Insect herbivory and avian insectivory in novel native oak forests: Divergent effects of stand size and connectivity
Introduction
Forest fragmentation is well-known to alter patterns of species distribution and abundance, relationships between organisms and resulting ecosystem processes (Ewers and Didham, 2006, Fahrig, 2017, Haddad et al., 2015, Lindenmayer and Fisher, 2013). Among others, it exerts strong effects on trophic cascades such as plant-herbivore-predator interactions, eventually affecting rates of tree damage and health (Bagchi et al., 2018, Chávez-Pesqueira et al., 2015, Rossetti et al., 2017). While forest fragmentation continues to occur in many regions of the world, forest cover is increasing in many others as a consequence of active planting and passive afforestation following rural abandonment (Fuchs et al., 2015, Hansen et al., 2013). For instance, Europe has experienced a steady increase of forested surfaces by 0.8 million ha per year since 1990 (Forest Europe, 2015), a trend that is expected to continue in the coming decades (Fuchs et al., 2015, Schroter, 2005). Habitat defragmentation through passive afforestation has been proposed as an effective tool to reinforce biodiversity and ecosystem functioning in rural and urban landscapes where forest stands were formerly sparse and isolated (Fischer et al., 2006, Rey Benayas et al., 2008, Rey Benayas and Bullock, 2012). Yet little ecological research has to date focused on newly established native forest stands and we largely ignore whether trophic interactions in such stands underlie similar mechanisms as in remnants of similar sizes but resulting from forest fragmentation.
Novel native forest stands establish from a few founder trees that colonize an available habitat patch within an unsuitable matrix through long-distance dispersal and fill their neighbourhood with their offsprings (Gerzabek et al., 2017, Sezen et al., 2005). Such stands share certain characteristics that set them apart from those created by fragmentation: (i) they typically are quite small-sized – even smaller than the smallest fragments of remnant forest; (ii) they are dominated by young trees, resulting in a reduced amount and range of habitats available to forest-dwelling species (Franklin, 1988, Fuller et al., 2018); and (iii) all their species necessarily originate from colonization events over a limited period of time, implying that these systems are triggered by immigration credit instead of extinction debt (Jackson and Sax, 2010). Recent studies on insect and bird species richness along chronosequences of novel native forest development have shown that these are rapidly colonized by woodland generalists whereas specialists can still remain absent even 150 years after forest establishment (Fuentes-Montemayor et al., 2015, Fuller et al., 2018, Whytock et al., 2018). These studies also revealed that local stand characteristics are relatively more important than landscape characteristics for successful colonization by insects and birds. Similar findings have been reported for planted forests (reviewed in Burton et al., 2018). However, their consequences for trophic relationships between plants, insect herbivores and insectivores remain unknown.
Despite the differences between novel native forest stands and remnant forest fragments, the ecological mechanisms underlying trophic cascades involving trees, insect herbivores and birds can to some extent be inferred from fragmentation studies. These have documented that the size and connectivity of forest stands can shape trophic cascades very differently depending on the relative importance of the bottom-up and top-down effects involved (De La Vega et al., 2012, Rossetti et al., 2014). Thus, small and isolated forest stands provide less and possibly lower-quality resources to herbivores (Chávez-Pesqueira et al., 2015) and their colonization requires longer-distance movements that increase energetic and fitness costs (O’Rourke and Petersen, 2017), eventually resulting in lower herbivore abundance (De La Vega et al., 2012, Simonetti et al., 2007). However, small stands also experience greater edge effects which typically go along with increased herbivory (Bagchi et al., 2018, De Carvalho Guimarães et al., 2014). On the other hand, insect herbivores are more likely to colonize small but closer novel forest stands while their predatory vertebrates are more likely to colonize more distant but larger ones (Barbaro et al., 2014, Bereczki et al., 2014, Cooper et al., 2012, Maguire et al., 2015).
There is broad consensus that, generally, predators can notably reduce insect herbivory by regulating herbivore populations (Böhm et al., 2011, Letourneau et al., 2009, Maguire et al., 2015, Rosenheim, 1998). However, their actual relevance in novel native forest stands depends strongly on how both prey and predators respond to stand size and connectivity (Gripenberg and Roslin, 2007). This study investigated how levels of insect herbivory, avian predation and the abundance and diversity of insectivorous birds in recently established native Pedunculate oak (Quercus robur) forest stands are influenced by their size and the cover of broadleaf forest in the surrounding landscape. Specifically, we addressed the following questions: (i) Does herbivory increase or decrease along gradients of increasing stand size and connectivity? (ii) Does avian predation increase or decrease along the same gradients? (iii) Are the observed trends related with the local abundance and diversity of insectivorous birds? We contrast our findings with those reported from studies of forest fragmentation and discuss implications in a context of increasing forest connectivity following ongoing changes in landscape use and management (Burton et al., 2018, Rey Benayas and Bullock, 2012).
