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Micro-Evolutionary Change and Population Dynamics of a Brood Parasite and Its Primary Host: the Intermittent Arms Race Hypothesis

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Micro-Evolutionary Change and Population Dynamics of a Brood Parasite and Its Primary Host: the Intermittent Arms Race Hypothesis Oecologia (1998) 117:381±390 Ó Springer-Verlag 1998 Manuel Soler á Juan J. Soler á Juan G. Martinez Toma sPe rez-Contreras á Anders P. Mùller Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis Received: 7 May 1998 / Accepted: 24 August 1998 Abstract A long-term study of the interactions between Key words Brood parasitism á Clamator glandarius á a brood parasite, the great spotted cuckoo Clamator Coevolution á Parasite counter-defences á Pica pica glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of Introduction both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive Avian brood parasites exploit hosts by laying eggs in mechanisms: nest density and breeding synchrony in- their nests, and parental care for parasitic ospring is creased dramatically and rejection rate of cuckoo eggs subsequently provided by the host. Parasitism has a increased more slowly. A stepwise multiple regression strongly adverse eect on the ®tness of hosts, given that analysis showed that parasitism rate decreased as host the young parasite ejects all host ospring or outcom- density increased and cuckoo density decreased. A lo- petes them during the nestling period (Payne 1977; gistic regression analysis indicated that the probability Rothstein 1990). Thus, there is strong selection acting on of changes in magpie nest density in the study plots was hosts to evolve defensive mechanisms against a brood signi®cantly aected by the density of magpie nests parasite which, in turn, will develop adaptive counter- during the previous year (positively) and the rejection defences. The scenario is thus set for an evolutionary rate of mimetic model eggs (negatively). These results arms race between the brood parasite and its host(s) are consistent with a hypothesis (the intermittent arms which is presumed to result in rapid coevolution (Payne race hypothesis) of spatially structured cyclic changes in 1977; Dawkins and Krebs 1979; Mason and Rothstein parasitism. During periods of parasitism, host defences 1986; Davies and Brooke 1988, 1989; Moksnes and continuously improve, and as a consequence, the ®tness Rùskaft 1989; Rothstein 1990). This assumption has gains for parasites decrease. When host defences against recently received strong experimental support (Brooke parasites reach a high level, dispersing parasites have a and Davies 1988; Davies and Brooke 1988, 1989; Mo- selective advantage if they are able to emigrate to areas ksnes and Rùskaft 1989; Soler and Mùller 1990; Briskie of low resistance. Once parasites have left an area hosts et al. 1992; Soler et al. 1994b). However, arms races have will lose their defensive adaptations due to their cost usually been considered to be continuous (Payne 1977; in the absence of parasitism. The scene is then set for Dawkins and Krebs 1979; Davies and Brooke 1988; re-colonization by great spotted cuckoos. Rothstein 1990). The puzzling absence of adaptations, such as the lack of chick discrimination, or the lack of egg rejection in some hosts, has been explained in two exclusive ways: a stable outcome of the continuous brood parasite-host arms race (an evolutionary equilib- M. Soler (&) á J.J. Soler á J.G. Martinez á T. Pe rez-Contreras rium explanation) (Rohwer and Spaw 1988; Brooker Departamento de Biologõ a Animal y Ecologõ a, and Brooker 1990, 1996; Lotem et al. 1992, 1995), or as Facultad de Ciencias, Universidad de Granada, evolutionary lag in the host's response during a con- E-18071 Granada, Spain tinuing evolutionary arms race (Dawkins and Krebs e-mail: [email protected], fax: +34-58-243238 1979; Rothstein 1990; Davies and Brooke 1988, 1989; A.P. Mùller Moksnes et al. 1990). Laborotaire d'Ecologie, CNRS URA 258, Davies and Brooke (1989), when describing a num- Universite Pierre et Marie Curie, BaÃt. A, 7eÁ me e tage, 7 quai St. Bernard, Case 237, ber of stages in a continuous coevolutionary arms race F-75252 Paris Cedex 05, France between the common cuckoo (Cuculus canorus) and its 382 hosts, assumed that if the host species is free from gust (Soler et al. 1994a). An average of 2.4 (n 411) cuckoo eggs parasitism, then, as a consequence of the costs associ- are laid per magpie nest (Soler et al. in press). As a rule, the egg of the great spotted cuckoo hatches several days before the eggs of the ated with rejection behaviour, defences would disappear magpie host. After hatching, the cuckoo chick does not eject from the host population. Furthermore, it has been magpie eggs; however, magpie nestlings usually starve because they suggested that the loss of discrimination behaviour in lose in intense