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Temporal Resource Continuity Increases Predator Abundance in a Metapopulation Model: Insights for Conservation and Biocontrol

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Temporal Resource Continuity Increases Predator Abundance in a Metapopulation Model: Insights for Conservation and Biocontrol land Article Temporal Resource Continuity Increases Predator Abundance in a Metapopulation Model: Insights for Conservation and Biocontrol Brian Spiesman 1, Benjamin Iuliano 2,* and Claudio Gratton 2,3 1 Department of Entomology, Kansas State University, Manhattan, KS 66506, USA; [email protected] 2 Department of Integrative Biology, University of Wisconsin-Madison, Madison, WI 53726, USA; [email protected] 3 Department of Entomology, University of Wisconsin-Madison, Madison, WI 53726, USA * Correspondence: [email protected] Received: 18 October 2020; Accepted: 24 November 2020; Published: 28 November 2020 Abstract: The amount of habitat in a landscape is an important metric for evaluating the effects of land cover on biodiversity, yet it fails to capture complex temporal dimensions of resource availability that could be consequential for species population dynamics. Here, we use a spatially-explicit predator–prey metapopulation model to test the effect of different spatiotemporal resource patterns on insect predators and their prey. We examined population responses in model landscapes that varied in both the amount and temporal variability of basal vegetation. Further, we examined cases where prey comprised either a single generalist species or two specialist species that use different resources available either early or late in the growing season. We found that predators and generalist prey benefitted from lower temporal variance of basal resources, which increased landscape-scale abundances. However, increasing the amount of basal resources also increased the variability of generalist prey populations. Specialist prey, on the other hand, did not benefit from less temporally variable basal resources, as they were restricted by habitat type, while also suffering greater predation. Predators achieved greater prey suppression in landscapes with less temporally variable resources, but the overall effects on prey abundance depended on prey habitat specialization. Our simulations demonstrate the joint importance of both the amount and temporal variability of resources for understanding how landscape heterogeneity influences biodiversity and ecosystem services such as the biological control of agricultural pests. Keywords: predator–prey interactions; landscape ecology; agroecosystems; ecosystem services; biological control; resource complementation 1. Introduction The abundance and diversity of species in a landscape generally increase with greater habitat area [1], presumably because larger areas can provide more limiting resources to consumers. This is a central principle of biodiversity conservation and the conservation of beneficial species that provide ecosystem services in working landscapes. For example, increasing non-crop habitat surrounding agricultural fields can promote insect abundance, diversity, pollination, and natural pest control [2–6]. Yet, a facile understanding of habitat versus non-habitat or cropland versus natural area ignores the substantial heterogeneity that exists within land use categories [6] as well as the complex temporal dynamics of mobile consumers and their resources [7–9]. “Landscape complementation” describes the processes in which mobile organisms acquire key resources by traversing multiple patch types in a landscape [10]. This process may be especially important in Land 2020, 9, 479; doi:10.3390/land9120479 www.mdpi.com/journal/land Land 2020, 9, 479 2 of 16 Land 2020, 9, x FOR PEER REVIEW 2 of 17 agriculturally-dominatedavailability brought about landscapes, by landscape where temporal simplifica gapstion—e.g., or bottlenecks increasing in food annu availabilityal cropland brought area about or by landscapedecreasing simplification—e.g., crop diversity—may increasing negatively annual croplandaffect beneficial area or decreasing species cropthat diversity—mayrequire nourishment negatively affectcontinuously beneficial speciesthroughout that require the growing nourishment season continuously [8]. Differences throughout in the composition the growing of season habitats [8]. between Differences inlandscapes the composition can result of habitats in differential between temporal landscapes patte canrns result of resource in differential availability temporal for mobile patterns consumers. of resource availabilityIn homogenous for mobile landscapes, consumers. temporal In homogenous gaps co landscapes,uld result temporal if ephemeral gaps could resources result if ephemeralemerge synchronously across different patches (Figure 1A,C) and then disappear for the rest of the growing resources emerge synchronously across different patches (Figure1A,C) and