Section snippets
Study area and selection of study sites
The study was carried out in the Landes de Gascogne region (south-western France) about 40 km southwest of Bordeaux (44°41′N, 00°51′W). The region is characterized by an oceanic climate with mean annual temperature of 12.8 °C and annual precipitation of 873 mm over the last 20 years. The area is covered by extensive plantations of maritime pine (Pinus pinaster Ait.) interspersed with small stands of broadleaved forests that are dominated by Pedunculate oak (Quercus robur) and contain Pyrenean
Results
Insect herbivory was on average (± se, n = 72) 8.02 ±4.51% (Table A1). The effect of stand size on herbivory depended on the connectivity of the stand (significant Size × Connectivity interaction, Table 1): herbivory tended to increase with stand size in landscapes with a low stand connectivity whereas it decreased in landscape where broadleaf forests where more abundant (Fig. 1). Neither avian predation on plasticine caterpillars nor bird abundance or richness had a significant effect on
Discussion
Our study revealed that the size and connectivity of novel native forest stands affect herbivorous insects and insectivorous birds in different ways. While the abundance of leaf miners depended on stand connectivity alone, herbivory by chewers and skeletonizers was influenced by an interplay between stand size and connectivity, and bird abundance (but not species richness) showed consistent independent and opposite responses to stand size and connectivity. This divergence of relationships is
Acknowledgements
We thank Christophe Poileux, Victor Rébillard, Fabrice Vetillard and Elias Garrouj for their technical assistance in the field and in the laboratory. We also thank two anonymous reviewers for helpful comments. E.V.C was founded by the project SPONFOREST (grant BIODIVERSA 2015-58).
Author contributions
E.V.C., B.C., A.H and I.V.H conceived the study and acquired the data. E.V.C and B.C analysed the data. E.V.C., B.C and A.H drafted the first version of the manuscript. All authors wrote the final version of the manuscript.
References (78)
- et al.
Effects of host-plant population size and plant sex on a specialist leaf-miner
Acta Oecol.
(2011) - et al.
Effects of forest heterogeneity on the efficiency of caterpillar control service provided by birds in temperate oak forests
For. Ecol. Manage.
(2014) - et al.
Reviewing the evidence base for the effects of woodland expansion on biodiversity and ecosystem services in the United Kingdom
For. Ecol. Manage.
(2018) - et al.
Synthesizing habitat fragmentation effects on plant-antagonist interactions in a phylogenetic context
Biol. Conserv.
(2015) - et al.
Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover
Trends Ecol. Evol.
(2010) - et al.
Ambient temperature affects the utility of plasticine caterpillar models as a tool to measure activity of predators across latitudinal and elevational gradients
Biol. Control
(2019) - et al.
Extending the ‘resource concentration hypothesis’ to the landscape-scale by considering dispersal mortality and fitness costs
Agric. Ecosyst. Environ.
(2017) - et al.
Inquiring into the causes of depressed folivory in a fragmented temperate forest
Acta Oecol.
(2009) - et al.
Herbivory and seedling performance in a fragmented temperate forest of Chile
Acta Oecol.
(2007) - et al.
Landscape supplementation in adjacent savannas and its implications for the design of corridors for forest birds in the central Cerrado
Brazil. Biol. Conserv.
(2004)
Anthropogenic fragmentation of landscapes: mechanisms for eroding the specificity of plant–herbivore interactions
Oecologia
Comparative responses of bird, carabid, and spider assemblages to stand and landscape diversity in maritime pine plantation forests
Ecoscience
Bird functional diversity enhances insectivory at forest edges: a transcontinental experiment
Divers. Distrib.
Diversity and abundance of birds in relation to forest fragmentation, habitat quality and heterogeneity
Bird Study
Top-down control of herbivory by birds and bats in the canopy of temperate broad-leaved oaks (Quercus robur)
PLoS One
Species interactions regulate the collapse of biodiversity and ecosystem function in tropical forest fragments
Ecology
Bird assemblages in forest fragments within Mediterranean mosaics created by wild fires
Landsc. Ecol.
Are fragments Islands? Landscape context and density-area relationships in boreal forest birds
Am. Nat.
Bottom-up and top-down effects of tree species diversity on leaf insect herbivory
Ecol. Evol.
Egg mortality in the pine processionary moth: habitat diversity, microclimate and predation effects
Agric. For. Entomol.
A meta-analysis of crop pest and natural enemy response to landscape complexity
Ecol. Lett.
Intermediate fragmentation per se provides stable predator-prey metapopulation dynamics
Ecol. Lett.
A meta-analysis of the effects of fragmentation on herbivorous insects
Environ. Entomol.
Is top-down control by predators driving insect abundance and herbivory rates in fragmented forests?
Austral. Ecol.
Honeydew feeding increased the longevity of two egg parasitoids of the pine processionary moth
J. Appl. Entomol.
Ecological processes that affect populations in complex landscapes
Nord. Soc. Oikos
Plant population size and isolation affect herbivory of Silene latifolia by the specialist herbivore Hadena bicruris and parasitism of the herbivore by parasitoids
Oecologia
Confounding factors in the detection of species responses to habitat fragmentation
Biol. Rev. Camb. Philos. Soc.
Ecological Responses to Habitat Fragmentation Per Se
Annu. Rev. Ecol. Evol. Syst.
Rethinking patch size and isolation effects: the habitat amount hypothesis
J. Biogeogr.
Biodiversity, ecosystem function resilience: ten guiding principle commodity production landsca
Front. Earth Sci.
Forest Europe (2015) State of Europe’s forests 2015. Ministerial Conference on the Protection of Forests in Europe: Forest Europe, UNECE and FAO. State of Europe’s Forests 2015. Status and Trends in Sustainable Forest Management in Europe, 2015. [WWW Document]
Minist. Conf. Prot. For. Eur. For. Eur. UNECE FAO
An {R} companion to applied regression
Structural and functional diversity in temperate forests
Gross changes in reconstructions of historic land cover/use for Europe between 1900 and 2010
Glob. Chang. Biol.
Are woodland creation schemes providing suitable resources for biodiversity? Woodland moths as a case study
Biodivers. Conserv.
Local-scale attributes determine the suitability of woodland creation sites for Diptera
J. Appl. Ecol.
Fragment size affects plant herbivory via predator loss Lucy
Oikos
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