DOI: 10.5061/dryad.n5tb2rc1s
title: Periodical cicadas disrupt trophic dynamics via community-level shifts in Avian Foraging

description: Once every 13 or 17 years within eastern North American deciduous forests,
 billions of periodical cicadas concurrently emerge from the soil and
 briefly satiate a diverse array of naive consumers, offering a rare
 opportunity to assess the cascading impacts of an ecosystem-wide resource
 pulse on a complex food web. Here, we quantify the effects of the 2021
 Brood X emergence, and report that &gt;80 bird
 species opportunistically switched their foraging to include cicadas,
 releasing herbivorous insects from predation, and essentially doubling
 both caterpillar densities and accumulated herbivory levels on host oak
 trees. These short-lived but massive emergence events help us to
 understand how resource pulses can rewire interaction webs and disrupt
 energy flows in ecosystems, with potentially long-lasting
 effects.   
description: Avian Foraging Observations
 (2021) Throughout the Brood X cicada emergence (May 15 -
 June 24, 2021), teams of 1-3 researchers used binoculars to observe and
 record the foraging behavior of individual birds at our main study site,
 the Izaak Walton League Conservation Farm (IWL hereafter), located in
 Poolesville, Maryland, USA (39.095, -77.432). Avian foraging observations
 were made in a variety of habitats including managed fields, a pond,
 deciduous forest understory, deciduous forest edge, and old field. A
 foraging observation began when an identifiable bird attempted to consume
 food items or transport food and ended when the bird was no longer
 visible. The observations took place between the 0700 and 1400 hours, and
 ranged in duration from 5 seconds to 4 minutes. Prey items were easily
 classified as cicada or non-cicada, due to the conspicuous size and color
 of cicadas in relation to other common prey items. Bird trait data
 (feeding guild, size) were extracted from the Elton trait dataset
 (<em>51</em>) or from the Cornell Lab of Ornithology All About
 Birds website (<em>52</em>). For our focal dataset containing
 both cicada and non-cicada foraging observations (<strong>Table
 S3</strong>), we analyzed the effect of bird size and feeding guild
 on the likelihood that a foraging bout included a cicada. The analysis
 used binomial GLMM with bird size (g) and feeding guild (insectivores:
 ​​N=11
 spp., n=69 observations; omnivores: N=10 spp., n=​​76; granivores: N=8
 spp., n=72) as fixed effects, and species as a random effect using
 ​​​​lme4
 (<em>53</em>), with emmeans (<em>54</em>) for
 post-hoc comparisons in R (<em>55</em>). Because we recorded
 detailed foraging data for only a single frugivorous bird species (the
 cedar waxwing, <em>Bombycilla cedrorum</em>) and for no
 species of carnivores/scavengers, we did not include those as categories
 in this analysis. To supplement our own data collection, we enlisted the
 assistance of the larger recreational birding community with a campaign
 entitled ‘Brood X Bird Feast’ (<em>56</em>). Participants were
 provided protocols and datasheets for observations of both cicada and
 non-cicada foraging events. A second citizen-science project initiated by
 the coordinators for the 3rd Maryland-DC Breeding Bird Atlas
 (<em>57</em>) included observations of bird species observed
 foraging on cicadas, but did not record incidences of birds foraging on
 non-cicada food sources (<strong>Table S2</strong>). We used a
 complete list of the birds of ​​Maryland (<em>58</em>) to construct a
 pruned phylogeny of the local avian community
 (<strong>Fig. S1</strong>), excluding birds that
 were extinct or vagrants based on their typical habitat range as detailed
 on the Cornell Lab of Ornithology All About Birds website
 (<em>52</em>). We mapped lineages that contained
 cicada-feeding individuals (one or more observed instances of
 cicada-feeding from our combined foraging datasets) on this pruned
 phylogeny using the ape package in R
 (<em>59</em>).    Avian
 Predation
 (2020-2022) At IWL,
 from May to July (2020) and May-August (2021-2022), we conducted weekly
 inspections of 5-cm long plasticine caterpillar models (<strong>Fig.
