Costs of breeding far away from neighbors: Isolated host nests are more vulnerable to cuckoo parasitism

Accepted Manuscript Title: Costs of breeding far away from neighbors: isolated host nests are more vulnerable to cuckoo parasitism Authors: Laikun Ma, Canchao Yang, Jianping Liu, Jianwei Zhang, Wei Liang, Anders Pape Møller PII: DOI: Reference:

S0376-6357(18)30132-3 https://doi.org/10.1016/j.beproc.2018.07.017 BEPROC 3711

To appear in:

Behavioural Processes

Received date: Revised date: Accepted date:

25-3-2018 25-7-2018 26-7-2018

Please cite this article as: Ma L, Yang C, Liu J, Zhang J, Liang W, Møller AP, Costs of breeding far away from neighbors: isolated host nests are more vulnerable to cuckoo parasitism, Behavioural Processes (2018), https://doi.org/10.1016/j.beproc.2018.07.017 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Costs of breeding far away from neighbors: isolated host nests are more vulnerable to cuckoo parasitism

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Running headline: Cuckoo parasitism and host defense

Laikun Ma1, Canchao Yang1, Jianping Liu1, Jianwei Zhang1, Wei Liang1, *, Anders

Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of

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Pape Møller2

Ecologie Systématique Evolution, Université Paris-Sud, CNRS, AgroParisTech,

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Life Sciences, Hainan Normal University, Haikou 571158, China

Corresponding author. E-mail: [email protected]

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Université Paris-Saclay, F-91405 Orsay Cedex, France

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Word count: 5214

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Hightlights

 This study showed that isolated nests of Oriental reed warblers (Acrocephalus orientalis) with distant neighbors were more

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suggesting a cost of breeding far away from neighbors.

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vulnerable to common cuckoo (Cuculus canorus) parasitism

 Choice and parasitism of isolated host nests far away from

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neighbors may be an adaptive parasitic strategy by common

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cuckoos to increase the probability of successful parasitism. We

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hypothesize that cooperative behavior within local populations of

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Oriental reed warblers can probably be considered as an

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Abstract

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anti-parasitic strategy developed through long-term coevolution.

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A series of parasitic and anti-parasitic strategies has evolved during the long-term coevolution between cuckoos and their hosts. The first stage of the arms race is host nest choice by cuckoos, followed by nest defense by hosts. This study examined nest defense strategies of the Oriental reed warbler (Acrocephalus orientalis) in relation to parasitism by the common cuckoo (Cuculus canorus). Attack rate of Oriental reed 2

warblers against common cuckoo dummies was 100% and neighboring individuals participated in 87.1% of such attacks. Furthermore, the number of hosts attacking cuckoo dummies was significantly positively correlated with the number of neighbors at a distance from 40 to 70 m, indicating social anti-parasitic behavior. Analysis of

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nest-site parameters indicated that the distance to the nearest neighboring unparasitized nest was significantly shorter than that of parasitized nests. Our study

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demonstrated that isolated nests of Oriental reed warblers with distant neighbors were

more vulnerable to common cuckoo parasitism suggesting a cost of breeding far away

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from neighbors. We hypothesize that cooperative behavior within local populations of

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Oriental reed warblers can probably be considered as an anti-parasitic strategy

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developed through long-term coevolution. Choice and parasitism of isolated host

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nests far away from neighbors may be an adaptive parasitic strategy by common

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cuckoos to increase the probability of successful parasitism.

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Keywords: coevolution; conspecific assistance; isolated nests; nest defense

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Introduction

The arms race-like adaptations and counter-adaptations of cuckoos and their hosts are a model system in coevolution (Davies 2000, 2011; Soler 2014). Long-term

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coevolution involves a series of parasitic and anti-parasitic strategies in the two interacting parties that thereby increase their fitness (Brooke and Davies 1988; Davies

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and Brooke 1988; Langmore et al. 2003; Grim 2007; Li et al. 2016; Sato et al. 2010; Spottiswoode and Stevens 2010; Yang et al. 2010, 2015a, 2015b; Langmore et al.

