Beavers, Bugs and Chemistry: a Mammalian Herbivore Changes Chemistry Composition and Arthropod Communities in Foundation Tree Species
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Article Beavers, Bugs and Chemistry: A Mammalian Herbivore Changes Chemistry Composition and Arthropod Communities in Foundation Tree Species Rachel M. Durben 1,2, Faith M. Walker 1,2,3, Liza Holeski 1,2,4, Arthur R. Keith 1,2, Zsuzsi Kovacs 1,2, Sarah R. Hurteau 5, Richard L. Lindroth 4 , Stephen M. Shuster 1,2 and Thomas G. Whitham 1,2,* 1 The Environmental Genetics and Genomics Laboratory, Department of Biological Sciences, Northern Arizona University, P.O. Box 5640, Flagstaff, AZ 86011, USA; [email protected] (R.M.D.); [email protected] (F.M.W.); [email protected] (L.H.); [email protected] (A.R.K.); [email protected] (Z.K.); [email protected] (S.M.S.) 2 The Center for Adaptable Western Landscapes, Department of Biological Sciences, Northern Arizona University, P.O. Box 5640, Flagstaff, AZ 86011, USA 3 School of Forestry, Northern Arizona University, Flagstaff, AZ 86001, USA 4 Department of Entomology, University of Wisconsin-Madison, Madison, WI 53706, USA; [email protected] 5 Geography and Environmental Studies Department, University of New Mexico, Albuquerque, NM 87131, USA; [email protected] * Correspondence: [email protected] Citation: Durben, R.M.; Walker, F.M.; Abstract: The North American beaver (Castor canadensis Kuhl) and cottonwoods (Populus spp.) are Holeski, L.; Keith, A.R.; Kovacs, Z.; foundation species, the interactions of which define a much larger community and affect a threatened Hurteau, S.R.; Lindroth, R.L.; riparian habitat type. Few studies have tested the effect of these interactions on plant chemistry Shuster, S.M.; Whitham, T.G. Beavers, and a diverse arthropod community. We experimentally examined the impact of beaver foraging Bugs and Chemistry: A Mammalian on riparian communities by first investigating beaver food preferences for one cottonwood species, Herbivore Changes Chemistry Fremont cottonwood (P. fremontii S. Watson), compared to other locally available woody species. Composition and Arthropod We next examined the impact of beaver foraging on twig chemistry and arthropod communities Communities in Foundation Tree in paired samples of felled and unfelled cottonwood species in northern Arizona (P. fremontii) and Species. Forests 2021, 12, 877. southwestern Colorado (narrowleaf cottonwood, P. angustifolia James, and Eastern cottonwood, https://doi.org/10.3390/f12070877 P. deltoides W. Bartram ex Marshall). Four major patterns emerged: (1) In a cafeteria experiment, Academic Editors: Ben Moore and beavers chose P. fremontii six times more often than other woody native and exotic species. (2) With Julianne O’Reilly-Wapstra two cottonwood species, we found that the nitrogen and salicortin concentrations were up to 45% greater and lignin concentration 14% lower in the juvenile resprout growth of felled trees than the Received: 29 May 2021 juvenile growth on unfelled trees (six of seven analyses were significant for P. fremontii and four Accepted: 1 July 2021 of six were significant for P. angustifolia). (3) With two cottonwood species, arthropod community Published: 3 July 2021 composition on juvenile branches differed significantly between felled and unfelled trees, with up to 38% greater species richness, 114% greater relative abundance and 1282% greater species diversity Publisher’s Note: MDPI stays neutral on felled trees (six of seven analyses with P. fremontii and four of six analyses with P. angustifolia with regard to jurisdictional claims in were significant). The above findings indicate that the highest arthropod diversity is achieved in the published maps and institutional affil- heterogenous stands of mixed felled and unfelled trees than in stands of cottonwoods, where beavers iations. are not present. These results also indicate that beaver herbivory changes the chemical composition in 10 out of 13 chemical traits in the juvenile growth of two of the three cottonwood species to potentially allow better defense against future beaver herbivory. (4) With P. deltoides, only one of five analyses in chemistry was significant, and none of the four arthropod community analyses were significant, Copyright: © 2021 by the authors. suggesting that this species and its arthropod community responds differently to beaver. Potential Licensee MDPI, Basel, Switzerland. reasons for these differences are unknown. Overall, our findings suggest that in addition to their This article is an open access article impact on riparian vegetation, other mammals, birds, and aquatic organisms, beavers also may define distributed under the terms and the arthropod communities of two of three foundation tree species in these riparian ecosystems. conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Forests 