 3a</strong>) affixed with a drop of cyanoacrylate adhesive
 (‘superglue’) to branches of 20 understory white oak trees &lt;3m
 tall. Focal trees were located adjacent to a small forest trail in the
 interior of a closed canopy second growth oak-hickory forest approximately
 2.5 km upslope from the Potomac River (39.101, -77.420). Four model
 caterpillars were affixed to each tree every week, and were replaced with
 fresh plasticine caterpillars immediately following inspection one week
 later (N= 80 caterpillars observed/week). All plasticine caterpillars were
 inspected in the field using 10x hand lenses to identify predation marks
 (<em>60</em>). The vast majority of marks were clearly made by
 birds (i.e., were distinctive beak imprints); a variety of attacks by
 non-bird predators, including various arthropods and even a snail, were
 recorded, but we restricted our predation analysis to those models
 exhibiting definitive bird strikes. During the spring and summer of 2021
 (the Brood X emergence year), we concurrently deployed an additional set
 of caterpillar models on planted white oak saplings growing in the
 BiodiversiTREE plots (<em>61</em>) of the Smithsonian
 Environmental Research Center (SERC; 38.834, -76.557); this second study
 site is located about 100 km east of IWL in Edgewater, MD. Because the
 white oak saplings at SERC were somewhat smaller than those at IWL, we
 placed 2 plasticine caterpillars/sapling on each of 30 saplings (N = 60
 caterpillars observed each week) to maintain a comparable density/tree.
 The proportion of caterpillar models/sapling that were attacked by birds
 was compared among years and censuses (at the IWL site only), between
 sites (SERC vs. IWL in 2021), and among censuses within sites using
 repeated measures GLMM (link = "logit") followed by EMM [emmeans package
 (54)] post-hoc comparisons in R.
     Insect Herbivore Surveys
 (2021-2022) At our
 IWL site, we non-destructively recorded the abundance and identity of each
 externally-feeding folivore (predominantly caterpillars, sawflies, and
 beetles; <strong>Table S4</strong>) present on the foliage or
 stems of 25 understory white oak saplings with accessible branches
 (&lt; 3m tall). Most insects were identified to species; a small
 number were assigned to morphospecies. These censuses were conducted in
 mid-May (just prior to the appearance of adult cicadas at IWL in 2021) and
 again in late June of 2021, 2022, and 2023. Covid-related restrictions
 precluded the collection of herbivore data in the first year of the study
 (2020); hence we sampled the oak herbivore community for an extra year
 (2023), enabling us to compare the herbivore community sampled in the
 emergence year (2021) to the two subsequent non-emergence years (2022 and
 2023). The May census was timed to sample the distinct insect herbivore
 fauna associated with young expanding oak foliage, which by late May gives
 way to an entirely different summer herbivore fauna that feeds exclusively
 on mature oak leaves (<em>62</em>). The June census was timed
 to sample the summer herbivores that were present during the cicada
 emergence at the study site in 2021. During the June censuses, we also
 recorded the size of the most abundant caterpillar species
 (<em>Acronicta increta</em>: Noctuidae) as small (larval
 instars 1-2) or large (larval instars 3-5). For each census, herbivore
 abundance was calculated by summing counts across taxa, and sampling
 effort was quantified by counting the total number of leaves examined per
 tree. We compared insect herbivore abundances among years with generalized
 linear models, using ln-transformed total number of leaves as an offset,
 to test for among-year differences in abundance of 1) total herbivores and
 2) the most common free-feeding caterpillar (<em>Acronicta
 increta</em>: Noctuidae). The distribution of counts was
 over-dispersed (variance &gt; mean) and violated Poisson assumptions;
 we therefore applied negative binomial GLMs with the log-link, followed by
 posthoc comparisons of means across years with Tukey family-wise
 adjustments of p-values. One-way ANOVAs on herbivore densities
 (free-feeding herbivore/leaf) yielded qualitatively similar results and
 thus are not reported here. Additionally, we used Fisher’s exact tests to
 compare the frequencies of small (instars 1-2) vs. large (instars 3-5)
 <em>A. increta</em> caterpillars censused during the late June
 census of each year.     Herbivore Damage Surveys
