Tatyana A. Rand

Resource Heterogeneity Moderates the Biodiversity-Function Relationship in Real World Ecosystems

Numerous recent studies have tested the effects of plant, pollinator, and predator diversity on primary productivity, pollination, and consumption, respectively. Many have shown a positive relationship, particularly in controlled experiments, but variability in results has emphasized the context-dependency of these relationships. Complementary resource use may lead to a positive relationship between diversity and these processes, but only when a diverse array of niches is available to be partitioned among species. Therefore, the slope of the diversity-function relationship may change across differing levels of heterogeneity, but empirical evaluations of this pattern are lacking. Here we examine three important functions/properties in different real world (i.e., nonexperimental) ecosystems: plant biomass in German grasslands, parasitism rates across five habitat types in coastal Ecuador, and coffee pollination in agroforestry systems in Indonesia. We use general linear and structural equation modeling to demonstrate that the effect of diversity on these processes is context dependent, such that the slope of this relationship increases in environments where limiting resources (soil nutrients, host insects, and coffee flowers, respectively) are spatially heterogeneous. These real world patterns, combined with previous experiments, suggest that biodiversity may have its greatest impact on the functioning of diverse, naturally heterogeneous ecosystems.

EXOTIC WEED INVASION INCREASES THE SUSCEPTIBILITY OF NATIVE PLANTS TO ATTACK BY A BIOCONTROL HERBIVORE

Landscape change has great, yet infrequently measured, potential to influence the susceptibility of natural systems to invasive species impacts. We quantified attack by an invasive biological control weevil (Rhinocyllus conicus) on native thistles in relation to two types of landscape change: agricultural intensification and invasion by an exotic thistle, Carduus nutans, the original target of biological control. Weevil egg load was measured on native thistles in three landscape types: (1) agriculture dominated, (2) grassland dominated with exotic thistles, and, (3) grassland dominated without exotic thistles. We found no difference in egg load on native thistles within grassland landscapes without exotic thistles vs. within agricultural landscapes, suggesting that agricultural intensification per se does not influence levels of weevil attack. However, attack on the native Cirsium undulatum increased significantly (three- to fivefold) with increasing exotic thistle density. Within-patch exotic thistle density explained >50% of the variation in both the intensity and frequency of weevil attack. Since R. conicus feeding dramatically reduces seed production, exotic thistles likely exert a negative indirect effect on native thistles. This study provides some of the first empirical evidence that invasion by an exotic plant can increase attack of native plants by shared insect herbivores.

EVALUATION OF ECOLOGICAL RISK TO POPULATIONS OF A THREATENED PLANT FROM AN INVASIVE BIOCONTROL INSECT

Controversy exists over estimation of ecological risk in biological control. At present, the risk to the rare, federally listed Pitchers thistle (Cirsium pitcheri )i nNorth America from Rhinocyllus conicus ,a biological control weevil now feeding on many native thistles, is unknown. We hypothesized that quantification of host specificity and potential phenological overlap between insect and plant would improve assessment of the magnitude of risk. In laboratory host specificity tests, we found no significant difference in R. conicus feeding or oviposition preference between the rare C. pitcheri and the targeted exotic weed (Carduus nutans )o rbetween C. pitcheri and Platte thistle (C. canescens), a closely related native North American species known to be affected by R. conicus .I na garden environment, R. conicus spontaneously found, oviposited, and developed completely on C. pitcheri .T aller plants with more flower heads were significantly more vulnerable, suggesting that the greatest impact is likely to be on individuals that generally contribute the most to recruitment and population persistence. For eight sites in two national parks over three years, the calculated period of expected R. conicus activity overlapped 99% and 78% of the flower heads initiated by C. pitcheri in the southern and the northern park, respectively. A de- mographic model suggests that population growth rate ( )o fC. pitcheri will decrease from 0.9897 to 0.8686, while time to halve the population will decrease from 66.9 to 4.9 years, under the conservative assumption that oviposition by R. conicus on C. pitcheri will occur at the same rate as on the related C. canescens. Calculated decreases in and t0.5 are larger if the rate of oviposition actually observed in the laboratory tests is used. These results indicate that the weevil poses a serious quantitative, demographic risk to the threatened C. pitcheri. The study supports the suggestion that ecological data can be used to improve the quantification of risk to native nontarget plant populations within the potential physiological host range of a biological control insect.

