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Forest Decline Differentially Affects Trophic Guilds of Canopy-Dwelling

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Forest Decline Differentially Affects Trophic Guilds of Canopy-Dwelling bioRxiv preprint doi: https://doi.org/10.1101/2020.02.11.943753; this version posted February 12, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Forest decline differentially affects trophic guilds of canopy-dwelling beetles 2 3 Guilhem Parmain1, Benoît Nusillard1, Xavier Pineau2, Ravène Brousse2, Tiphanie Fontaine- 4 Guenel1,2, Romain Ledet1, Cécile Vincent-Barbaroux2, Christophe Bouget1*, Aurélien Sallé2* 5 6 1 INRAE, UR EFNO, Domaine des Barres, Nogent-sur-Vernisson, France 7 2 Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRAE, Université d'Orléans, 8 45067, Orléans, France 9 * both authors contributed equally to this work 10 11 Submitted to Annals of Forest Science 12 13 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.11.943753; this version posted February 12, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 14 Abstract 15 Key message 16 Decline can affect the structure, resources and microclimates of the forest canopy, and 17 potentially have cascading effects on canopy-dwelling species. Our survey shows that an oak 18 decline can promote saproxylic beetles, especially xylophagous ones, and generalist 19 phyllophagous weevils. However, it negatively affects specialist phyllophagous species and has 20 no effect on seminiphagous weevils. 21 Context 22 Decline in a context of climate change is expected to induce considerable changes in forest 23 structure, potentially affecting habitat opportunities and trophic resources for numerous species. 24 Nonetheless, the consequences of decline on forest biodiversity have rarely been studied. 25 Aim 26 We aimed to characterize the impact of oak decline on different guilds of canopy-dwelling 27 beetles. 28 Methods 29 Beetles were sampled for three consecutive years in oak stands exhibiting different levels of 30 decline. Several guilds were considered: (i) buprestids, (ii) other saproxylic beetles split into 31 xylophagous and non-xylophagous species, (iii) seminiphagous weevils, and (iv) specialist and 32 generalist phyllophagous weevils. 33 Results 34 Overall, decline had positive effects on the abundance and biomass of beetles, though 35 contrasted variations were observed at the species or guild levels. Xylophagous species, 36 especially the main oak-associated buprestids, and other saproxylic species benefitted from 37 decline conditions. However, at odds with the insect performance hypothesis, decline had a 38 positive effect on generalist phyllophagous species, a negative effect on specialist 39 phyllophagous species, and a null effect on seminiphagous species. 40 Conclusion 41 The increase in species richness for saproxylic and phyllophagous beetle communities suggests 42 that decline might promote forest biodiversity. Our results call for further studies to thoroughly 43 assess the functional outcomes of forest decline, and to suggest management strategies for 44 conservation biologists. 45 46 Keywords: Agrilus, Quercus, saproxylic beetles, phyllophagous beetles, seminiphagous beetles 47 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.11.943753; this version posted February 12, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 48 Introduction 49 50 Global change can dramatically affect the organization and functioning of forest ecosystems by 51 promoting the introduction and establishment of invasive species (Liebhold et al. 2017), by 52 intensifying land-use at the landscape level (Seibold et al. 2019), and through the direct and 53 indirect effects of climate change on forest health (Seidl et al. 2017). Climate change already 54 challenges the ability of European forests to adapt (Allen et al. 2010; Carnicer et al. 2011), and 55 unprecedented forest declines are expected in response to the predicted increase in frequency 56 and severity of droughts and heat waves (Allen et al. 2010; IPCC 2013). 