University of Groningen
Better together
Groenewoud, Frank
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from
it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date:
2018
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Groenewoud, F. (2018). Better together: Cooperative breeding under environmental heterogeneity.
University of Groningen.
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum.
Box A
Anti-predator benefits drive
communal breeding
in the Seychelles warbler
Sjouke A. Kingma, Kathryn L. Bebbington, Martijn Hammers, Frank Groenewoud, Hannah Dugdale, Marco van der Velde, Michael Taborsky, Terry Burke, Franz J. Weissing, David S. Richardson, Jan Komdeur
ANTI-PREDATOR BENEFITS DRIVE COMMUNAL BREEDING IN
THE SEYCHELLES WARBLER
Mutualistic benefits, like enhanced access to food and protection against predators, are generally believed to promote group living, and can ultimately facilitate communal breed-ing (Krause & Ruxton 2002; Clutton-Brock 2009). Concession models (or transactional mod-els; Reeve et al. 1998) of reproductive skew predict that dominants may grant subordinates access to reproduction if this provides a net benefit to the fitness of dominants. These re-productive concessions may persuade subordinates to stay and cooperate when they would otherwise leave or withhold help (Johnstone 2000). In the Seychelles warbler (hereafter ‘SW’), an individual can stay as a subordinate in a stable territorial group for years (Kom-deur 1992; Kingma et al. 2016a). Subordinate males sometimes stay and provision offspring, but only subordinate females participate in incubation. The main egg predator of the Sey-chelles warbler is the endemic SeySey-chelles fody Foudia sechellarum, (hereafter ‘fody’). These small passerines approach unattended Seychelles warbler nests, rapidly toss the eggs onto the floor (within 4-17 seconds; Komdeur & Kats 1999) and consume them. Since the majority of nests contain only one egg (Komdeur 1991; Bebbington et al. 2017), predation normally results in the loss of the entire brood. Our data show that helpers substantially increase the percentage of time for which eggs are incubated (nest incubation attendance with helper: 71.0 ± 1.9% of time (n = 88) vs. no helper: 50.0 ± 0.8% (n = 301); t = 12.1, P < 0.0001; irrespective of food abundance: β = 0.009 ± 0.025, t = 0.355, P = 0.72). Fodies have a greater opportunity to predate nests with a single incubating female because these nests are unattended for longer periods than nests with multiple incubating females (time between incubation bouts; 7.2 min vs. 2.4 min). Consequently, hatching success decreased with increasing predation risk (assessed as the number of fodies) in territories without subordinates (β ± SE = -0.175 ± 0.075, Z = -2.339, P = 0.019), but was unaffected by predation risk in territories with additional sub-ordinates (β ± SE = 0.159 ± 0.117, Z = 1.361, P = 0.173, Fig. A.1). Although having helpers may im-prove the dominant pair’s breeding success, they also impose costs in Seychelles warblers; adult survival decreases as a result of additional group members due to increased compe-tition over food (Brouwer et al. 2006). Therefore, this system provides an ideal situation in which to test if females provide reproductive concessions in exchange for help, when the need for help (i.e. predation risk) is high.
We compared this plasticity in subordinate reproduction with natural variation in nest pre-dation pressure – and hence in the benefits dominants gain from subordinate help – to test whether reproductive concessions can explain communal breeding. Our data show that subordinate females in territories with high predation risk (i.e. when subordinates provide a direct benefit to dominants) were substantially more likely to reproduce (Fig. A.2).
126
Number of fodies in territory 0 1 2 3 4 5 6 7 8 9 10 Pr opo rti on ha tc hed c lu tc he s 0.0 0.2 0.4 0.6 0.8 1.0 without subordinates with female subordinate
FIGURE A.1. The effect of predator density (number of Seychelles fodies in the territory) and the presence of a subor-dinate female on hatching success in Seychelles warbler nesting attempts. Hatching success is lower in territories where
more egg predators are present (black line; n = 385 clutches), but the presence of subordinate females (who help protect the clutch by incubation) mitigate this effect (red line; n = 146 clutches). Solid and dashed lines respectively reflect model predicted means and standard errors.
Number of fodies in territory 0 1 2 3 4 5 6 7 8 9 10 Pr opo rti on s ubo rd ina te fe m al es rep rodu ci ng 0.0 0.2 0.4 0.6 0.8 1.0
FIGURE A.2. Subordinate female Seychelles warblers are more likely to reproduce if the risk of egg predation is higher.
The solid and dashed lines respectively reflect model predicted means and standard errors from a logistic regression controlling for food abundance.
