James T. Cronin

THE MATRIX ENHANCES THE EFFECTIVENESS OF CORRIDORS AND STEPPING STONES

Conservation strategies often call for the utilization of corridors and/or stepping stones to promote dispersal among fragmented populations. However, the extent to which these strategies increase connectivity for an organism may depend not only on the corridors and stepping stones themselves, but also on the composition of the surrounding matrix. Using an herbivore–host-plant system consisting of the planthopper Prokelisia crocea and its sole host plant, prairie cordgrass (Spartina pectinata), we show that the effectiveness of corridors and stepping stones for promoting planthopper dispersal among patches depended strongly on the intervening matrix habitat. In a low-resistance matrix (one that facilitates high rates of interpatch dispersal), both stepping stones and corridors promoted high connectivity, increasing the number of colonists by threefold relative to patches separated by matrix habitat only. The effectiveness of stepping stones and corridors was significantly lower in a high-resistance matrix...

Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle

Feedback from community interactions involving mutualisms are a rarely explored mechanism for generating complex population dynamics. We examined the effects of two linked mutualisms on the population dynamics of a beetle that exhibits outbreak dynamics. One mutualism involves an obligate association between the bark beetle, Dendroctonus frontalis and two mycangial fungi. The second mutualism involves Tarsonemus mites that are phoretic on D. frontalis (“commensal”), and a blue-staining fungus, Ophiostoma minus. The presence of O. minus reduces beetle larval survival (“antagonistic”) by outcompeting beetle-mutualistic fungi within trees yet supports mite populations by acting as a nutritional mutualist. These linked interactions potentially create an interaction system with the form of an endogenous negative feedback loop. We address four hypotheses: (1) Direct negative feedback: Beetles directly increase the abundance of O. minus, which reduces per capita reproduction of beetles. (2) Indirect negative feedback: Beetles indirectly increase mite abundance, which increases O. minus, which decreases beetle reproduction. (3) The effect of O. minus on beetles depends on mites, but mite abundance is independent of beetle abundance. (4) The effect of O. minus on beetles is independent of beetle and mite abundance. High Tarsonemus and O. minus abundances were strongly correlated with the decline and eventual local extinction of beetle populations. Manipulation experiments revealed strong negative effects of O. minus on beetles, but falsified the hypothesis that horizontal transmission of O. minus generates negative feedback. Surveys of beetle populations revealed that reproductive rates of Tarsonemus, O. minus, and beetles covaried in a manner consistent with strong indirect interactions between organisms. Co-occurrence of mutualisms embedded within a community may have stabilizing effects if both mutualisms limit each other. However, delays and/or non-linearities in the interaction systems may result in large population fluctuations.

Host–parasitoid spatial ecology: a plea for a landscape-level synthesis

A growing body of literature points to a large-scale research approach as essential for understanding population and community ecology. Many of our advances regarding the spatial ecology of predators and prey can be attributed to research with insect parasitoids and their hosts. In this review, we focus on the progress that has been made in the study of the movement and population dynamics of hosts and their parasitoids in heterogeneous landscapes, and how this research approach may be beneficial to pest management programs. To date, few studies have quantified prey and predator rates and ranges of dispersal and population dynamics at the patch level—the minimum of information needed to characterize population structure. From host–parasitoid studies with sufficient data, it is clear that the spatial scale of dispersal can differ significantly between a prey and its predators, local prey extinctions can be attributed to predators and predator extinction risk at the patch level often exceeds that of the prey. It is also evident that populations can be organized as a single, highly connected (patchy) population or as semi-independent extinction-prone local populations that collectively form a persistent metapopulation. A prey and its predators can also differ in population structure. At the landscape level, agricultural studies indicate that predator effects on its prey often spill over between the crop and surrounding area (matrix) and can depend strongly on landscape structure (e.g. the proportion of suitable habitat) at scales extending well beyond the crop margins. In light of existing empirical data, predator–prey models are typically spatially unrealistic, lacking important details on boundary responses and movement behaviour within and among patches. The tools exist for conducting empirical and theoretical research at the landscape level and we hope that this review calls attention to fertile areas for future exploration.

