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Cascading Effects of a Highly Specialized Beech-Aphid-Fungus Interaction on Forest

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Cascading Effects of a Highly Specialized Beech-Aphid-Fungus Interaction on Forest A peer-reviewed version of this preprint was published in PeerJ on 17 June 2014. View the peer-reviewed version (peerj.com/articles/442), which is the preferred citable publication unless you specifically need to cite this preprint. Cook-Patton SC, Maynard L, Lemoine NP, Shue J, Parker JD. 2014. Cascading effects of a highly specialized beech-aphid–fungus interaction on forest regeneration. PeerJ 2:e442 https://doi.org/10.7717/peerj.442 1 Cascading effects of a highly specialized beech-aphid-fungus interaction on forest 2 regeneration 3 4 OR: Boogie-woogie aphids shake up tree seedlings 5 6 Susan C. Cook-Patton: Smithsonian Environmental Research Center; [email protected] 7 Lauren Maynard: Smithsonian Environmental Research Center; [email protected] 8 Nathan Lemoine: Florida International University; [email protected] 9 Jessica Shue: Smithsonian Environmental Research Center; [email protected] 10 John D. Parker: Smithsonian Environmental Research Center; [email protected] PrePrints 11 12 1Corresponding author: [email protected] 13 14 Keywords: Fagus grandifolia, Grylloprociphilus imbricator, Scorias spongiosa, seedling 15 survival, forest regeneration 16 17 1 PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.340v1 | CC-BY 4.0 Open Access | received: 31 Mar 2014, published: 31 Mar 2014 17 Abstract 18 19 Specialist herbivores are often thought to benefit the larger plant community, because 20 they prevent their host species from becoming competitively dominant. In contrast, specialist 21 enemies are not generally expected to have negative impacts on non-hosts. However, we 22 describe a cascade of indirect interactions whereby a specialist sooty mold (Scorias spongiosa) 23 colonizes the honeydew from a specialist beech aphid (Grylloprociphilus imbricator), ultimately 24 decreasing the survival of seedlings beneath American beech trees (Fagus grandifolia). A 25 common garden experiment indicated that this mortality resulted from moldy honeydew 26 impairing leaf function rather than from chemical or microbial changes to the soil. In addition, PrePrints 27 aphids consistently colonized the same beech trees regardless of host density, suggesting that 28 seedling-depauperate islands may form beneath these trees. Thus this highly specialized three- 29 way beech-aphid-fungus interaction has the potential to impact local forest regeneration via a 30 cascade of indirect effects. 31 32 33 2 PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.340v1 | CC-BY 4.0 Open Access | received: 31 Mar 2014, published: 31 Mar 2014 33 Introduction 34 Natural enemies play important roles in structuring plant communities (Janzen 1970; 35 Webb and Peart 1999; Carson and Root 2000; Petermann et al. 2008). While specialist enemies 36 (i.e., those that feed on one or a few closely related species) can in some cases remove entire 37 species from the plant community (e.g., Herms and McCullough 2014), they are generally 38 thought to be beneficial overall because they prevent any one species from becoming 39 competitively dominant (Janzen 1970; Connell 1971; Terborgh 2012). Moreover, the loss of 40 specialist enemies can allow plant species to spread aggressively and disrupt natural ecosystems 41 (Keane and Crawley 2002). In contrast, it is not expected that specialist enemies will negatively 42 impact the growth and survival of non-host plant species. However, ecological systems are PrePrints 43 usually made up of complex interaction webs, and species may impact ecologically distant 44 species indirectly, due to changes in either the densities or in the traits of intermediary species 45 (Abrams 1995). 46 Here, we document the negative effects of a highly specialized three-way plant- 47 herbivore-fungal interaction on non-host plant species. Specifically, we examined beech blight 48 aphids (Grylloprociphilus imbricator; Fig. 1a,b), which are common consumers of American 49 beech trees (Fagus grandifolia) in eastern North American forests (Hottes and Frison 1931; 50 Smith 1974; Blackman and Eastop 1994; Aoki et al. 2001). We observed a paucity of seedlings 51 beneath infested beech trees, and we combined observational and experimental data to decipher 52 the underlying mechanisms. With two years of field observations in a mapped 16-ha forest and a 53 common garden experiment, we explored the factors determining aphid distributions across the 54 forest landscape at multiple spatial scales, as well as the consequences of aphids for the forest 55 seedling community. We tested two principal hypotheses: first, the beech-aphid-sooty mold 3 PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.340v1 | CC-BY 4.0 Open Access | received: 31 Mar 2014, published: 31 Mar 2014 56 interaction will have negative effects on seedling communities and second, that this negative 57 effect will results from changes in soil quality. 