Reprint of “Conservation biological control and enemy diversity on a landscape scale” [Biol. Control 43 (2007) 294–309]

Abstract Conservation biological control in agroecosystems requires a landscape management perspective, because most arthropod species experience their habitat at spatial scales beyond the plot level, and there is spillover of natural enemies across the crop–noncrop interface. The species pool in the surrounding landscape and the distance of crop from natural habitat are important for the conservation of enemy diversity and, in particular, the conservation of poorly-dispersing and specialized enemies. Hence, structurally complex landscapes with high habitat connectivity may enhance the probability of pest regulation. In contrast, generalist and highly vagile enemies may even profit from the high primary productivity of crops at a landscape scale and their abundance may partly compensate for losses in enemy diversity. Conservation biological control also needs a multitrophic perspective. For example, entomopathogenic fungi, plant pathogens and endophytes as well as below- and above-ground microorganisms are known to influence pest-enemy interactions in ways that vary across spatiotemporal scales. Enemy distribution in agricultural landscapes is determined by beta diversity among patches. The diversity needed for conservation biological control may occur where patch heterogeneity at larger spatial scales is high. However, enemy communities in managed systems are more similar across space and time than those in natural systems, emphasizing the importance of natural habitat for a spillover of diverse enemies. According to the insurance hypothesis, species richness can buffer against spatiotemporal disturbances, thereby insuring functioning in changing environments. Seemingly redundant enemy species may become important under global change. Complex landscapes characterized by highly connected crop–noncrop mosaics may be best for long-term conservation biological control and sustainable crop production, but experimental evidence for detailed recommendations to design the composition and configuration of agricultural landscapes that maintain a diversity of generalist and specialist natural enemies is still needed.

Complementarity and redundancy of interactions enhance attack rates and spatial stability in host-parasitoid food webs.

Complementary resource use and redundancy of species that fulfill the same ecological role are two mechanisms that can respectively increase and stabilize process rates in ecosystems. For example, predator complementarity and redundancy can determine prey consumption rates and their stability, yet few studies take into account the multiple predator species attacking multiple prey at different rates in natural communities. Thus, it remains unclear whether these biodiversity mechanisms are important determinants of consumption in entire predator-prey assemblages, such that food-web interaction structure determines community-wide consumption and stability. Here, we use empirical quantitative food webs to study the community-wide effects of functional complementarity and redundancy of consumers (parasitoids) on herbivore control in temperate forests. We find that complementarity in host resource use by parasitoids was a strong predictor of absolute parasitism rates at the community level and that redundancy in host-use patterns stabilized community-wide parasitism rates in space, but not through time. These effects can potentially explain previous contradictory results from predator diversity research. Phylogenetic diversity (measured using taxonomic distance) did not explain functional complementarity or parasitism rates, so could not serve as a surrogate measure for functional complementarity. Our study shows that known mechanisms underpinning predator diversity effects on both functioning and stability can easily be extended to link food webs to ecosystem functioning.

VARIATION IN HERBIVORE-MEDIATED INDIRECT EFFECTS OF AN INVASIVE PLANT ON A NATIVE PLANT

Theory predicts that damage by a shared herbivore to a secondary host plant species may either be higher or lower in the vicinity of a preferred host plant species. To evaluate the importance of ecological factors, such as host plant proximity and density, in determining the direction and strength of such herbivore-mediated indirect effects, we quantified oviposition by the exotic weevil Rhinocyllus conicus on the native wavyleaf thistle Cirsium undulatum in midgrass prairie on loam soils in the upper Great Plains, USA. Over three years (2001-2003), the number of eggs laid by R. conicus on C. undulatum always decreased significantly with distance (0-220 m) from a musk thistle (Carduus nutans L.) patch. Neither the level of R. conicus oviposition on C. undulatum nor the strength of the distance effect was predicted by local musk thistle patch density or by local C. undulatum density (<5 m). The results suggest that high R. conicus egg loads on C. undulatum near musk thistle resulted from the native thistles co-occurrence with the coevolved preferred exotic host plant and not from the weevils response to local host plant density. Mean egg loads on C. undulatum also were greater at sites with higher R. conicus densities. We conclude that both preferred-plant proximity and shared herbivore density strongly affected the herbivore-mediated indirect interaction, suggesting that such interactions are important pathways by which invasive exotic weeds can indirectly impact native plants.

Community‐level net spillover of natural enemies from managed to natural forest

Edge effects in fragmented natural habitats may De exaceroateci by intensive land use in the surrounding landscape. Given that most managed systems have higher primary productivity than adjacent natural systems, theory suggests that bottom-up subsidized consumers are likely to spill over from managed to natural habitats. Furthermore, the magnitude of spillover is likely to differ between generalist and specialist consumers, because of differences in their ability to use the full spectrum of resources. However, it is unknown whether there is indeed asymmetrical spillover of consumers between managed and natural habitats, and whether this is related to resource abundance or the trophic specialization of the consumer. We used flight intercept traps to measure spillover of generalist predators (Vespula wasps, Vespidae) and more specialist predators (106 species of parasitoids, Ichneumonidae and Braconidae) across habitat edges between native New Zealand forest and exotic plantation forest over a summer season. We found net spillover of both generalist and specialist predators from plantation to native forest, and that this was greater for generalists. To test whether natural enemy spillover from managed habitats was related to prey (caterpillar) abundance (i.e., whether it was bottom-up productivity driven, due to increased primary productivity), we conducted a large-scale herbivore reduction experiment at half of our plantation sites, by helicopter spraying caterpillar-specific insecticide over 2.5 ha per site. We monitored bidirectional natural enemy spillover and found that herbivore reduction reduced generalist but not specialist predator spillover. Trophic generalists may benefit disproportionately from high resource productivity in a habitat, and their cross-habitat spillover effects on natural food webs may be an important source of consumer pressure in mosaic landscapes.