then disappear for the rest of the season (e.g., before planting or after harvesting in a monocropped landscape). Although mobile growing season (e.g., before planting or after harvesting in a monocropped landscape). Although mobile organisms could travel within a landscape to access potential food resources in different locations, organisms could travel within a landscape to access potential food resources in different locations, there may be there may be temporal gaps at critical points in the organism’s life cycle that could affect growth, temporal gaps at critical points in the organism’s life cycle that could affect growth, survival, and reproduction. survival, and reproduction. On the other hand, food resources in different habitat patches could Onemerge the other asynchronously hand, food resources (Figure in different1B,D). Such habitat asynchrony patches could creates emerge an asynchronouslyensemble of temporally (Figure1B,D). Suchcomplementary asynchrony patches creates anthat ensemble minimize ofs resource temporally gaps complementary and, for mobile patches species,that results minimizes in continuous resource gapsresource and, forprovisioning mobile species, at a landscape results in scale continuous over the resource course provisioningof a season (e.g., at a landscapein a landscape scale of over thephenologically course of a season divergent (e.g., annual in a landscape and perennial of phenologically crops). We refer divergent to this process annual as “temporal and perennial resource crops). Wecomplementation”. refer to this process as “temporal resource complementation”. FigureFigure 1. 1. ConceptualConceptual diagrams diagrams (left) (left) and and corresponding corresponding model model landscapes landscapes (right) (right)for landscapes for landscapes with withdifferent different proportions proportions of ofhigh-resource high-resource habitat habitat (pR (pmaxR)max and) and temporal temporal variance variance (CV (CVR). RGray). Gray lines lines representrepresent the the amount amount of resourcesof resources provided provided by early-season by early-season habitat habitat (gray patches).(gray patches). Black linesBlack represent lines therepresent amount the of amount resources of providedresources byprovided late-season by late-season habitat (blackhabitat patches). (black patches). White White patches patches provide consistentlyprovide consistently few basal few resources basal resources year-round. year-round. Panels (PanelsA–D) show(A–D) model show landscapesmodel landscapes with di withfferent patternsdifferent of patterns resource of amount resource and amount continuity. and continuity. Land 2020, 9, 479 3 of 16 The value of temporal resource complementation has received empirical support in beneficial insects such as wild bees, which can benefit from the existence of temporally asynchronous floral resources in heterogeneous landscapes [11–13]. However, less is known about how temporal resource complementation affects predatory arthropods, the dynamics of tritrophic interactions, and the consequences for conservation biological control [9]. A population of mobile predators may track ephemeral prey resources across a landscape as they emerge in one location, decline, and then emerge in another. Yet, a predator population’s ability to track herbivorous prey depends on the prey’s ability to track their own resources, constituted by the vegetation present in the landscape (hereafter, “basal resources”). Habitat-generalist prey may benefit more from temporal resource complementation than habitat-specialists if mobile generalists can utilize multiple basal resource types that emerge in different locations throughout the season. Such generalist prey may thus support larger predator populations over time than would specialist prey. However, it is not clear whether (1) an increase in predator population size would enhance generalist prey suppression or (2) lower predator density could maintain suppression of specialist prey. This latter scenario might be especially relevant to biological control in agroecosystems, where many pests specialize on particular crop types (e.g., cereals or legumes), but are frequently consumed by generalist predators such as spiders or lady beetles. Because of the difficulty of conducting empirical studies rigorously investigating the spatio-temporal dynamics of insect populations across multiple generations, modeling approaches are frequently employed [14–16]. For example, Le Gal et al. [17] recently modeled the effect of overwintering (i.e., seminatural) habitat amount and arthropod species traits on multiple indicators of pest control services, finding that landscapes with more overwintering habitat supported earlier visitation and improved pest suppression by natural enemies; yet the study does not consider how temporal heterogeneity in the crop mosaic itself “cascades up” to higher trophic levels when predators
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