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2011). Before parasitizing a nest, the common cuckoo Cuculus canorus usually

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removes one or more host eggs. And the cuckoo chicks evict remaining eggs or chicks

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in the same nest after hatching so that they receive exclusive access to food from the

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foster parents (Davies 2000). This at least results in reproductive losses of one or

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more eggs by the hosts, even though their defence was successful during the egg laying and incubation stages. Hence, preventing cuckoos from laying eggs in the nest

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is a more advantageous anti-parasitic nest defense strategy for hosts (Feeney et al.

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2012). Studies have shown that hosts are able to recognize cuckoos and perform different defensive behaviors against cuckoos that approach their nests. Hosts even attack cuckoos directly to dissuade them from parasitizing their nests (Trnka and

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Prokop 2012; Trnka and Grim 2013, 2014; Li et al. 2015). Furthermore, alerts by potential hosts can trigger conspecifics and heterospecifics to attack cuckoos (Grim 2008; Welbergen and Davies 2008; Li et al. 2015). While hosts can minimize the risk of cuckoo parasitism through informed 4

nest-site choice, e.g., avoiding patches with high risk of parasitism (Forsman and Martin 2009; Expósito-Granados et al. 2017; Tolvanen et al. 2017), how cuckoos choose a suitable nest for parasitism is still a largely unsolved research topic (Clarke et al. 2001; Yang et al. 2016, 2017). For example, the ‘perch proximity’ hypothesis

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(Anderson and Storer 1976; Freeman et al. 1990; Øien et al. 1996) and the ‘spatial structure hypothesis’ (Røskaft et al. 2002) state that host nests near trees or other

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perch sites are more susceptible to parasitism. The ‘nest exposure hypothesis’ (Clotfelter 1998) takes into account concealment of host nests affecting cuckoo

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parasitism. Other factors such as host activity (Fiorini et al. 2009; Svagelj et al. 2009)

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and mating system (Trnka and Prokop 2011) may also affect cuckoo parasitism. In

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addition, the risk of cuckoo parasitism was lower in larger populations that benefited

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from cooperative vigilance and defense (Brown and Lawes 2007). Previous studies

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also revealed that parasitized nests have longer nearest neighbor distances than unparasitized nests, and nests far away from neighbors were more likely to suffer

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from parasitism (Moskat and Honza 2000; Begum et al. 2011; Feeney et al. 2012).

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Studies of reed warblers (Acrocephalus scirpaceus) indicated that a host can alert others to the threat of cuckoo parasitism through social communication within the community and rapidly strengthen its defence abilities by learning defensive

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behaviors from neighbors (Davies and Welbergen 2009; Thorogood and Davies 2012, 2016). Furthermore, host alerts attract nearby individuals of the same or different species, and some individuals will join the defence and attack cuckoos, thereby decreasing the success rate of cuckoo parasitism (Grim 2008; Welbergen and Davies 5

2008; Li et al. 2015). Obviously, social factors play an important role in the coevolution of cuckoos and their hosts (Thorogood and Davies 2012), and this also explains why common cuckoos parasitize nests secretly and lay eggs rapidly (Thorogood and Davies 2016).

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The Oriental reed warbler (Acrocephalus orientalis) is one of the main hosts of common cuckoos. Due to their long-term coevolution, both species show an advanced

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stage of the arms race (Yang et al. 2014; Li et al. 2016). Oriental reed warblers can discriminate and fiercely attack common cuckoos, and social behaviors such as

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cooperative defence with neighbors were observed (Li et al. 2015). The sibling

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species great reed warbler (Acrocephalus arundinaceus) has even been observed to

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kill adult cuckoos (Molnár 1944; Mérő and Žuljević 2014). Social anti-parasite

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behaviour may include special anti-parasitic strategies developed through long-term

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coevolution with common cuckoos. Whether the cooperative nest-defence by these fierce hosts influences the parasitism strategy of common cuckoos remains an open

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question. This study examined the nest defense strategies of the Oriental reed warbler

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and the nest choice by the common cuckoo, and it analyzed the interaction between the two parties at the nest defence stage. We predicted that (1) the defence of the Oriental reed warbler increased with the

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number of neighbors with hosts with more neighbors showing an intensified defence against the cuckoo. (2) The number of neighbors close to the nest of Oriental reed warblers reduced the risk of parasitism, while isolated Oriental reed warbler nests with fewer and more distant neighbors should be more vulnerable to common 6

cuckoos.