Local- vs. landscape-scale indirect effects of an invasive weed on native plants

Abstract Insect-mediated indirect interactions between native plant species recently have been shown to be important determinants of plant performance in a number of ecological communities. However, the potential indirect effects of exotic plant invasion on native plant species are not well understood. We examined whether the presence or proximity of the targeted exotic weed, musk thistle, influences the magnitude of attack on native thistles by the introduced biological control, flowerhead weevil. At the local scale, we quantified weevil egg densities on heads of the native wavyleaf thistle growing at different distances (0 to 100 m) from patches of the exotic thistle. Densities were significantly higher when the native thistle occurred within, vs. 30 to 50 m or 80 to 100 m from, patches of the exotic thistle, indicating a strong local “spillover effect.” At larger scales, we measured egg densities on wavyleaf thistle within grassland landscapes (2.4 × 2.4 km2) with varying infestation densities of the invasive musk thistle. We found that egg densities increased significantly with increasing invasive thistle densities measured at larger site and landscape scales. Because flowerhead weevil feeding substantially reduces seed production of wavyleaf thistle, exotic thistle populations are likely to have indirect negative effects on these native thistles. Our results provide strong empirical evidence that exotic plants can increase the attack on native plant species by maintaining populations of a shared insect herbivore. This finding suggests that persistence of exotic weeds in less-successful biocontrol programs will magnify the nontarget effects of weed biocontrol insects. Nomenclature: Musk thistle, Carduus nutans spp. leiophyllus (Petrovic) Stoj. & Stef. #3 CRUNU; wavyleaf thistle, Cirsium undulatum (Nutt.) Spreng. # CIRUN; flowerhead weevil, Rhinocyllus conicus Frölich. Additional index words: Associational susceptibility, biological control, indirect effects, nontarget effects, spillover effects, thistles.

Apparent competition drives community-wide parasitism rates and changes in host abundance across ecosystem boundaries

Species have strong indirect effects on others, and predicting these effects is a central challenge in ecology. Prey species sharing an enemy (predator or parasitoid) can be linked by apparent competition, but it is unknown whether this process is strong enough to be a community-wide structuring mechanism that could be used to predict future states of diverse food webs. Whether species abundances are spatially coupled by enemy movement across different habitats is also untested. Here, using a field experiment, we show that predicted apparent competitive effects between species, mediated via shared parasitoids, can significantly explain future parasitism rates and herbivore abundances. These predictions are successful even across edges between natural and managed forests, following experimental reduction of herbivore densities by aerial spraying of insecticide over 20 hectares. This result shows that trophic indirect effects propagate across networks and habitats in important, predictable ways, with implications for landscape planning, invasion biology and biological control.

Host Density Drives Spatial Variation in Parasitism of the Alfalfa Weevil, Hypera postica, Across Dryland and Irrigated Alfalfa Cropping Systems

ABSTRACT Classical biological control against the alfalfa weevil, Hypera postica (Gyllenhal), a destructive pest of alfalfa (Medicago sativa L.), has resulted in the establishment of nine parasitoid species in the United States. Despite widespread redistribution of a number of species, there remains little postrelease data on their establishment and potential effectiveness in many regions. I surveyed parasitoids associated with alfalfa weevil larvae across 30 or more sites in eastern Montana and western North Dakota over 2 yr. Replicate sites were sampled in two habitat types that differ in their physical characteristics, flood-irrigated and dryland alfalfa fields. Irrigated systems are more productive but also more intensively disturbed habitats because of increased harvest frequency and repeated flooding. Given evidence that both habitat disturbance and herbivore density, which often increases with productivity, can influence parasitoid dynamics, I predicted that parasitism levels, the relative importance of different species, or both, would differ across these two system types. Of four larval parasitoid species released previously or recovered in the region, two were found in this study, Bathyplectes curculionis (Thomson) and Oomyzus incertus (Ratzenberg), with average levels of parasitism across habitat types and years of 37.2 and 3.5%, respectively. Parasitism levels differed between habitat types, but the effect was driven by concomitant differences in host densities that were higher in irrigated than dryland fields. Parasitoid responses to host density varied across years and species. B. curculionis exhibited positive density dependence in parasitism across sites in 2009 and negative density dependence in 2010 when host densities were higher regionally. In contrast, O. incertus exhibited positive density dependence in 2010. Our results suggest that these species may be differentially effective at different host densities. Thus, variation in host density could represent an important axis along which parasitoids exhibit spatial complementarity in function.