupted, as is typical under conventional management. Our results were independent of the numerically dominant predator or pathogen species, and so resulted from evenness itself. Moreover, evenness effects among natural enemy groups were independent and complementary. Our results strengthen the argument that rejuvenation of ecosystem function requires restoration of species evenness, rather than just richness. Organic farming potentially offers a means of returning functional evenness to ecosystems.

INTERACTIONS BETWEEN SPECIALIST AND GENERALIST NATURAL ENEMIES: PARASITOIDS, PREDATORS, AND PEA APHID BIOCONTROL

Most biological control systems involve a diverse community of natural enemies. We investigated how specialist and generalist natural enemies differ as biological control agents of pea aphids (Acyrthosiphon pisum), and how interactions among natural enemies affect successful control. In alfalfa, pea aphids are attacked by a specialist parasitoid wasp, Aphidius ervi, and a guild of generalist predators primarily made up of Nabis and Orius bugs, coccinellid and carabid beetles, and web-building spiders. In three field experiments, we manipulated the parasitoid, then the generalist predator guild, and finally both classes of natural enemy, and recorded resulting impacts on pea aphid population control. The parasitoid caused little immediate reduction in aphid population growth but caused a large decline after a delay corresponding to the generation time of the parasitoid. In contrast, the generalist guild caused an immediate decline in the aphid population growth rate. However, the generalists did not exert density-dependent control, so aphid densities continued to increase throughout the experiment. The third field experiment in which we simultaneously manipulated parasitoids and predators investigated the possibility of “nonadditive effects” on aphid control. Densities of parasitoid pupae were 50% lower in the presence of generalist predators, indicating intraguild predation. Nonetheless, the ratio of parasitoids to aphids was not changed, and the impact of the two types of natural enemies was additive. We constructed a stage-structured model of aphid, parasitoid, and predator dynamics and fit the model to data from our field experiments. The model supports the additivity of parasitoid and predator effects on aphid suppression but suggests that longer-term experiments (32 d rather than 20 d) would likely reveal nonadditive effects as predation removes parasitoids whose response to aphid densities occurs with a delay. The model allowed us to explore additional factors that could influence the additivity of parasitoid and predator effects. Aphid density-dependent population growth and predator immigration in response to aphid density would likely have little influence on the additivity between parasitism and predation. However, if a parasitoid were to show a strong Type II functional response, in contrast to A. ervi whose functional response is nearly Type I, interactions with predators would likely be synergistic. These analyses reveal factors that should be investigated in other systems to address whether parasitism and predation act additively on host densities. Corresponding Editor: E. Evans.

SPECIES IDENTITY DOMINATES THE RELATIONSHIP BETWEEN PREDATOR BIODIVERSITY AND HERBIVORE SUPPRESSION

Agricultural pest suppression is an important ecosystem service that may be threatened by the loss of predator diversity. This has stimulated interest in the relationship between predator biodiversity and biological control. Multiple-predator studies have shown that predators may complement or interfere with one another, but few experiments have determined if the resulting effects on prey are caused by changes in predator abundance, identity, species richness, or some combination of these factors. We experimentally isolated the effect of predator species richness on the biological control of an important agricultural pest, the green peach aphid. We found no evidence that increasing predator species richness affects aphid biological control; overall there was no strong complementarity or interference among predator species that altered the strength of aphid suppression. Instead, our experiments revealed strong effects of predator species identity, because predators varied dramatically in their per capita consumption rates. Our results are consistent with other multiple-predator studies finding strong species-identity effects and suggest that, for the biological control of aphids, conservation strategies that directly target key species will be more effective than those targeting predator biodiversity more broadly.