Methods Study area

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The study area was located in the Yongnian Wetland in Yongnian County, Hebei Province, China (36°40'60''–36°41'06'' N, 114°41'15''–114°45'00'' E). The area is a

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natural wetland on the alluvial plain of the Fuyang River. The water system is

well-developed with numerous tributaries and perennial stagnant water. The elevation

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of the area is only 40.3 m. The region has a temperate, semi-humid, continental

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monsoon climate with four distinct seasons. It is dry and cold in winter, and wet and

Field data collection

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latifolia, and other herbaceous plants.

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hot in summer. The dominant types of vegetation are Phragmites australis, Typha

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Field investigations were conducted during the breeding seasons May-July 2016–

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2017. A systematic search for nests across the study area was conducted. GPS locations and parameters such as nest size were measured and recorded. Previous studies discovered that host alerts attracted nearby individuals of the same or different

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species which even joined the defense and attacked cuckoos (Grim 2008; Welbergen and Davies 2008; Li et al. 2015). The distance to the nest of neighbors affected parasitism by cuckoos (Øien et al. 1996; Feeney et al 2012). Clark and Robertson (1979) also reported that hosts sought refuge through breeding within the territory of 7

aggressive birds. Therefore, we took neighborhood parameters into consideration which may influence the risk of parasitism by cuckoos. Landscape parameters potentially affecting the risk of parasitism were (1) distance to road (m): the nearest distance between the nest and roads with human

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activity; (2) distance to tree or other perch site (m): the nearest distance between the nest and available sites for common cuckoos to rest and observe nests; (3) distance to

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human resident (m): the nearest distance between the nest and residential areas; (4)

distance to edge of the reed (m): the nearest distance between the nest and edge of the

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reed habitat; (5) water boundary (m): the nearest distance between the nest and

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surface water boundary; and (6) nest visibility (Moskát and Honza 2000): the number

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of directions in which common cuckoos were able to monitor host nest building

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activities from perch sites without obstacles.

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Micro-habitat niches of the nest included (1) nest height (m): the height of the nest above water or land surface; (2) nest cover: the crown density at 10 cm above the

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nest; (3) reed height (m): the height of reeds in a 1 m × 1 m area centered at the nest,

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which is equivalent to the natural height of reeds above water; (4) number of reeds: the number of reeds in the 1 m × 1 m area; and (5) water depth (cm): the average

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water depth immediately below the nest. Structural parameters of the nest included (1) diameter (cm): the diameter of the

outer circumference at the top of the nest; (2) depth (cm): the distance from the top to the bottom of the nest; (3) cup diameter (cm): the diameter of the inner circumference at the top of the nest; and (4) cup depth (cm): the depth of the nest interior. 8

Neighborhood parameters included: (1) distance to the nearest neighbor: the distance between the target nest and the nearest active nest of the same species during the egg-laying period. As Oriental reed warblers normally produce five eggs, the egg-laying period is defined as a 4-day period after the first egg is laid. (2) Number of

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from 10 to 70 m during the egg-laying period of the target nest.