Importantly, the likelihood of subordinate reproduction was not related to food abundance (β ± SE = -0.011 ± 1.202, Z = -0.009, P = 0.993). Unlike subordinate females who did not repro-duce, reproducing subordinates always incubated (see Richardson et al. 2002; in this study 100% of 10 individuals vs 50% of 10 non-reproducing individuals; Fisher exact test: P = 0.033; Fig. A.3) and, given they were still alive, they always stayed in the territory until the next breeding season (100% of 11 reproducing individuals vs. 67% of 12 non-reproducing stayed; P = 0.09). Thus, as female subordinates are more likely to reproduce in areas with a higher number of fodies (Fig. A.2), territories with more fodies were also considerably more likely
to have two females incubating (β ± SE = 0.613 ± 0.135, Z = 4.525, P < 0.001). This was both the result of subordinates in territories with more fodies being substantially more likely to in-cubate (β ± SE = 0.588 ± 0.236, Z = 2.497, P = 0.013; Fig. A.3) and territories with more fodies being more likely to have a female subordinate in the first place (β ± SE = 0.383 ± 0.110, Z = 3.488, P < 0.001).
Studies of the mechanisms underlying communal breeding are often fraught with alterna-tive explanations and potential confounds (Clutton‐Brock 1998). Kin-selection theory pre-dicts that subordinates help if this improves the reproductive success of related dominants (Hamilton 1963), and that subordinates are more likely to stay in groups if they are related to dominants (i.e. nepotism; Kingma et al. 2016a). However, in our study, adult subordinate females were normally unrelated to one or both dominant individuals (73% of individuals). Therefore, the subordinate female’s presence and helping behaviour cannot be explained simply by kin-selected benefits or nepotism. However, concession models of reproductive skew predict that reproduction is more likely to be conceded to unrelated than to related subordinates (Johnstone 2000; Reeve 2000). If subordinate-dominant relatedness decreas-es with increasing predation risk as a rdecreas-esult of e.g. differential dispersal decisions and/or breeder turn-over, than reproductive concessions might be explained by changes in relat-edness. Previous studies have further indicated that reproductive success increases with age in the SW, with peak reproduction around 6 or 7 years of age (Komdeur 1995; Ham-mers et al. 2012). Subordinates that initially delay dispersal often stay to co-breed with the dominant female for several years, and increased reproduction by subordinates could thus be the consequence of increasing subordinate age. To conclusively show that reproductive concessions are the result of increased predation risk and not the consequences of age or relatedness, such effects should be taken into account.
Pr op ort io n su bo rd ina te fe m al es in cu ba tin g 0.0 0.2 0.4 0.6 0.8 1.0
Subordinate reproduced?yes no
0.0 0.2 0.4 0.6 0.8 1.0 0 1 2 3 4 5 6 7 8 9 10 Number of fodies in territory
A
B
FIGURE A.3 Egg predation risk promotes cooperation in Seychelles warblers.
When there are more fodies in the territory, (A) adult subordinate females are more likely help (n = 136), and (B) subordinates are almost twice as likely to help if they have reproduced. Solid and dashed lines, respectively, reflect model predicted means and standard errors.
128
Social species differ greatly regarding the mechanisms underlying cooperative breeding and the level of conflict over reproduction, ranging from no obvious conflict (this study) to infanticide (as e.g. in meerkats; Clutton-Brock, Hodge & Flower 2008). We argue that the an-swer to this diversity may lie in the different types of benefit (i.e., survival vs. reproduction) accruing to subordinates and dominants. Reproductive conflict is expected to be great-est in species where group formation occurs due to inherent benefits of group living, but where per capita reproduction decreases with increasing group size (i.e. resource defence benefits in Shen et al. 2017). However, in species where there are no direct benefits of being in a larger group, but per capita reproductive success increases due to mutualistic benefits (i.e. collective action benefits in Shen et al. 2017) conflict over reproduction should be small or absent. In line with this, previous studies have concluded that dominant warblers can evict subordinates from the territory (Eikenaar et al. 2007; Kingma et al. 2016a; Groenewoud
et al. 2018), but that conflict over reproduction is limited (Komdeur 1991). However, in other
species where there are clear benefits of group-living, such as meerkats (Clutton-Brock et al. 1999), but where per capita reproduction decreases in larger groups, reproductive conflict is rife, and the inability of dominants to fully control subordinate reproduction often leads to the occurrence of infanticide and egg destruction. Thus, overall, our results show that once groups are established, the mutual benefits of improved nest protection can explain cooperation and communal breeding as a peaceful transaction between group members, with few incentives for cheating and reproductive conflict.