 (2020-2022) We
 conducted non-destructive herbivory censuses in early June and mid-October
 of each year to estimate the damage to understory white oak trees incurred
 from feeding by the spring herbivore community (pre-cicada) and from the
 summer/fall herbivore community (during and post-cicada). In each census,
 we visually estimated (to the nearest 1.0%) the amount of leaf tissue
 missing from each of 30 leaves randomly selected from throughout the crown
 of each tree (N = 30 understory white oak saplings; damage estimated for
 900 total leaves per census). Prior to each census, our team of observers
 trained on a set of damaged leaves with known percent damage (measured in
 the field using the LeafByte app (<em>63</em>). During the
 fall census, 30 randomly selected leaves were harvested from each tree and
 analyzed using LeafByte for a more precise measure of total accumulated
 herbivory. For each year, the damage acrrued between the spring and fall
 herbivory<em> </em>surveys was estimated by subtracting the
 median % damage of the early June census from the median % damage of the
 October census for each tree. The means of these median differences
 (accrued herbivory) were then compared among years with one-way ANOVA
 followed by EMM (emmeans)
 post-hoc comparisons in R (<em>54</em>). Because
 the median % damage values were skewed by small values and bounded by
 zero<em>,</em> we also converted percentages to proportions
 and applied beta regression using the ‘betareg’ package in R
 (<em>64</em>)<em>. </em>Because the results were
 qualitatively identical, we report the simpler ANOVA
 results. 
description: R is needed to open the analysis scripts. 
description: # Dataset 1 of 4: BirdForaging Once every 13 or 17 years within eastern
 North American deciduous forests, billions of periodical cicadas
 concurrently emerge from the soil and briefly satiate an entire guild of
 naive consumers, offering a rare opportunity to assess the cascading
 impacts of an ecosystem-wide resource pulse on a complex food web. To test
 the effect of the cicada emergence on bird foraging behavior, we observed
 bird foraging using binoculars throughout the Brood X cicada emergence
 (May 15 - June 24, 2021), in and around the Izaak Walton League
 Conservation Farm located in Poolesville, MD. We combined our observations
 with those of two citizen science projects. Combined, our team and local
 birders recorded 983 individual birds from 82 different species foraging
 on periodical cicadas throughout the Mid-Atlantic portion of the Brood X
 range. to produce a total of 983 individual bird observations from (82
 different species. These birds spanned more than three orders of magnitude
 in body mass, ranging in size from &lt;7g (blue-gray gnatcatchers) to
 &gt;11,000g (trumpeter swans), and represented, included all major
 avian feeding guilds that eat insects. Our team's focal observations
 of avian foraging during the eight-week-long emergence at our study site
 in central Maryland indicated that 52% of all foraging bouts (N = 229)
 involved periodical cicadas. Surprisingly, the proportion of foraging
 bouts that included cicadas did not vary among feeding guild (df = 2, χ2=
 3.6, P = 0.31) or with birds of all sizes (df =1, χ 2 = 0.65, P = 0.42).
 The enormous biomass pulse created by the emergence shifted the adaptive
 foraging of mobile, generalist consumers (birds) to a superabundant prey
 resource (cicadas), releasing insect herbivore populations from predation
 and doubling herbivory on oak trees. ## Description of the data and file
 structure Column Headers: Scientific- The scientific name of the bird
 observed is formatted as "Genus species". NameCode- The 4-letter
 species code based on the Bird Banding Laboratory standard bird codes.
 Date- The date that the observation data in this row was collected is
 formatted as mm/dd/yy. Week- The week that the observation data in this
 row was collected, e.g. "Week 1". Week 1-4 data collection took
 place in May, Week 5-8 took place in June, Week 9-12 took place in July,
 and Week 13-14 took place in August. Location- The location where the
 observation occurred. LengthOfObservation- The length of the observation
 in seconds. An observation began when a bird was observed, and ended when
 the bird was no longer visible. Observations where the observed bird did
 not eat anything were discarded. NumberOfCicadasEaten- The number of
 cicadas eaten by an individual bird during an observation period.