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neighbors: the number of active nests of conspecific species within a radius ranging

Dummy experiment

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We assessed the correlations between the intensity of defence by Oriental reed

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warbler and the number of neighboring nests using a dummy experiment with

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taxidermic mounts of the common cuckoo. Oriental reed warblers were able to

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discriminate and fiercely attack common cuckoos (Li et al. 2015). However, as enemy

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recognition was not our main interest in this study, we did not use a control dummy in the present study (see also Trnka and Grim 2014). Taxidermic mounts of the common

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cuckoo were selected and fixed using stands at 0.5 m in front of nests of Oriental reed

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warblers. The mounts remained standing with heads facing towards host nests. Responses of Oriental reed warblers to the mounts were observed and recorded. The responses were classified from low to high as: 1) no reaction, the bird was not

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observed or watched the mount silently without clear responsive behavior; 2) alert, the bird approached the nest (hopped onto the reed stems), but gave alert calls from a safe distance (more than 1 m); 3) mobbing, the bird jumped or flew around/over the mount, persistently giving alarm and distress calls; and 4) attack, the birds physically 9

attacked the mount (Li et al. 2015). The latter two types of defence often attracted non-parental individuals to join in defense. The responsive behavior of the hosts and the number of attackers were recorded by LM. Each nest was mounted only once in the egg stage. To reduce the probability of pseudo-replication, two mounts were

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prepared, and one was randomly selected during the experiment (see Trnka and

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Prokop 2012).

Data analysis and statistics

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SPSS 16.0 statistical software was used for all statistical analyses. Logistic regression

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was used to analyze the effects of nest parameters on the success rate of cuckoo

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parasitism. Fisher’s exact test was used to compare cuckoo parasitism rate between

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the two years. The correlation between the number of attacks on the common cuckoo

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dummy and the number of neighboring nests was determined using Kendall rank

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mean ± SD.

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correlation analysis. The level of significance was set at 0.05. Data are reported as

Results

Factors contributing to rates of cuckoo parasitism

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A total of 257 Oriental reed warbler nests with an overall parasitism rate of 14.8% were recorded during the breeding seasons 2016-2017. In 2016, 133 nests were found, with 18 nests parasitized, and in 2017, 124 nests, with 18 nests parasitized including 2 double parasitized. The parasitism rate was similar in the two years (Fisher’s exact 10

test, P=0.861). Parasitized nests were generally located on the edge of the reed habitat with fewer neighbors, and they were far away from neighbors (Figure 1). Nest parameters of 123 nests were measured and recorded, with the remaining nests not being measured for logistic reasons. Only the nearest distance to neighbors (Wald

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chi-square = 6.541, df = 1, P = 0.011) was significantly associated with cuckoo parasitism of the target nest (Table 1). The nearest distance to neighbors was

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considerably longer for parasitized than unparasitized nests (Figure 2). None of the

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other variables significantly predicted risk of cuckoo parasitism.

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Nest defense behavior of Oriental reed warbler hosts

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All parental Oriental reed warblers attacked common cuckoo dummies (100%, n = 31

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nests), and participation of non-parental individuals was observed in 27 attacks, which

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accounted for 87.1% of the total nests. The number of individuals assisting in attacks varied from 1 to 8 Oriental reed warblers. Kendall rank correlations indicated that the

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number of hosts attacking was positively correlated with the number of active nests

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within a distance from 40 to 70 m (40 m: r=0.449, n=31, P =0.002; 50 m: r=0.408, n=31, P =0.003; 60 m: r=0.421, n=31, P =0.002; 70 m: r=0.371, n=31, P =0.007) (Figure 3). However, significant correlations were also found among the number of

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active nest from 40 to 70 m (P < 0.001 for all pairs of comparison).

Discussion Oriental reed warblers showed strong responses to parasitic common cuckoos. Social 11

behavior by neighbors occurred as neighboring individuals assisted in nest defense and attacked cuckoo dummies. In addition, isolated nests with relatively distant neighbors were more vulnerable to cuckoo parasitism. Some cuckoo hosts are able to discriminate between intruders and cuckoos and

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perform different defensive behaviors against cuckoos that approach their nests (Welbergen and Davies 2008; Trnka and Prokop 2012；Li et al. 2015). Previous

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studies showed that nest defense by hosts can result in severe harm to cuckoos,

including feather loss and injuries (Welbergen and Davies 2008, 2009; Feeney et al.

