Reed warbler hosts fine-tune their defenses to track three decades of cuckoo decline

Abstract

Interactions between avian hosts and brood parasites can provide a model for how animals adapt to a changing world. Reed warbler (Acrocephalus scirpaceus) hosts employ costly defenses to combat parasitism by common cuckoos (Cuculus canorus). During the past three decades cuckoos have declined markedly across England, reducing parasitism at our study site (Wicken Fen) from 24% of reed warbler nests in 1985 to 1% in 2012. Here we show with experiments that host mobbing and egg rejection defenses have tracked this decline in local parasitism risk: the proportion of reed warbler pairs mobbing adult cuckoos (assessed by responses to cuckoo mounts and models) has declined from 90% to 38%, and the proportion rejecting nonmimetic cuckoo eggs (assessed by responses to model eggs) has declined from 61% to 11%. This is despite no change in response to other nest enemies or mimetic model eggs. Individual variation in both defenses is predicted by parasitism risk during the host's egg-laying period. Furthermore, the response of our study population to temporal variation in parasitism risk can also explain spatial variation in egg rejection behavior in other populations across Europe. We suggest that spatial and temporal variation in parasitism risk has led to the evolution of plasticity in reed warbler defenses.

Keywords: Brood parasitism; coevolution; environmental change; phenotypic plasticity.

Figure 1

Changes in (A) population sizes (1985 scored as 100%) of reed warbler hosts (black circles) and female cuckoos (white circles); (B) parasitism rate; and (C) host defenses (mobbing of adult cuckoos, black circles, and rejection of non-mimetic eggs, white circles) at Wicken Fen, Cambridgeshire, U.K., from 1985–2012. Lines of best fit (± SE) come from linear regressions (A), or binomial generalized linear models (B, C). See Table S1 for raw data.

Figure 2

Seasonal changes on Wicken Fen in the proportion of reed warblers that (A) were parasitized by cuckoos; (B) mobbed an adult cuckoo model at the nest; and (C) rejected nonmimetic model eggs, with week 1 beginning May 14. White circles (with short dashed lines) represent data from 1985 to 1986, gray circles (with long-dashed lines) represent data from 1996 to 1997, and black circles (with solid lines) represent data from 2010 to 2012. Circle diameters are relative to sample size and an x-axis jitter of 0.1 was applied to display overlapping data.

Figure 3

Variation in defenses by reed warblers on Wicken Fen in response to parasitism rate at the time of laying, as predicted by a generalized linear model with binomial errors (solid line, dashed lines ± SE) of (A) mobbing of adult cuckoo models at the nest (not mobbed (0) or mob (1), n = 205 nests from 1985 to 1986, 1996 to 1997, 2010 to 2011) and (B) acceptance (0) or rejection (1) of nonmimetic model eggs (n = 201 nests from 1985 to 1986, 1997, 2012). The relative sizes of pairs of data points (open circles) show the proportion of birds that did or did not defend themselves. Also plotted are the data for geographic variation in reed warbler defenses at various populations across Europe: black squares represent population-level estimates of mobbing or egg rejection at varying parasitism rates from other study sites (see Table S3 for details). Population-level data from different years on Wicken Fen were not used to investigate fit of other populations, but are presented here for comparison (white squares).

Figure 4

Data from Wicken Fen (gray circle) were compared to data from reed warbler populations across Europe (black circles). Details of these studies are given in Table S3. Map adapted from http://neethis.deviantart.com.