57 Forest decline generally consists in a progressive loss of vigor in the trees, over several years, in 58 response to multiple, successive or concomitant driving factors (Manion 1981). These factors 59 include i) predisposing factors such as site conditions that constantly affect the stands, ii) 60 contributing factors such as defoliation or droughts that trigger declines, and inciting factors such 61 as secondary pests and pathogens, which aggravate the deleterious effects of contributing 62 factors, ultimately killing trees (Manion 1981; Thomas et al. 2002; Sallé et al. 2014). The gradual 63 loss of tree vigor progressively affects all forest compartments but the canopy is certainly the 64 first to exhibit conspicuous modifications as decline progresses. The crown of a declining tree is 65 characterized by an accumulation of dead branches, cavities and opportunistic fungi, but also by 66 reduced foliage density and decreased seed production (Houston 1981; Ishii et al. 2004). 67 Therefore, forest decline tends to increase the structural complexity of the canopy at stand, tree 68 and branch scales and considerably modifies the corresponding microclimates (Ishii et al. 2004). 69 Such profound structural modifications affect habitat opportunities and trophic resources, with 70 likely marked cascading effects on canopy-dwelling communities. 71 72 The tree canopy and the soil are the two key compartments supporting forest biodiversity and 73 their contribution is tremendous (Stork and Grimbacher 2006). Compared to tropical forests, 74 temperate forests have less vertical stratification and a more marked seasonality with leaf fall, so 75 temperate forest canopies probably shelter a lower proportion of specific taxa (Ulyshen 2011). 76 Canopy functional biodiversity in temperate forests has therefore received relatively little 77 attention to date (Ulyshen 2011). However, the studies conducted in temperate forests (e.g. 78 Bouget et al. 2011; Vodka and Cizek 2013; Plewa et al. 2017) have shown a clear vertical 79 stratification of insect assemblages, just as in tropical forests, with 20 – 40% of all forest insect 80 species strictly associated with canopies (Bouget et al. 2011). In addition to these specialist 81 species, many Arthropods also rely on the canopy for a part of their life cycle, for maturation 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.11.943753; this version posted February 12, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 82 feeding and mating on foliage, for instance (Ulyshen 2011; Sallé et al. 2014). However, canopies 83 are still relatively unknown biotic frontiers. These crown ecosystems harbor poorly understood, 84 rarely described (both in terms of composition and abundance) insect communities (Bouget et al. 85 2011). They potentially shelter an underestimated pool of rare or patrimonial species (Plewa et 86 al. 2017), but also native and invasive pests. 87 88 Canopy modifications in response to decline may change resource availability and microclimates 89 and may create novel colonization opportunities, thus modulating in different ways the 90 community dynamics of canopy-dwelling insects, depending on their functional guilds. Changes 91 in foliage quality during plant stress may influence the performance of leaf feeders, but the 92 magnitude and orientation of the herbivore response likely depends on both stress intensity and 93 the feeding strategy of the herbivore (Larsson 1989; Herms and Mattson 1992). In addition, the 94 decrease in the number of living branches in the canopy of declining trees may also negatively 95 affect leaf-, seed-, and flower-feeding species (Martel and Mauffette 1997). A survey of 96 Lepidopteran communities in declining maple stands indicated that exposed caterpillars became 97 more abundant while the density of semi-concealed or endophagous species decreased (Martel 98 and Mauffette 1997). This suggests that phyllophagous or seminiphagous insects with an 99 intimate relationship with their host-tree, like specialist species with an endophytic larval 100 development, may be negatively affected by the decrease in foliage quantity or quality and/or the 101 change in microclimate, while these modifications might promote generalist species (Martel and 102 Mauffette, 1997). Conversely, saproxylic beetles are likely to show a marked positive response 103 to forest decline, both in terms of abundance and species richness. Saproxylic beetles form a 104 functional guild associated with dead and decaying wood, related microhabitats, and other 105 saproxylic taxa (Stokland et al. 2012). This guild also includes xylophagous species developing 106 on weakened trees and acting as secondary pests, like the buprestids (Coleoptera: 107 Buprestidae), which are aggravating agents during declines (Sallé et al., 2014; Tiberi et al. 108 2016). The weakened trees and the accumulation of dead wood and related microhabitats 109 typically of declining
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