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2012; Trnka and Prokop 2012; Li et al. 2015), and even death (Molnár 1944; Mérő

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and Žuljević 2014). Studies of the behavior of Oriental reed warblers concluded that

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they can accurately discriminate between the cuckoo and other intruders. Warblers

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sometimes engage in fierce attacks and nest defense behavior, and conspecific

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individuals occasionally participate in attacks by Oriental reed warblers (Li et al. 2015). Previous studies reported that there were onlookers of other species due to

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alerts from hosts, but that it was comparatively rare for them to take part in an attack

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(Grim 2008; Welbergen and Davies 2008). The present study showed that cooperative defenses and assistance during attacks by neighbors were common during nest defense by Oriental reed warblers. Here we further showed that the number of

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Oriental reed warblers attacking cuckoos increased with the number of neighbor near nests from 40 to 70 m. This may be due to the fact that warning calls of Oriental reed warblers would not effectively spread beyond 40 m. The number of Oriental reed warblers attacking increased when there were more neighbors in the surrounding area 12

suggesting that it was more difficult for cuckoos to parasitize host nests with more conspecific neighbors and with larger breeding groups. Our study was inconsistent with previous studies showing that the number of neighbors did not enter the final model, and that it was not a predictor of cuckoo

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parasitism of host nests. Common cuckoos typically lay their eggs in the afternoon (Wyllie 1981; Moksnes et al. 2000; Honza et al. 2002). Such a strategy would help

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reduce encountering the aggressive hosts. However, we found that cuckoos did not deliberately choose the time when hosts were far away from the nest to lay, although

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the Oriental reed warbler was a strongly aggressive host (Yang et al. 2016, 2017). The

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fact that female cuckoos encountered hosts in most cases when laying suggests that

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cuckoos may use host activities as a cue to search for and locate nests (Davies 2000;

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Yang et al. 2017). Previous studies indicated that the size of the host population

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affects choice of nests by brood parasites as cooperative alerts in a large population effectively decreases the risk of parasitism (Lawes and Kirkman 1996; Brown and

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Lawes 2007). Similar examples were also found in cases of predation in which the

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success rate of a predator decreases with an increasing prey population while isolated individuals encounter more attacks and higher predation risk (van Orsdol 1984; Krause and Godin 1995; Jackson et al. 2006). In the present study, the parasitized

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nests were obviously far away from neighbors. However, they did not have significantly fewer neighbors. This may be due to the fact that host nest defense enhanced by the presence of more neighbors still would not completely prevent cuckoo females from laying eggs in a nest. For example, Nakamura et al. (2005) 13

reported that a female cuckoo laid an egg into the nest of an Oriental reed warbler at the ninth attempt, despite always being attacked by up to four warblers. Previous studies found that host nests close to neighbors suffered from lower parasitism risks due to cooperative vigilance (Clark and Robertson 1979; Barber and Martin 1997;

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Moskát and Honza 2000; Begum et al. 2011; Feeney et al. 2012). The study by Canestrari et al. (2009) also found that nests of unassisted pairs of carrion crows

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suffered high risk of parasitism by the great spotted cuckoo (Clamator glandarius) due to the lack of cooperative defense.

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Previous studies showed that polygyny was important determinants of risk of

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parasitism because neighboring nests may attract males more frequently than females

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thereby increasing the risk of cuckoo parasitism (Požgayová et al. 2009, 2013). Thus

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the mating status of the closest nest (monogamous or polygynous) may affect the

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number of birds attracted. For example, in great reed warblers (Acrocephalus arundinaceus), socially polygynous males provided less nest defense and nest

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guarding, and this could contribute to the higher rate of cuckoo parasitism on

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polygynous pairs than monogamous pairs suggesting that individual assistance reduced parasitism risk (Požgayová et al. 2009, 2013; Trnka and Prokop 2011). The Oriental reed warbler is also polygynous, with polygyny varying from 26 to 80% (e.g.