MATRIX COMPOSITION AFFECTS THE SPATIAL ECOLOGY OF A PRAIRIE PLANTHOPPER

To date, there is a lack of well-controlled field experiments that disentangle the effects of the intervening matrix from other landscape variables (e.g., patch geography or quality) that might influence animal dispersal among patches. We performed a field experiment to investigate how the movement of a delphacid planthopper (Prokelisia crocea) among discrete patches of prairie cordgrass (Spartina pectinata) is affected by the composition of the matrix (mudflat, native nonhost grasses, and the introduced grass smooth brome [Bromus inermis]). Within each matrix type, marked planthoppers were released onto experimental cordgrass patches that were made identical in size, isolation, and host plant quality. We found that the emigration rate (planthoppers lost per patch per day) was 1.3 times higher for patches embedded in the two nonhost grass matrix types than for patches in mudflat. The rate of immigration (immigrants per patch per day) into patches isolated by 3 m was 5.4 times higher in the brome than in the mudflat matrix. Patches in the native grass matrix had intermediate immigration rates. In addition, a survey of planthopper distributions in nature revealed that both the within- and among-patch distributions of the planthopper were related to the composition of the matrix. Within patches, individuals accumulated against mudflat edges (relative to patch interiors) but not against nonhost grass edges. Among patches, incidence and density increased with the proportion of the matrix composed of open mud. The matrix was equal to that of patch geography (size and isolation) in its ability to explain the distribution of the planthopper. We suggest that the low permeability of the mudflat relative to a nonhost grass edge may explain these planthopper distributional patterns. Also, because natural cordgrass patches in mudflat were richer in nutrients than those in nonhost grasses, planthoppers may have been more likely to remain and build up densities on the former patches. We predict that the displacement of native matrix types by invasive brome will result in increased connectivity and greater spatial synchrony in densities of planthoppers among cordgrass patches.

Response of Native Insect Communities to Invasive Plants

Invasive plants can disrupt a range of trophic interactions in native communities. As a novel resource they can affect the performance of native insect herbivores and their natural enemies such as parasitoids and predators, and this can lead to host shifts of these herbivores and natural enemies. Through the release of volatile compounds, and by changing the chemical complexity of the habitat, invasive plants can also affect the behavior of native insects such as herbivores, parasitoids, and pollinators. Studies that compare insects on related native and invasive plants in invaded habitats show that the abundance of insect herbivores is often lower on invasive plants, but that damage levels are similar. The impact of invasive plants on the population dynamics of resident insect species has been rarely examined, but invasive plants can influence the spatial and temporal dynamics of native insect (meta)populations and communities, ultimately leading to changes at the landscape level.

MOVEMENT AND SPATIAL POPULATION STRUCTURE OF A PRAIRIE PLANTHOPPER

The transfer of organisms among patches is a key process influencing the spatial structure and regional dynamics of a population; yet, detailed experimental studies of animal movement among patches are uncommon. I performed a series of mark–recapture studies to quantify the movement of a planthopper, Prokelisia crocea (Hemiptera: Delphacidae), among discrete patches of its host plant, prairie cordgrass (Spartina pectinata). Results from these dispersal studies were used to predict the natural distributions and to characterize the spatial population structure of P. crocea. Planthopper emigration loss per patch increased linearly with the density of female conspecifics and was nonlinearly related to patch size (small > large > intermediate sized patches). Planthopper spatial spread was diffusive and 2.7 times faster among cordgrass patches in a heterogeneous habitat (patches embedded in nonhost vegetation) than within a homogeneous habitat (pure cordgrass). Immigration by planthoppers was an increasing function of patch size but was independent of patch isolation (at the scale of this study). The natural distribution of planthoppers in a prairie fragment, obtained from a survey of 146 cordgrass patches over five generations, was well predicted from the dispersal experiments. Planthopper densities and patch occupancy rates were positively correlated with patch size (cordgrass patches ≥0.8 ha were continually occupied), but uncorrelated with patch isolation. Based on this survey, the rate of patch extinction was 21% per generation, highest in small and moderately isolated patches, and approximately equal to the recolonization rate per generation. Finally, the dynamics of local patch populations were asynchronous, even for patch pairs <10 m apart. I conclude that P. crocea exhibits a population structure most closely resembling a mainland–island metapopulation, but with high patch connectivity. Under these circumstances, processes operating within the few mainland patches are probably more important than regional processes (patch extinctions/recolonizations) in influencing population persistence. Corresponding Editor: N. J. Gotelli.