 NumberOfNonCicadasEaten- Number of non-cicada items eaten by an individual
 bird during an observation period. Diet- The Diet classification of the
 bird species as determined by the EltonTraits 1.0 dataset
 [https://doi.org/10.1890/13-1917.1](https://doi.org/10.1890/13-1917.1)
 BodyMassValue-The average body mass of the species in grams as determined
 by the EltonTraits 1.0 dataset
 [https://doi.org/10.1890/13-1917.1](https://doi.org/10.1890/13-1917.1).
 CicadaBinary-This is If a bird consumed a cicada during an observation
 period NA-In the data set, cells filled with "NA" indicate that
 data was not available for that particular bird species in the EltonTraits
 1.0 dataset. Methods: Throughout the Brood X cicada emergence (May 15 -
 June 24, 2021), teams of 1-3 researchers used binoculars to record the
 foraging behavior of individual birds in and around our main study site,
 the Izaak Walton League Conservation Farm (IWL hereafter), located in
 Poolesville, Maryland, USA (39.095, -77.432), with additional observations
 in urban and suburban habitats around Washington, DC. Avian foraging
 observations took place in a variety of habitats including managed fields,
 a pond, deciduous forest understory, deciduous forest edge, and old field.
 A foraging observation began when an identifiable bird attempted to
 consume food items or transport food and ended when the bird was no longer
 visible. The observations varied in duration from 5 seconds to 4 minutes
 between the hours of 7am and 2pm. Prey items were easily classified as
 cicada or non-cicada, due to the conspicuous size and color of cicadas in
 relation to other prey items. Bird trait data (feeding guild, size) were
 extracted from the Elton trait dataset (36). For our focal data set,
 containing observations of both cicada-feeding a​nd non-cicada feeding, we
 analyzed the effect of bird size and feeding guild on the likelihood that
 a foraging bout included a cicada, using binomial GLMM with bird size (g)
 and feeding guild (insectivores:N=11 spp., n=69; omnivores: N=10 spp.,
 n=​​76; granivores: N=8 spp., n=72) as fixed effects, and species as a
 random effect using ​lme4 (37), with emmeans (38) for post-hoc comparisons
 in R(39). Because we recorded detailed foraging data for only a single
 frugivore (cedar waxwings, Bombycilla cedrorum), we did not include
 frugivores as a category in this analysis. We enlisted the assistance of
 the larger recreational birding community with a campaign entitled
 'Brood X Bird Feast'
 ([https://friendtocicadas.org/brood-x-bird-feastprotocol/](https://friendtocicadas.org/brood-x-bird-feastprotocol/)), providing protocols and datasheets that supplemented our own data collection on both cicada and non-cicada foraging events. ## Sharing/Access information Bird trait data was sourced from EltonTraits 1.0 dataset [https://doi.org/10.1890/13-1917.1](https://doi.org/10.1890/13-1917.1) ## Code/Software Data were analyzed with the script labeled "BirdForagingAnalysis.R". *** # Dataset 2 of 4: BirdPredation Once every 13 or 17 years within eastern North American deciduous forests, billions of periodical cicadas concurrently emerge from the soil and briefly satiate an entire guild of naive consumers, offering a rare opportunity to assess the cascading impacts of an ecosystem-wide resource pulse on a complex food web. We assessed the impact of cicadas on bird predation of caterpillars. We affixed plasticine caterpillar models on white oak saplings. From May to August 2021, we conducted weekly inspections of the caterpillars for evidence of avian predation (i.e., beak marks). Plasticine caterpillar models were replaced weekly. At both sites, the bird strikes on model plasticine caterpillars dipped dramatically during the 2021 season (GLMM, df =24, χ 2 = 102, P &lt; 0.001). Specifically, in May, when the first cicada nymphs began emerging, bird strike frequency declined from \~30% to below 10%, remaining low until early July. when the last adult male cicadas were heard calling (Fig. 43b); by early August, bird strike frequencies had returned to pre-emergence levels. The enormous biomass pulse created by the emergence shifted the adaptive foraging of mobile, generalist consumers (birds) to a superabundant prey resources (cicadas), releasing insect herbivore populations from predation and doubling herbivory on oak trees. ## Description of the data and file structure Data were analyzed using hte file titled "BirdPredationAnalysis.R". #Column headers for data file "BirdPredation.csv" Year- The year the data in this row was collected, e.g."2022". Week- The week that the data in this row was collected, e.g. "Week 1". Week 1-4 data collection took place in May, Week 5-8 took place in June, Week 9-12 took place in July, and Week 13-14 took place in August. TreeNumber- Unique identifying number for individual White Oak (Quercus alba) sapling, e.g. "1". This data should be treated as a factor rather than as a number. Successes- The absolute number of clay caterpillars on a tree that received bird damage after being left on the white oak sapling for one week. Caterpillars that were unrecoverable were not counted as successes or failures. The term "success" is used with reference to this number being the success input to a binomial GLMM input. Failures- The absolute number of clay caterpillars on a tree that did not receive bird damage after being left on the white oak sapling for one week. Caterpillars that were unrecoverable were not counted as successes or failures. The term "failure" is used with reference to this number being the failure input to a binomial GLMM input. Cicadas- This is a binary variable where "Yes" means that live, adult, periodical cicadas were heard or seen at the field site when the data was collected, and "No" means that no live, adult, periodical cicadas were heard or seen at the field site when the data was collected. #Column headers for data file "BirdPredation\_CompareFieldSites2021.csv" Year- The year the data in this row was collected, e.g."2022". FieldSite-The field site where the data was collected. IWLA refers to data collected at the Izaak Walton League of America Conservation Farm located in Poolesville, Maryland, USA (39.095, -77.432) and SERC refers to data collected at the Smithsonian Environmental Research Center (SERC; 38.834, -76.557), located about 100 km east of IWL in Edgewater, MD. Week- The week that the data in this row was collected, e.g. "Week 1". Week 1-4 data collection took place in May, Week 5-8 took place in June, Week 9-12 took place in July, and Week 13-14 took place in August. WhiteOakTree- Unique identifying number for individual White Oak (Quercus alba) sapling, e.g. "1". This data should be treated as a factor rather than as a number. Successes- The absolute number of clay caterpillars on a tree that received bird damage after being left on the white oak sapling for one week. Caterpillars that were unrecoverable were not counted as successes or failures. The term "success" is used with reference to this number being the success input to a binomial GLMM input. Failures- The absolute number of clay caterpillars on a tree that did not receive bird damage after being left on the white oak sapling for one week. Caterpillars that were unrecoverable were not counted as successes or failures. The term "failure" is used with reference to this number being the failure input to a binomial GLMM input. Cicadas- This is a binary variable where "Yes" means that live, adult, periodical cicadas were heard or seen at the field site when the data was collected, and "No" means that no live, adult, periodical cicadas were heard or seen at the field site when the data was collected. ## Sharing/Access information N/A *** # Dataset 3 of 4: OakHerbivoreCommunity Once every 13 or 17 years within eastern North American deciduous forests, billions of periodical cicadas concurrently emerge from the soil and briefly satiate an entire guild of naive consumers, offering a rare opportunity to assess the cascading impacts of an ecosystem-wide resource pulse on a complex food web. To test how the emergence of periodical cicadas impacts populations of free-feeding arthropod herbivores, we non-destructively recorded the abundance and identity of each externally-feeding folivore (predominantly caterpillars, sawflies, and beetles) present on the foliage or stems of 25 understory white oak saplings with accessible branches (&lt; 3m tall) in the year of the cicada emergence and the two following years. These trees hosted similar densities of herbivores in early May (just prior to the large pulse of adult cicadas in 2021) of both all three years (paired t-test: df = 18; t = 0.86; P = 0.40). In contrast, during the late June census of the emergence year, the density of externally-feeding insect herbivores was more than double that of the subsequent two non-emergence years. This pattern was driven in part by