competition for food with the large, fast-growing the absence of parasitism could enable subsequent cuckoo young (Cramp 1985; Soler 1990; Soler and Soler 1991). re-exploitation by the parasite (Brooker and Brooker Magpies do not recognize the parasitic chick, and thus do not respond by not providing food to a parasite (Rothstein 1990; Soler 1990; Marchetti 1992). In order to account for obser- et al. 1995). vations and experiments we here propose the intermit- The magpie is a medium-size, omnivorous passerine bird tent arms race hypothesis, which suggests that periods (43±50 cm) that occurs in widely diering environments. It builds of frequent parasitism will alternate with periods of no large domed nests in bushes or trees. The breeding success of magpies is strongly reduced by the brood-parasitic great spotted or rare parasitism. During periods of intense parasit- cuckoo. Most parasitized nests produce no magpie chicks; on ism, host defences are continuously improving and, as a average, there are only 0.6 magpie ¯edglings per parasitized nest consequence, the reproductive bene®ts for parasites are while the success of unparasitized nests in comparison is 3.5 magpie decreasing. Once host defences have reached a high ¯edglings (Soler et al. 1996). The reproductive failure of the magpie is due to both egg destruction by adult cuckoos and nestling level, brood parasites will bene®t from emigration from cuckoos outcompeting magpie chicks (Soler et al. 1996). the area. After a period of parasites being absent, hosts The ®eld work was carried out in Hoya de Guadix, an area of will lose their defensive adaptations against parasites, presumably recent sympatry between cuckoos and magpies, a high- and it will then be advantageous for the brood parasite altitude plateau at about 1000 m above sea level, with a semi-arid to re-colonize the area. We investigate this hypothesis climate. It is covered by sparse vegetation and agricultural crops. Habitat is patchy, treeless areas alternating with holm oak (Quercus by analysing data on the history of parasitism by the rotundifolia) patches and almond (Prunus dulcis) plantations; the great spotted cuckoo (Clamator glandarius) and its preferred nesting habitat of magpies. A total of ten study plots magpie (Pica pica) host in a number of study plots in separated by treeless areas were studied in Hoya de Guadix over southern Spain over a period of 14 years. The inter- more than 3 years. Relevant information about each study plot is given in Table 1. The distance between neighbouring study plots mittent arms race hypothesis predicts that parasitism was 0.5±8 km, and the two most distant study plots were 25 km rate should continuously increase for a number of apart. More detailed information about the study area and a map years, and after having reached a maximum, decrease, can be found in Soler et al. (in press). giving rise to a cycle. The evolutionary equilibrium In some analyses we have distinguised between study plots with abundant resources and resource-poor plots. The former are on hypothesis predicts a constant parasitism rate, while irrigated land, which considerably increases the abundance of in- the continuous arms race hypothesis predicts a contin- vertebrates [the main food of magpies (Soler and Soler 1988) and uous increase (or decrease) in parasitism rate, but never their chicks (Martinez et al. 1992)] in this otherwise very dry part of a cycle. Spain. General ®eld procedures Methods We studied host-parasite interactions during 1982±1995, but most Species and study area data were collected in 1982±1983 and 1990±1995. In Hoya de Guadix, a total of 912 magpie nests were found, 496 of which The great spotted cuckoo (38±40 cm) is an obligate brood parasite (54.4%) were parasitized by the great spotted cuckoo. Magpie nests which in Europe mainly parasitizes the magpie, although other were located during regular visits (usually once per week) to our species of the corvid family are known to be used occasionally study plots from the start of the nest-building period. The nests (Soler 1990). Palaearctic populations of the great spotted cuckoo were visited at least once a week. We recorded the percentage of are migratory and those breeding in Europe are believed to winter magpie nests parasitized in each plot counting a nest as parasitized in Africa, south of the Sahara (Cramp 1985). They arrive in our if it contained at least one cuckoo egg. study area in late February or early March (Soler 1990). Adults The size of study plots was calculated using aerial photographs leave the study area in mid-June, disappearing over a few days, taken in 1990 at a scale of 1:8.000. These areas were subsequently while ¯edglings usually leave during July or the beginning of Au- used for calculating population density. Table 1 Characteristics of study plots in Hoya de Guadix Plot Quality Area Duration of study No.
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