SPIDER EFFECTS ON PLANTHOPPER MORTALITY, DISPERSAL, AND SPATIAL POPULATION DYNAMICS

Nonlethal (trait-mediated) effects of predators on prey populations, particularly with regard to prey dispersal, scarcely have been considered in spatial ecological studies. In this study, we report on the effects of spider predators on the mortality, dispersal, and spatial population dynamics of Prokelisia crocea planthoppers (Hemiptera: Delphacidae) in a prairie landscape. Based on a three-generation survey of host-plant patches (Spartina pectinata; Poaceae), the density of cursorial and web-building spiders declined significantly with increasing patch size (a pattern the opposite of that for the planthopper). Independent of patch size effects, an increase in the density of web-building and cursorial spiders had a negative effect on planthopper density in one of three generations each. Finally, the likelihood of extinction of local (patch) populations of planthoppers increased significantly with an increase in the density of web-building spiders. Planthoppers in small host-plant patches with high densit...

MATRIX HETEROGENEITY AND HOST–PARASITOID INTERACTIONS IN SPACE

In this study, I experimentally examined how the landscape matrix influenced the movement, oviposition behavior, and spatial distribution of Anagrus columbi, a common egg parasitoid of the planthopper Prokelisia crocea. Both species exist among discrete patches of prairie cordgrass (Spartina pectinata), the sole host plant of P. crocea. Based on out-planted cordgrass pots bearing host eggs (to assess parasitism) or sticky leaves (traps for adult A. columbi), I found that the distribution of adult female A. columbi and pattern of ovipositions within a cordgrass patch were strongly matrix dependent. Female densities were 59% lower on the edge than interior of patches embedded in a mudflat matrix, but were evenly distributed within patches embedded in a matrix consisting of either native grasses or the exotic grass smooth brome (Bromus inermis). In contrast, parasitism was higher in the interior than edge for patches in all three matrix types. The lack of correspondence between A. columbi density and parasitism was attributed to differences in oviposition behavior: A. columbi parasitized 71% more hosts per capita in the interior than edge for patches embedded in nonhost grasses, but equal numbers on the edge and interior of patches embedded in mudflat. Matrix-dependent differences in the within-patch distribution and oviposition behavior of A. columbi can influence the distribution of parasitism risk and host–parasitoid stability at the patch level. Matrix composition also affected the pattern of movement through the matrix and the colonization of nearby cordgrass patches. Anagrus columbi females emigrating from a mudflat-embedded patch were captured at very low, but constant, numbers with distance out into the matrix, suggesting that they were reluctant to enter or remain in the mudflat. In contrast, A. columbi females entering a nonhost grass matrix had numbers that were high near the patch border and then declined exponentially with distance. These patterns of movement were likely responsible for the very different colonization rates for experimental patches embedded in different matrix types and located 3 m from a source patch of A. columbi. Patches embedded in brome were colonized at a rate that was 3.0 and 5.7 times higher than for patches in native grass or mudflat, respectively. Finally, based on a census of cordgrass patches spanning five generations, A. columbi densities and proportion of patches occupied generally increased with increasing host density, patch isolation, and the proportion of the surrounding matrix that was mudflat. Patch size had no effect on the distribution of A. columbi. Overall, these data suggest that cordgrass patches in a nonhost grass matrix, particularly smooth brome, have high connectivity relative to patches in a mudflat matrix. Changes in connectivity due to changes in matrix composition can significantly influence host–parasitoid persistence at the metapopulation level. Corresponding Editor (ad hoc): J. A. Rosenheim.