58 59 Methods 60 Study organisms: Beech blight aphids (Grylloprociphilus imbricator (Fitch); Fig. 1a) are 61 common sights in eastern North American forests. Known colloquially as “boogie-woogie aphids” 62 for their tendency to shake their abdomen when disturbed, these aphids are frequently discussed 63 in environmental blogs and state extension publications (e.g., Childs 2011; Virginia Department 64 of Forestry 2013). Their basic natural history is somewhat described, but their ecology and 65 impacts on co-occurring species is almost entirely uncharacterized. The aphids colonize the PrePrints 66 branches of American beech tree (Fagus grandifolia (Ehrh.)) in autumn. Their fuzzy white 67 bodies form highly conspicuous colonies (Fig. 1b; Hottes and Frison 1931; Smith 1974; 68 Blackman and Eastop 1994; Aoki et al. 2001), which can be up to 1.5 meters in length (Smith 69 1974) and contain thousands of individuals (Aoki et al. 2001). Aphid colonies are made more 70 obvious by the fungal masses that form below them. This fungus (Scorias spongiosa (Schwein.) 71 Fr.) specializes on the aphid’s sugar-rich excrement or “honeydew” (Hughes 1976). S. spongiosa 72 is found primarily in association with Fagus species (Reynolds 1978), but also on Alnus species 73 (Chomnunti et al. 2011). Initially the fungus forms a brown, spongy mass (Fig. 1c) that 74 eventually turns black, hardens, and persists through much of the winter. The fungus also coats 75 the leaves of seedlings directly beneath the aphid colonies (Fig. 1d). We never observed aphid 76 colonies without S. spongiosa suggesting that the aphids either carry the fungus with them, or 77 that the fungus is ubiquitous (but dormant) in the environment. 4 PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.340v1 | CC-BY 4.0 Open Access | received: 31 Mar 2014, published: 31 Mar 2014 78 Experimental site: All field surveys and soil collections occurred in the Smithsonian 79 Environmental Research Center (SERC) Forest Dynamics Plot (38° 53’ 11.4822”, - 76° 33’ 80 31.2464”). In this 16-ha plot, the diameter and spatial location of all woody species > 1.0 cm dbh 81 are known. Each hectare of the SERC Forest Dynamics Plot is divided into 100 10m x 10m 82 subplots. We selected 12 to 13 evenly spaced subplots in each hectare (Fig. 2A; N = 204) and we 83 censused every adult beech tree (N = 659) within these subplots. For a random subset of the 84 subplots (N = 258, N = 129 per year), we also had light availability and soil moisture data. We 85 collected light availability data in August 2011 using an AccuPAR LP-80 ceptometer to record 86 photosynthetically available light in the center of each plot, taking all measurements between 87 11am and 4pm on a mostly cloudless day. We then collected ambient light measurements from a PrePrints 88 nearby, unshaded area and calculated ‘light transmittance’ as the fraction of light in each forested 89 location relative to ambient light. We collected soil moisture data in June 2011 using a 90 Fieldscout TDR 300, with two soil moisture measurements taken from the southwest corner of 91 each 10m x 10m subplot. 92 Field survey: We first explored the spatial and temporal dynamics of the beech-aphid- 93 fungus interaction within the forest, and asked whether this specialized three-way interaction had 94 negative effects on the seedling community. During the last week of September 2012 and the 95 third week of October 2013, we recorded aphid infestation on the focal beech trees. Aphids 96 usually only colonized a single branch or a cluster of connected branches, and were packed 97 densely along that branch. We therefore scored the intensity of damage on each tree using an 98 ordinal scale: 0 = no aphids, 1 = presence of aphids, 2 = greater than 30 cm of branch covered by 99 aphid colony, and 3 = greater than 100 cm of branch covered with aphids. In the second week of 100 October 2012, we also selected 19 focal beech trees that occurred within the northwest hectare of 5 PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.340v1 | CC-BY 4.0 Open Access | received: 31 Mar 2014, published: 31 Mar 2014 101 the SERC Forest Dynamics Plot. We chose trees that were 10-20 cm dbh, because the trees in 102 this size class were sufficiently large (only 7% of trees were bigger), common, and varied in 103 aphid infestation status. Six of the focal beech trees had no aphids, seven had an aphid score of 104 two, and six had an aphid score of three. We individually tagged and identified every woody 105 seedling within 1-m of the focal tree (N = 575 total; 30 per adult on average, ranging from 7 to 106 58), measured its initial height, and noted whether its leaves were directly coated in sooty mold. 107 In mid-June 2013, we returned to these seedlings to reassess height and survival. 108 Common Garden Experiment: We also asked whether the impacts of the beech-aphid- 109 fungal interaction were soil related.
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