marked differences in the larval density of the oak dagger moth, Acronicta increta, the most abundant externally-feeding caterpillars at our site (paired t-test: df = 22; t = 3.14, P = 0.005). These results, in conjunction with the results of our within- and among-year avian predation surveys (clay plasticine caterpillars) support the hypothesis that a cicada-mediated community-wide avian diet shift was responsible for the dramatic release in predation we observed in the understory throughout the emergence. ## Description of the data and file structure WhiteOakTree- Unique identifying number for individual White Oak (Quercus alba) sapling, e.g. "1". This data should be treated as a factor rather than as a number. Year- The year the data in this row was collected, e.g."2022". Season- Season the data was collected, either "Spring", where data was collected in mid-May or "Summer", where data was collected in late June. Type- Type of herbivorous arthropods being recorded in the HerbivoreCount and Density in this row. "FF" refers to free feeders, which are externally-feeding arthropod folivores (predominantly caterpillars, sawflies, and beetles). "Acronicta" refers to Acronicta increta (Noctuidae) caterpillars. For any given combination of Year, Season, and WhiteOakTree, there will be a row of data for both "FF" and "Acronicta". Note that Acronicta is a particular type of free feeder, so the HerbivoreCount in the FF row includes the count of Acronicta caterpillars. Thus, the HerbivoreCount in the FF row will always be at least that of the HerbivoreCount in the Acronicta row. Note also that leaf roller and leaf tier arthropods were recorded but are not included in this data set. LeafCount- The number of leaves on the tree. HerbivoreCount- The total number of free-feeding arthropod folivores observed on the tree. Density- The density of herbivores on the given tree as described by HerbivoreCount/LeafCount\*100. For example, if there are 12 herbivores and 666 leaves, the density would be 1.802. NA-In the dataset, cells filled with "NA" mean that data was not collected from that tree in that particular year. A tree would not be censused in a given year if it could not be located, if it had died, or if it was added to the study late to replace a tree that had died or could not be located. ## Sharing/Access information N/A ## Code/Software Data were analyzed with the script labeled "OakHerbivoreCommunityAnalysis.r". *** # Dataset 4 of 4: Herbivory We conducted non-destructive herbivory censuses in early June and mid-October of each year to estimate the damage incurred by trees from feeding by the spring herbivore community (pre-cicada) and that resulting from the summer/fall herbivore community (during and post-cicada). In each census, we visually estimated (to the nearest 1.0%) the amount of removed tissue from 30 randomly sampled leaves selected from throughout the crown of each tree (N = 30 understory white oak saplings). At the producer level, understory white oak trees experienced a spike in cumulative leaf damage in mid-summer of the cicada emergence year, relative to both pre- and post-emergence years (ANOVA: F2,89 = 11.5, P &lt; 0.001), which did not differ from each other (t = 0.524, df = 87, P = 0.602). The observed emergence-year doubling of both accumulated herbivory and of insect herbivore density on understory white oak trees strongly suggests a causal linkage. The peak in accumulated herbivory during the summer of 2021 relative to both the pre- and post-emergence years (Fig. 5) indicates that the community-wide shift in avian foraging cascaded down to impact plant damage by herbivores. While increased herbivory levels on understory white oak trees have been documented when birds were excluded from individual trees and small stands, we provide the first empirical evidence that the protective function of an entire community of insectivorous birds can be disrupted by a synchronous resource pulse. ## Description of the data and file structure Year- The year the data in this row was collected, e.g."2022". WhiteOakTree- Unique identifying number for individual White Oak (Quercus alba) sapling, e.g. "1". This data should be treated as a factor rather than as a number. MedianPercentHerb-Median percent herbivory on a tree based on visual estimations of 30 randomly selected leaves per tree. ## Sharing/Access information N/A ## Code/Software Data were analyzed with the script labeled "HerbivoryAnalysis.r".