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Killing Behaviour of Adult Brood Parasites

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Killing Behaviour of Adult Brood Parasites 1 SPECIAL: ANECDOTES IN ANIMAL BEHAVIOUR 2 Killing behaviour of adult brood parasites 3 Šulc M.1,*, Štětková G.1,2, Jelínek V. 1, Czyż B.3, Dyrcz A.3, Karpińska O.4, 4 Kamionka-Kanclerska K.4, Rowiński P.4, Maziarz M.5, Gruszczyński A.5, Hughes A.E.6, 5 Honza M. 1 61Institute of Vertebrate Biology of the Czech Academy of Sciences, Brno, Czech Republic 72Department of Botany and Zoology, Faculty of Sciences, Masaryk University, Brno, Czech 8Republic 93Department of Behavioural Ecology, University of Wrocław, Wrocław, Poland 104Department of Forest Zoology and Wildlife Management, Warsaw University of Life 11Sciences (SGGW), Warsaw, Poland 125Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, Poland 136Department of Psychology, University of Essex, Colchester, U.K. 14*corresponding author: Michal Šulc ([email protected]) 15 16Summary 17Decades of studies have revealed the striking adaptations of avian brood parasites for 18their unique reproductive lifestyle. Several have reported that adult brood parasites 19sometimes kill host nestlings, although the reasons for this behaviour remain unclear. 20Using continuous video-recording and camera traps, we observed the same behaviour in 21the common cuckoo Cuculus canorus, showing that both host and parasite nestlings can 22be killed. The latter has never previously been observed in any avian brood parasite. 23Here, we review this phenomenon and discuss possible explanations. 24 25Keywords: nestling infanticide, chick ejection, farming, Mafia, co-evolution 26 27Main text 28Infants are an obvious target for extermination because of their vulnerability, therefore they 29are often exploited by various predators (Weidinger 2009). Apart from this relatively simple 30predator–prey relationship, there is also the phenomenon of infanticide when a young 31offspring is killed by an adult animal of the same species. This has been observed in 32numerous species from diverse taxonomic groups including insects, fish, amphibians, birds 33and mammals (Hrdy 1979; Hausfater & Hrdy 2017). Although this behaviour was originally 34considered to be pathological (especially cases of filial infanticide when a parent kills their 35own offspring), we now know that it may be an adaptive behaviour, e.g. reducing competition 36for limited resources (Hoogland 1985) or allowing monopolization of reproduction (Haines et 37al. 2018). 38 Over the last 130 years, adults of several avian brood parasitic species have been also 39observed killing host nestlings (Table 1) for reasons that are less understood. This behaviour 40has predominantly been observed in the two most frequently studied parasitic species, the 41common cuckoo Cuculus canorus (15 nests) and the brown-headed cowbird Molothrus ater 42(20 nests) but also in the Himalayan cuckoo Cuculus saturatus (one nest) and the Shining 43bronze cuckoo Chrysococcyx lucidus (two nests). Indirect evidence for this behaviour has also 44been found in the great spotted cuckoo Clamator glandarius. It appears to be a relatively rare 45phenomenon; we found only 24 studies (including this one) reporting about 41 events (Table 461). Many reports have involved only circumstantial evidence; however, more recent studies 47have recorded this behaviour on video-cameras (Table 1). Using continuous video-recording 48and camera traps, we observed this killing behaviour in the common cuckoo (hereafter 49cuckoo) in four different hosts: the European robin Erithacus rubecula, the wood warbler 50Phylloscopus sibilatrix, the great reed warbler Acrocephalus arundinaceus and the reed 51warbler Acrocephalus scirpaceus. Here, we present five pieces of evidence (four videos and 52photos; Videos 1-4 and Figure 1) showing the adult cuckoos ejecting nestlings out of host 53nests. Three of these cases are particularly interesting because the nestlings were young 54cuckoos (Videos 1 and 2, Figures 1 and 2). All events are independent observations recorded 55in four geographically separate breeding areas in the Czech Republic and Poland and 56therefore were performed by different cuckoo females. We believe that our literature review 57and video evidence demonstrating parasitic behaviour during these incidents may help to 58explain this peculiar behaviour of brood parasites. 