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705241 1 .Pdf Edinburgh Research Explorer A spatial perspective on the phenological distribution of the spring woodland caterpillar peak Citation for published version: Shutt, JD, Burgess, MD & Phillimore, AB 2019, 'A spatial perspective on the phenological distribution of the spring woodland caterpillar peak', The American Naturalist. https://doi.org/10.1086/705241 Digital Object Identifier (DOI): 10.1086/705241 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: The American Naturalist General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 30. Sep. 2021 vol. 194, no. 5 the american naturalist november 2019 E-Article A Spatial Perspective on the Phenological Distribution of the Spring Woodland Caterpillar Peak Jack D. Shutt,1,* Malcolm D. Burgess,2,3 and Albert B. Phillimore1 1. Institute of Evolutionary Biology, University of Edinburgh, King’s Buildings, Edinburgh EH9 3FL, United Kingdom; 2. Centre for Research in Animal Behaviour, University of Exeter, Exeter, Devon EX4 4QG, United Kingdom; 3. RSPB Centre for Conservation Science, The Lodge, Sandy, Bedfordshire SG19 2DL, United Kingdom Submitted October 23, 2018; Accepted April 19, 2019; Electronically published August 28, 2019 Online enhancements: appendix. Dryad data: https://doi.org/10.5061/dryad.71568mt. – abstract: A classic system for studying trophic mismatch focuses caterpillar insectivorous passerine bird food chain in tem- on the timing of the spring caterpillar peak in relation to the breed- perate deciduous woodlands (Visser et al. 1998; Both et al. ing time and productivity of woodland passerine birds. Most work 2006; Charmantier et al. 2008). At the center of this food has been conducted in single-site oak woodlands, and little is known chain is the ephemeral annual spring caterpillar peak, which about how insights generalize to other woodland types or across space. varies in height (i.e., abundance/biomass) and timing from Here we present the results of a 3-year study on the species composi- year to year (Southwood et al. 2004; Forkner et al. 2008). In tion and temporal distribution of the spring caterpillar peak on differ- deciduous woodlands, this peak coincides with the timing ent tree taxa across 40 woodland sites spanning 27 of latitude in Scot- land. We used molecular barcoding to identify 62 caterpillar species, of newly emerged leaves before they become tanninized and with winter moth (Operophtera brumata) being the most abundant, less palatable (Feeny 1970; van Asch and Visser 2007). Breed- comprising one-third of the sample. Oak (Quercus sp.) and willow ing in synchrony with this peak is of vital importance for the (Salix sp.) hosted significantly higher caterpillar abundances than other productivity of some passerine birds, such as certain tit (Pa- tree taxa, with winter moth exhibiting similar trends and invariantly ridae)andflycatcher (Ficedula) species (Both et al. 2004; proportionate across tree taxa. Caterpillar peak phenology was broadly Visser et al. 2006; Burger et al. 2012). similar between tree taxa. While latitude had little effect, increasing Despite its central position, the caterpillar peak is the least elevation increased the height of the caterpillar peak and retarded tim- ing by 3.7 days per 100 m. These findings extend our understanding of well understood component of this food chain, with its tim- how mismatch may play out spatially, with caterpillar peak date vary- ing and abundance having been predominantly studied in- ing with elevation and tree taxa varying in the caterpillar resource that directly through frass fall (fecal matter; Visser et al. 1998; they host. Smith et al. 2011) or half-fall (intercepting fully grown cater- pillars of certain species falling to earth to pupate; Charm- Keywords: host tree species, Lepidoptera caterpillars, oak Quercus, phenology, trophic mismatch, winter moth Operophtera brumata. antier et al. 2008; Hinks et al. 2015) and usually in the context of oak-dominated (Quercus sp.) woodlands (Charmantier et al. 2008; Smith et al. 2011; Burgess et al. 2018). These stan- Introduction dard methods for monitoring caterpillar biomass have lim- — itations, with frass not revealing caterpillar species compo- Trophic mismatches where asynchrony between a con- sition or the contribution made by other invertebrates and sumer and an ephemeral resource negatively impacts the ’ fi — half-fall capturing only the full-grown larvae of species that consumer s tness have received much research attention descend to ground level, which may not correlate perfectly (Durant et al. 2007; Forrest and Miller-Rushing 2010). One – with the arboreal abundance of earlier life stages of these of the most popular study systems is the deciduous tree species or caterpillars of other species that do not descend. Temperate deciduous woodlands comprise many differ- ent tree species across wide latitudinal and elevational gra- * Corresponding author; email: [email protected]. dients, and the passerine birds studied as part of this food ORCIDs: Shutt, https://orcid.org/0000-0002-4146-8748; Burgess, https:// chain typically forage and nest in a variety of woodland types orcid.org/0000-0003-1288-1231; Phillimore, https://orcid.org/0000-0002-6553 -1553. (Perrins 1979; Blair and Hagemeijer 1997). To understand – q whether this induces spatial variation in phenological mis- Am. Nat. 2019. Vol. 194, pp. E000 E000. 