2021, 12, 877. https://doi.org/10.3390/f12070877 https://www.mdpi.com/journal/forests Forests 2021, 12, 877 2 of 18 Keywords: beaver; Castor canadensis; cottonwood; Populus spp.; chemistry; arthropod communities; foundation species 1. Introduction The ecological processes that structure communities are fundamental aspects of ecol- ogy and evolution. Holling [1] proposed that “a small set of plant, animal, and abiotic processes structure ecosystems across scales in time and space”. In other words, not all species are equal, and a few are likely to contribute disproportionately to the structure and evolution of communities and ecosystems. Species that are strong interactors, affecting many other species and modifying their environments (e.g., dam building and selective foraging by beavers; shading and cooling of the understory by tree canopies) likely play a major role in structuring communities. Dayton [2] defined a foundation species as “a single species that defines much of the structure of a community by creating locally stable conditions for other species, and by modulating and stabilizing fundamental ecosystem processes”. Ellison et al. [3] reviewed this literature and concluded that dominant species, keystone species, ecosystem engineers and other strong interactors all fall within this category of foundation species. Because all ecosystems of the world likely have multiple and potentially interacting foundation species, it is especially important to identify and understand the interactions of these species as their loss due to global change (including climate change, invasive species, and altered species interactions) could cascade to affect the rest of the community [4]. Keith et al. [5,6] proposed and experimentally tested the interacting foundation species hypothesis and found that the interactions of two foundation species better explained community diversity, stability and species interaction networks than either one alone. Beavers and cottonwoods are considered foundation species because their presence in an ecosystem has far-reaching effects on community dynamics and ecosystem processes [3]. By felling trees that are used for food and construction activities (e.g., building dams that slow water flow and create ponds and lodges), beavers affect fish populations [7], stream flow and water temperature [8,9], nutrient cycling and availability [9–11], individual species and communities of arboreal arthropods [12–14], the composition of mixed cottonwood riparian forests and their genetic composition [15], communities of aquatic arthropods [16], vegetation diversity [17], tree architecture [18], and genetic diversity and productivity at the individual tree level [19]. Even in areas where beavers are no longer active but have cut trees and built dams in the recent past, their impact is evident in the structure of the riparian zone and has long-term effects on vegetation types [9,11,20–23]. Compared with the amount of land they cover, riparian corridors contain disproportionately high biodiversity [24] and are an important resource for birds and mammals. In the arid southwest USA, the narrow riparian “ribbon of green” (Figure1A) has been shown to support exceptionally high bird [25] and vegetation diversity [26]. However, the extent to which beavers interact with a foundation tree species to affect arthropod diversity in these southwestern stream systems has not been studied (but see [14]). One mechanism by which beaver herbivory might affect arthropod diversity is by altering the chemistry of the plants they browse. To determine whether there was a difference in twig chemistry between the juvenile resprout growth of beaver-felled trees (Figure1B), and the juvenile shoots at the base of unfelled trees, we collected samples from each to assess the concentrations of a suite of chemicals known to be present in these tissues. Since beavers eat the inner bark, or cambium layer of trees [27], we chose to sample twig tissue to quantify how beaver herbivory might affect the phytochemistry of resprouting cottonwoods for future feeding by beavers. While we cannot extrapolate on how twig chemistry may influence foliar arthropods, we were also interested in understanding how herbivory by beavers may differentially affect arthropods on multiple cottonwood species, which has not previously been examined in this system. Forests 2021, 12, 877 3 of 18 Forests 2021, 12, x FOR PEER REVIEW 3 of 18 (A) (B) (C) (D) Figure 1. (AFigure) Riparian 1. (A “ribbon) Riparian of green” “ribbon of ofP. fremontii green” of nearP. fremontii Moab, UT;near (B Moab,) Resprout UT; growth (B) Resprout of P. angustifolia growth of after felling by beavers;P. (C angustifolia) Leaf rollingafter moth felling (Anacampsis by beavers; niveopulvella (C) Leaf rollingChambers, moth 1875;