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Urano et al. 1985; Ezaki et al. 1990; Choi et al. 2010). Unfortunately, there was no data on polygyny in our population of Oriental reed warblers and future work is needed to address this open question. In the present study, Oriental reed warblers were strongly aggressive and bred at high density with a clumped aggregation of nests. 14

The alert from target nests could trigger conspecific cooperative defenses of attack against cuckoos. Therefore, the distance to neighbors not only affected the quick detection of cuckoo parasitism, but also influenced the time before receiving assistance for mobbing and attacking cuckoos.

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Although distance to the nearest perch was generally regarded as an important predictor of parasitism risk in the common cuckoo (Øien et al. 1996; Moskat and

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Honza 2000; Clarke et al. 2001; Roskaft et al. 2002; Antonov et al. 2007), we did not

confirm such a relationship. This was probably because there were sufficiently many

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perches to allow cuckoos to monitor all available host nests in our study area.

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In conclusion, isolated Oriental reed warbler nests with more distant neighbors

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were more vulnerable to common cuckoo parasitism suggesting a cost of breeding far

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away from neighbors. This further provided an example of confrontation between

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common cuckoos and Oriental reed warblers consistent with coevolution during the nest defense stage. Cooperative behavior within local populations of Oriental reed

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warblers can probably be considered an anti-parasitic strategy developed through

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long-term coevolution. Selection and parasitism of isolated host nests far away from neighbors may also be an adaptive parasitism strategy by common cuckoos to

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increase their success of parasitism.

Acknowledgments We are grateful to Prof. Johan Bolhuis, Prof. Jeremy Wilson and six anonymous referees for their constructive comments that significantly improved our manuscript. 15

We would like to thank the Forestry Bureau of Yongnian County, Hebei Province, China, for permission to undertake this study including all experimental procedures. The experiments comply with the current laws of China. Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial

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Education Centre for Ecology and Environment, Hainan Normal University (permit no. HNECEE-2012-003). This work was supported by the National Natural Science

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Foundation of China (Nos. 31672303 to CY, 31472013 and 31772453 to WL). We

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declare that the authors have no competing interests.

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Legends to figures

Figure 1. Distribution of parasitized and unparasitized nests of Oriental reed warblers.

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A and B refer to the years 2016 and 2017, respectively. Red symbol refers to parasitized nests while the larger ones refer to double parasitized nests. Blue symbol

A

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ED

M

A

N

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refers to unparasitized nests.

24

IP T SC R U N A M ED PT CC E A Figure 2. Comparison of distance (m) to the nearest neighbor between parasitized and unparasitized warbler host nests. Box plots show median, quartiles and 5- and 95-percentiles. 25

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Figure 3. Rank correlation between the number of Oriental reed warblers attacking

P <0.05; **P <0.01.

A

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PT

*

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the cuckoo dummy and the number of neighbors from different distances. NS P >=0.05;

26

Table

Table 1. Logistic regression model of nest site parameters affecting the probability of cuckoo parasitism in nests of Oriental reed warblers. P values < 0.05 are statistically

Variable

Wald/Score df

Distance to nearest neighbor (m)

6.541

included in the

1

0.011

1

0.105

2.522

1

0.112

Distance to human resident (m)

0.902

1

0.342

Distance to reed edge (m)

1.612

1

0.204

Water boundary (m)

0.106

1

0.745

Variables not

Nest visibility

0.819

1

0.366

included in the

Nest height (m)

2.497

1

0.114

Nest cover (%)

0.154

1

0.695

Height of reed (m)

1.523

1

0.217

Number of reeds

0.083

1

0.774

Water depth (cm)

0.101

1

0.750

Nest diameter (cm)

0.075

1

0.785

Nest depth (cm)

1.863

1

0.172

U

equation

P

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Variables

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significant.

A

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PT

ED

M

Distance to perch (m)

2.625

N

Distance to road (m)

A

equation

27

0.355

1

0.551

Cup depth (cm)

1.351

1

0.245

A

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PT

ED

M

A

N

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Cup diameter (cm)

28