AN INVASIVE PLANT PROMOTES UNSTABLE HOST–PARASITOID PATCH DYNAMICS

In theory, the rate of interpatch dispersal significantly influences the population dynamics of predators and their prey, yet there are relatively few field experiments that provide a strong link between these two processes. In tallgrass prairies of North America, the planthopper, Prokelisia crocea, and its specialist parasitoid, Anagrus columbi, exist among discrete host-plant patches (prairie cordgrass, Spartina pectinata). In many areas, the matrix, or habitat between patches, has become dominated by the invasive exotic grass, smooth brome (Bromus inermis). We performed a landscape-level field study in which replicate cordgrass networks (identical in number, size, quality, and distribution of cordgrass patches) were embedded in a matrix composed of either mudflat (a native matrix habitat) or smooth brome. Mark–recapture experiments with the planthopper and parasitoid revealed that the rate of movement among cordgrass patches for both species was 3–11 times higher in smooth brome than in mudflat. Within three generations, planthopper and parasitoid densities per patch were on average ∼50% lower and spatially 50–87% more variable for patches embedded in a brome as compared to a mudflat matrix. A brome-dominated landscape also promoted extinction rates per patch that were 4–5 times higher than the rates per patch in native mudflat habitat. The effect was more acute for the parasitoid. We suggest that the differences in population dynamics between networks of patches in brome and those in mudflat were driven by underlying differences in interpatch dispersal (i.e., patch connectivity). To our knowledge, this is the first experimental study to reveal that matrix composition, in particular, the presence of an invasive plant species, affects the spatial and temporal dynamics of an herbivore and its natural enemy.

PATCH STRUCTURE, OVIPOSITION BEHAVIOR, AND THE DISTRIBUTION OF PARASITISM RISK

To date, almost no experimental field studies have attempted to assess the factors that generate heterogeneity in the distribution of parasitism risk, a putative indicator of host–parasitoid stability. In this study, I examined the interaction between a planthopper Prokelisia crocea and its egg parasitoid Anagrus columbi among discrete patches of prairie cordgrass, Spartina pectinata. In particular, I examined how patch geography and host distribution within a patch influenced the distribution of adult parasitoids, parasitoid oviposition behavior, the proportion of hosts parasitized, and the aggregation of parasitism (cv2) and adult parasitoids. Based on six generations of census data, the distribution of parasitism was strongly aggregated within (cv2 = 3.58), but not among (cv2 = 0.58) cordgrass patches. Parasitism was also spatially and temporally density independent. To determine what influences the distribution of parasitism risk, I selected 26 discrete cordgrass patches, removed all sources of A. columbi, and then quantified the immigration and subsequent oviposition behavior of A. columbi colonists. I found that the number of immigrants significantly increased with patch size and decreased with patch isolation. Patch size had no influence on the per capita hosts parasitized per leaf, but there was a significant twofold increase in per capita attacks from the least to the most isolated patches. The isolation effect was likely due to an optimal oviposition response to dispersal distance by A. columbi. For these experimental patches, substantial within-patch aggregation of parasitism (cv2 = 1.63) did not translate into strong among-patch aggregation (cv2 = 0.13). Searching adult parasitoids were randomly distributed within and among patches and thus did not explain the high cv2 within patches. Interestingly, the aggregation of parasitism risk within a patch was significantly negatively correlated with patch size and positively correlated with patch isolation. The distribution of parasitism risk could be divided into two general components. The within-parasitoid component was attributable to individuals engaging in multiple ovipositions within a leaf and the distance-dependent oviposition response. The latter response was likely the cause for the variation in cv2 with respect to patch size and isolation. Within-parasitoid aggregation has no effect on host–parasitoid stability. The among-parasitoid component of aggregation appears to have been due to heterogeneity in the vulnerability of hosts and an edge effect (parasitism risk is 60% more heterogeneous at the edge than interior of a patch) and is in theory stabilizing. Consequently, a change in landscape structure that leads to an increase in cordgrass edge habitat may promote a more stable host–parasitoid interaction. Corresponding Editor: R. F. Denno.