Niche Partitioning Increases Resource Exploitation by Diverse Communities

Classical ecological theory suggests that the coexistence of consumer species is fostered by resource-use differences, leading to greater resource use in communities with more species. However, explicit empirical support for this idea is lacking, because resource use by species is generally confounded with other species-specific attributes. We overcame this obstacle by co-opting behavioral plasticity in food choice among a group of animal consumers, allowing us to manipulate patterns of resource use while controlling for the effects of species identity and diversity. Within an aphid-parasitoid-radish community, we created a fully factorial manipulation of consumer resource-use breadth (specialist versus generalist) and species diversity (one versus three species) and found that resource exploitation improved with greater specialist, but not generalist, diversity. Therefore, resource partitioning, and not diversity per se, fostered greater overall resource consumption in our multispecies consumer communities.

Intraguild predation and successful invasion by introduced ladybird beetles

Introductions of two ladybird beetle (Coleoptera: Coccinellidae) species, Coccinella septempunctata and Harmonia axyridis, into North America for aphid biocontrol have been followed by declines in native species. We examined intraguild predation (IGP) between larvae of these two exotic species and larvae of the two most abundant native coccinellids in eastern Washington State, C. transversoguttata and Hippodamia convergens. In pairings between the two native species in laboratory microcosms containing pea (Pisum sativum) plants, neither native had a clear advantage over the other in IGP. When the natives were paired with either Harmonia axyridis or C. septempunctata, the natives were more frequently the victims than perpetrators of IGP. In contrast, in pairings between the exotic species, neither had an IGP advantage, although overall rates of IGP between these two species were very high. Adding alternative prey (aphids) to microcosms did not alter the frequency and patterns of relative IGP among the coccinellid species. In observations of encounters between larvae, the introduced H. axyridis frequently survived multiple encounters with the native C. transversoguttata, whereas the native rarely survived a single encounter with H. axyridis. Our results suggest that larvae of the native species face increased IGP following invasion by C. septempunctata and H. axyridis, which may be contributing to the speed with which these exotic ladybird beetles displace the natives following invasion.

Nutritional Benefits of Cannibalism for the Lady Beetle Harmonia axyridis (Coleoptera: Coccinellidae) When Prey Quality is Poor

Abstract Cannibalism, a widespread phenomenon in nature, can both reduce competitors and introduce a high-quality food into the cannibal’s diet. We investigated the dietary benefits of cannibalism for larvae of the multicolored Asian lady beetle, Harmonia axyridis (Pallas). Cannibalism might benefit the larvae by allowing cannibals to take advantage of prey-detoxification already completed by the victim or the different, and perhaps more diverse, feeding history of the victim. In two laboratory experiments we reared H. axyridis larvae with aphid prey, and with or without conspecifics to consume, and recorded larval development and survivorship. In the first experiment, we fed groups of H. axyridis larvae an aphid species of intermediate quality, Aphis nerii (Boyer deFonscolombe), and prevented or permitted consumption of conspecifics of varied quality—conspecific victims had either fed upon the same intermediate quality food as the focal individual or had fed upon a high quality food. Cannibalism increased survivorship and shortened development time, and eating conspecifics that had fed upon higher-quality food further shortened early development. In a second experiment, we reared groups of H. axyridis larvae with one or both of two aphid species of poor ( Uroleucon spp.) or intermediate [ Aphis fabae (Scopoli)] quality, and either permitted or prevented cannibalism. Larvae could complete development when fed both conspecifics and the intermediate quality aphid, but not on any other diet. Overall, when mixed with other foods, cannibalism allowed H. axyridis larvae to develop on prey that were otherwise nutrient deficient or toxic.