2019 by The University of Chicago. fi 0003-0147/2019/19405-58820$15.00. All rights reserved. match, we rst need to gain insight into how the temporal DOI: 10.1086/705241 distribution of caterpillars varies spatially and on tree species This content downloaded from 129.215.132.009 on September 03, 2019 02:57:39 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). E000 The American Naturalist other than oak. Several aspects of the seasonal caterpillar buffering hypothesis) or habitats provide a resource that is peak could vary, including the height (peak biomass), tim- available for a longer duration. ing of the peak date (phenology), and breadth (duration) of In temperate deciduous woodlands, the spring caterpil- the peak (fig. 1A). In locations or years when mismatch be- lar peak is often dominated by one or two abundant spe- tween the timing of peak avian demand and the timing of cies (Hunter 1992; Butler and Strazanac 2000; Wesolowski the oak caterpillar peak is pronounced, deleterious effects and Rowinski 2006), such as winter moth (Operophtera bru- on avian productivity could be buffered locally by a differ- mata) in Europe (Hunter 1992; Wesolowski and Rowinski ing caterpillar peak timing on other tree species providing 2006). The winter moth is a trophic generalist feeding on a alternative resources (Burger et al. 2012; fig. 1B; tree spe- broad range of tree and shrub species (Kerslake and Hartley cies buffering hypothesis) or at the landscape scale by better 1997; Wesolowski and Rowinski 2006; Waring and Town- matched caterpillar peaks at other locations (fig. 1D;land- send 2017) and a major dietary component for small wood- scape buffering hypothesis). Alternatively, a degree of buff- land passerines, especially for nestlings (Visser et al. 1998; ering might arise if some caterpillar species (fig. 1C;dietary Wilkin et al. 2009; Cholewa and Wesołowski 2011). Close A B Tree A Tree B Tree C b h pd undance C D Caterpillar A Location A Caterpillar B Location B Caterpillar ab Caterpillar C Location C Date Figure 1: Schematic of potential temporal distributions of arboreal caterpillar biomass peaks in spring. A, Parameters of caterpillar temporal distribution that could vary. Abbreviations: pd p peak date; h p height of the peak; b p breadth (duration) of the peak (50% of total peak). B–D, Different contributions to variation in caterpillar temporal distributions. B, Tree species buffering hypothesis: how different tree taxa may have different caterpillar temporal distributions, with tree B showing a later peak than trees A and C and tree C having a lower, longer peak than trees A and B. C, Dietary buffering hypothesis: how different caterpillar species may show different spring peaks even on the same tree, with caterpillar A having the highest peak and caterpillar C having the longest. D, Landscape buffering hypothesis: how geographical locations could have differently timed spring caterpillar peaks, with locations A and B sharing a similar peak date and location C having a later peak date. This content downloaded from 129.215.132.009 on September 03, 2019 02:57:39 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). The Spring Woodland Caterpillar Peak E000 synchrony of winter moth larval hatching with host leaf developmental rates of Lepidopteran larvae (Buse et al. 1999; bud burst is important for growth and survival (Feeny 1970; Bale et al. 2002; Hodkinson 2005). This is seen in the timing Buse and Good 1996; van Asch et al. 2007), and the same of the caterpillar biomass peak, which is delayed by approx- has been found for some other spring-feeding caterpillar spe- imately 1.3 days for each degree of latitude northward in UK cies (Klemola et al. 2003; van Asch and Visser 2007). Leafing oak woodlands (Smith et al. 2011; Burgess et al. 2018). The phenology of deciduous temperate tree species responds to timing of the caterpillar peak is also likely to delay with in- spring temperature (Polgar and Primack 2011; Roberts et al.
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