59 All studies apart from one (Igl 2003) showed that only females of parasites exhibit this 60behaviour which is supported also by our recordings. The act cannot be seen as predation 61because parasites never preyed on nestlings (but see, Wyllie 1975). Since there appear to be 62no cases where parasites ejected nestlings from nest of non-host species (Weidinger 2009, and 63>1000 video-monitored nests on non-host species, K. Weidinger, unpubl. data), it seems that 64parasitic killing is aimed only at their hosts. From behaviour of parasites while ejecting 65nestlings it seems that it is an intentional act. Parasitic females grabbed the nestling and tossed 66it out of the nest immediately after arrival at the nest (Videos 1 and 2). If there were multiple 67nestlings in the nest, parasites systematically removed them one at a time (Video 4 and see 68also video published at Youtube by P. Elliott; Elliott 1999). In some cases, they tried to eject 69even under host attacks (Videos 3 and 4). Moreover, in two of our videos (Videos 3 and 4) it 70is possible to see that parasites visited nests repeatably despite initially being attacked and 71flushed away by the hosts. The number of ejected nestlings varied from one to the whole 72clutch of six (Table 1). No study reported parasitism after the ejection event occurred (but see, 73Sheppard 1996) which could indicate that parasites were aware that the host nests were not 74suitable for parasitism. From the above, and due to the fact that observed ejection behaviour is 75identical in phylogenetically distant parasitic species of cuckoos and cowbirds and convergent 76evolution could take place, we suggest that this behaviour is adaptive (Losos 2011). 77 Birds of several species have been reported to kill immature birds of the same or other 78species in contexts other than predation: for example, to compete for nesting sites (Kattan 792016), mates (Freed 1986), paternal investment (Veiga 1990) or food (Belles-Isles & Picman 801986; Freed 1987). In brood parasites, two other hypotheses have been proposed to explain 81the killing of host nestlings by adult brood parasites: the “Mafia” hypothesis and the 82“farming” hypothesis (Soler et al. 2017). The Mafia hypothesis proposes that parasites cause 83nest failure to punish a host that ejected a parasitic egg and hence to enforce its compliance in 84the future. This tactic is presumably only effective in parasitic species where offspring do not 85kill host nestlings, as only in these cases may the host parents still benefit by raising their own 86young while also accepting a parasite egg or nestling (Zahavi 1979). Thus, this strategy could 87evolve in e.g., the great spotted cuckoo and the brown headed cowbird, but not the common 88cuckoo (and other Old World cuckoos) where the young cuckoo chick usually evicts all host 89eggs or chicks (Reboreda et al. 2017). In contrast, the farming hypothesis could relate to all 90parasite species. It suggests that parasites cause failure of the host nests to force the host to re- 91nest and so to increase the opportunity for future parasitism. Both hypotheses seem to be 92valid, however, only in the context of destroying eggs (Soler et al. 1995; Hoover & Robinson 932007) not ejecting nestlings. 94 The reason why these two interesting hypotheses have not been tested is because 95nestling ejection by adult brood parasites is relatively rare. Brown-headed cowbirds ejected 96host nestlings at 11 of 334 video-monitored host nests (summary data from Granfors et al. 972001; Stake & Cavanagh 2001; Stake et al. 2004), and we recorded this behaviour at five of 98311 host nests for the common cuckoo (summary data from four different localities, for 99details, see Supplementary material). It therefore seems to be similarly prevalent in both these 2 100parasitic species (chi-square test: χ 1=1.26, P=0.26). Moreover, we found that nestling 101ejection cannot be predicted by parasitism rate because it occurred both in rarely (e.g. the 102European robin Erithacus rubecula, see Supplementary material) and frequently parasitized 103host species (e.g. great reed warbler Acrocephalus arundinaceus, see Supplementary 104material). 105 Because of the small sample sizes involved, at present we can only speculate about the 106validity of these hypotheses in explaining killing behaviour. In cowbirds, we would expect 107killing behaviour to occur at nests where hosts rejected the parasitic egg if the Mafia 108hypothesis were true (see above). However, observations at ten video-recorded host nests did 109not support this prediction because all of them were assessed as non-parasitized (Granfors et 110al. 2001; Stake & Cavanagh 2001). Therefore, it seems that cowbirds do not kill host 111nestlings to punish hosts for their non-cooperation. 112 For the farming hypothesis, we had two predictions; 1) parasites should kill all 113nestlings to make the host re-nest, and 2) the killing parasite should benefit from the host re- 114nesting and parasitize the replacement nest. We found that ejection of all nestlings occurred 115only in seven of 19 and 11 of 14 nests in cowbirds and cuckoos, respectively (Table 1). 116Therefore, it seems that parasites (especially cowbirds) often do not succeed in making hosts 117re-nest. However,
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