INCREASING ENEMY BIODIVERSITY STRENGTHENS HERBIVORE SUPPRESSION ON TWO PLANT SPECIES

Concern over biodiversity loss, especially at higher trophic levels, has led to a surge in studies investigating how changes in natural enemy diversity affect community and ecosystem functioning. These studies have found that increasing enemy diversity can strengthen, weaken, and not affect prey suppression, demonstrating that multi-enemy effects on prey are context-dependent. Here we ask how one factor, plant species identity, influences multi-enemy effects on prey. We focused on two plant species of agricultural importance, potato (Solanum tuberosum), and collards (Brassica oleracea L.). These species share a common herbivorous pest, the green peach aphid (Myzus persicae), but vary in structural and chemical traits that affect aphid reproductive rates and which may also influence inter-enemy interactions. In a large-scale field experiment, overall prey exploitation varied dramatically among the plant species, with enemies reducing aphid populations by approximately 94% on potatoes and approximately 62% on collards. Increasing enemy diversity similarly strengthened aphid suppression on both plants, however, and there was no evidence that plant species identity significantly altered the relationship between enemy diversity and prey suppression. Microcosm experiments suggested that, on both collards and potatoes, intraspecific competition among natural enemies exceeded interspecific competition. Enemy species showed consistent and significant differences in where they foraged on the plants, and enemies in the low-diversity treatment tended to spend less time foraging than enemies in the high-diversity treatment. These data suggest that increasing enemy diversity may strengthen aphid suppression because interspecific differences in where enemies forage on the plant allow for greater resource partitioning. Further, these functional benefits of diversity appear to be robust to changes in plant species identity.

Cannibalism reverses male-biased sex ratio in adult mantids: female strategy against food limitation?

Adult populations of the mantid, Tenodera sinensis (Saussure) initially were malebiased, but females outnumbered males by the end of the life cycle because mortality was higher among males than among females. Male mantids were the most frequent items in the diet of females during oogenesis, when food limitation generally is greatest. Males had an 83% chance of escaping cannibalism during any given encounter with a female; however, females continued to attract males after first mating, raising the cumulative probability of male death with increasing number of intersexual encounters. We suggest female mantids continue to attract and cannibalize males beyond their need for sperm as a strategy to alleviate food limitation during oogenesis. This is more parsimonious than the adaptive suicide hypothesis, in which male fitness is enhanced by investment of his biomass in this offspring, since our hypothesis does not require that the victim share parenthood with his cannibal

Niche saturation reveals resource partitioning among consumers

More diverse communities of consumers typically use more resources, which often is attributed to resource partitioning. However, experimentally demonstrating this role of resource partitioning in diverse communities has been difficult. We used an experimental response-surface design, varying intra- and interspecific consumer densities, to compare patterns of resource exploitation between simple and diverse communities of aphid predators. With increasing density, each single consumer species rapidly plateaued in its ability to extract more resources. This suggests intraspecific competition for a subset of the resource pool, a hallmark of resource partitioning. In contrast, more diverse-predator communities achieved greater overall resource depletion. By statistically fitting mechanistic models to the data, we demonstrated that resource partitioning rather than facilitation provides the better explanation for the observed differences in resource use between simple and diverse communities. This model-fitting approach also allowed us to quantify overlap in resource use by different consumer species.

Eating their way to the top? Mechanisms underlying the success of invasive insect generalist predators

Insect generalist predators have been introduced outside of their native range intentionally to improve biological control, or accidentally during commerce, and can subsequently become invasive. Invasive insect generalist predators (IIGP) have widespread impacts on invaded communities because they consume both herbivores and other predators. Also, they often reach higher densities than and displace similar native species. Reflecting the complexity of their ecological roles, a wide variety of mechanisms might contribute to invasive success by IIGP. These species often drive resources to lower levels than do natives, leading to intense resource competition and sometimes competitive exclusion of other predators. The broader range of resources used by many IIGP can heighten their competitive advantage, particularly when IIGP exploit modified habitats. In either case, IIGP improve herbivore suppression by depressing prey densities below pre-invasion levels. Coexistence among native and invasive generalists is fostered when species differ substantially in their niche requirements. In this case, a larger proportion of the total prey population is subject to attack post- than pre-invasion, which strengthens prey suppression. On the other hand, some IIGP feed heavily on other predators, at times leading to a weakening of prey suppression. Future research should continue to explore the roles of competition and niche partitioning on larger spatial scales, and in both the native and invasive ranges of IIGP. Additionally, combining data from empirical studies with theory might be an effective way to predict the spread and community impacts of IIGP invasions.