Parasitoids indicate major climate-induced shifts in arctic communities

Abstract

Climatic impacts are especially pronounced in the Arctic, which as a region is warming twice as fast as the rest of the globe. Here, we investigate how mean climatic conditions and rates of climatic change impact parasitoid insect communities in 16 localities across the Arctic. We focus on parasitoids in a widespread habitat, Dryas heathlands, and describe parasitoid community composition in terms of larval host use (i.e., parasitoid use of herbivorous Lepidoptera vs. pollinating Diptera) and functional groups differing in their closeness of host associations (koinobionts vs. idiobionts). Of the latter, we expect idiobionts-as being less fine-tuned to host development-to be generally less tolerant to cold temperatures, since they are confined to attacking hosts pupating and overwintering in relatively exposed locations. To further test our findings, we assess whether similar climatic variables are associated with host abundances in a 22 year time series from Northeast Greenland. We find sites which have experienced a temperature rise in summer while retaining cold winters to be dominated by parasitoids of Lepidoptera, with the reverse being true for the parasitoids of Diptera. The rate of summer temperature rise is further associated with higher levels of herbivory, suggesting higher availability of lepidopteran hosts and changes in ecosystem functioning. We also detect a matching signal over time, as higher summer temperatures, coupled with cold early winter soils, are related to high herbivory by lepidopteran larvae, and to declines in the abundance of dipteran pollinators. Collectively, our results suggest that in parts of the warming Arctic, Dryas is being simultaneously exposed to increased herbivory and reduced pollination. Our findings point to potential drastic and rapid consequences of climate change on multitrophic-level community structure and on ecosystem functioning and highlight the value of collaborative, systematic sampling effort.

Keywords: Dryas; Arctic; DNA barcoding; climate change; food webs; functional traits; host-parasitoid interactions; insect herbivory; pollinators.

FIGURE 1

Conceptual summary of parasitoid life‐history strategies, host group preferences, and their links to multidecadal mean climate and climate change and its implications. For each of three aspects of parasitoid ecology, that is, parasitoid life‐history strategy, parasitoid host group taxonomy, and associated host abundances, we identify the expected responses to mean climate and recent climate change. We identify the response categories (classes) scored as Attributes contrasted, the biological features of each class as Distinguishing features, and expectations in terms of responses in terms of two types of patterns: changes in the dominance of the respective group with a change in mean conditions (column Mean climate), and changes in the dominance of the respective group with recent trends in a warming Arctic (column Recent change). Finally, we summarize the results obtained in terms of contemporary patterns across the Arctic (Spatial results) and matching patterns in the 22 year time series from Zackenberg, Northeast Greenland (temporal results). Given the dominance of Diptera among arctic pollinators and Lepidoptera among arctic herbivores, we note that changes in host use provide a window to the relative abundance of these key guilds. For clarity, we color code the taxonomically and ecologically separate Lepidoptera‐ and Diptera‐based food web modules in green and blue, respectively, reminding the reader that larval Lepidoptera form the dominant herbivores of Dryas, whereas adult Diptera form the dominant pollinators

FIGURE 2

The structure of the dataset and the links between data sources. The box on the left summarizes data collected across the Arctic on parasitoid community composition and level of herbivory. Parasitoid communities were characterized by host use and parasitoid life‐history strategy (as nested within host use). These spatial data were collected at each of 19 field sites, identified by pink markers on the central map. For each of these sites, we also extracted two types of climate data: variables describing mean temperature and precipitation over the time period 1970–2000 (illustrated in upper hemispheres) and variables describing the rate of the recent temperature change during 2000–2017 (illustrated in lower hemisphere). The box on the right summarizes data used to analyze temporal patterns of host availability at one of the study locations (Zackenberg, Northeast Greenland). The data encompass local climatic data since 1996–2017, counts of muscid flies in insect traps, and annual peak fractions of damaged Dryas flowers on permanent monitoring plots. For clarity and consistency with Figure 1, we show parasitoids in black, pollinators in blue and herbivores in green. Numbers identify sampling localities: 1. Zackenberg, 2. Churchill, 3. Igloolik, 4. Bylot Island, 5. Qeqertarsuaq/Disko Island (low and high altitudes), 6. Kangerlussuaq (low and high altitudes), 7. Kangerluarsunnguaq/Kobbefjord, 8. Hochstetter Forland, 9. Snæfellsnes, 10. Ny‐Ålesund, 11. Svare/Vågå, 12. Finse, 13. Kevo, 14. Finnmark (two different mountains), 15. Monchegorsk, 16. Yamal. For detailed site‐specific information, see Table S1. We note that data from the Russian‐Canadian Arctic are very sparse, reflecting logistic challenges during the focal study period (summer of 2016). For consistency with Figure 1, we color code the taxonomically and ecologically separate Lepidoptera‐ and Diptera‐based food web modules in green and blue, respectively, reminding the reader that larval Lepidoptera form the dominant herbivores of Dryas, whereas adult Diptera form the dominant pollinators

FIGURE 3

Relationship between host use (y axes), the rate of temperature change in the winter period (x axes) and in the summer period (in panel c), with the three curves corresponding to the models estimates for low, mean, and high values occurring in the data as indicated in the right‐hand side box, and the colored areas around them showing 95% confidence intervals. The colors of the data points show the local rate of temperature change for the summer period, adhering to the color scheme of the left‐hand legend. Panels (a) and (b) show the effects of these variables on the fraction of parasitoid species and individuals, respectively, which mainly use lepidopteran hosts. Panels (c) and (d) visualize the same trends but for parasitoids of Diptera. The size of the data points is proportional to the number of species or individuals, respectively whereas the colors of data points represent local rate of temperature change for the summer period

FIGURE 4

Relationship between the functional community composition of the parasitoids of Lepidoptera as the fraction of idiobionts (y axes), the average of mean winter temperatures (x axes), and the rate of change in summer temperatures (with the three curves corresponding to the models estimates for low, mean, and high values occurring in the data, and the colored areas around them showing 95% confidence intervals). Panel (a) shows the model‐fitted effects of these variables on the fraction of idiobionts out of all species of primary parasitoids of Lepidoptera and panel (b) shows the same relationship, but for the fraction of idiobionts out of all individuals of primary parasitoids of Lepidoptera. The size of each data point is proportional to the number of (a) species or (b) individuals, respectively. The colors of data points represent the rate of summer temperature change at the respective locality (see legend on the right)

FIGURE 5

The relationship between the fraction of flowers damaged by lepidopteran herbivores in Dryas plots and the rate of summer temperature change across arctic localities. The size of the marker illustrates the number of Dryas flowers in the survey plot. Color shades illustrate overlapping data points.

FIGURE 6

Temporal patterns in herbivory and pollinator abundances as observed at Zackenberg, Northeast Greenland. Panel a) shows chronological patterns in the level Dryas damage by Sympistis larvae and the abundance of muscid flies caught at Zackenberg. The solid lines show the actual mean peak percentage of damage recorded and the mean number of muscid flies caught in a trapping station during a summer season. The shaded areas show the confidence intervals of fitted values from models 6 and 7, respectively. The Dryas damage by lepidopteran larvae is shown separately for early plots (light green) and late plots (dark green). For comparison, surfaces in panels (b) and (c) illustrate the effects of two explanatory climatic variables shared between the two models: the air temperature during the focal summer and the soil temperature of the summer 2 years earlier, for Dryas damage and muscid fly abundance, respectively. Note that in panel (a), there is a gap in the line for muscid flies at year 2010. In this year, all arthropod samples were unfortunately and mysteriously lost in transit between Zackenberg and Aarhus, before being sorted, counted, or databased