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Carnus Hemapterus 1 Mixed life-history strategies in a local population of the ectoparasitic fly Carnus hemapterus M. AMAT-VALERO1*, R. VÁCLAV2, T. MARTÍNEZ3 and F. VALERA1 1 Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. Sacramento s/n, La Cañada de San Urbano, 04120 Almería, Spain 2 Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, 84506 Bratislava, Slovakia 3 C/Catavieja 31. 1°B, 04007 Almería, Spain (Received 6 December 2011; revised 13 February 2012; accepted 22 February 2012) SUMMARY A major issue for the proper understanding of the evolution of life-cycle histories is the regulation of voltinism and its variation. Diapause characteristics are known to regulate voltinism, but the underlying mechanisms are poorly understood. This paper studies diapause duration and voltinism variation in a haematophagous diptera parasitizing 2 sympatric hosts with very different breeding phenologies. We hypothesize that bivoltinism will be more frequent in carnid flies parasitizing an early breeding, multi-brooded species than in flies parasitizing a late breeder, single-brooded species. We obtained evidence of the co-occurrence of uni- and bivoltinism in both clutches of the multi-brooded Spotless starling (Sturnus unicolor) as well as in clutches of the single-brooded European roller (Coracias garrulus). Unexpectedly, the proportion of bivoltine flies was similar in both host species. A remarkable degree of host-parasite synchronization at the population level was found for bivoltine flies. Our findings reveal the facultative nature of diapause in Carnus. We discuss the influence of abiotic conditions and host availability on polymorphism in life-history cycles and the consequences both for the parasite and the host. Key words: Carnus hemapterus, voltinism, diapause, life-history strategies, phenotypic plasticity. INTRODUCTION the number of generations per year varies. In habitats with long favourable periods and high resource One of the central issues in the evolution of life availability, some species can shorten the cycle, histories in insects is the mechanism behind variation develop fast with short diapauses, and give rise to a in voltinism (Taylor and Spalding, 1988). Abiotic generation within days (Campbell and Mackauer, and biological factors, like food or natural enemies, 1975; Tillman and Powell, 1991; Sabelis and Janssen, are known to influence the number of generations 1994). These are multivoltine species. In regions with of insects per year (voltinism) (Masaki, 1980; Tauber short seasons and where the resources are not always et al. 1986). These animals have evolved to use available, multiple generations do not occur and developmental mechanisms, particularly diapause, to many species are strictly univoltine (Danks and synchronize their life cycles with seasonal changes in Foottit, 1989; Danks, 2002). resource availability and climatic conditions suitable In many parasitic insect species, life-cycle duration for their development, growth and reproduction. varies within the population (Tauber and Tauber, Diapause is a form of dormancy influenced both by 1981; Danks, 1987, 1992; Menu et al. 2000). In genetic and environmental factors. It enables insects animals with facultative diapause, dynamic temporal to survive unfavourable conditions, to synchronize risk spreading and adaptive developmental plasticity their active stages with resource availability and to (Stearns, 1976) appear to have evolved to regulate disperse and colonize new habitats efficiently (Tauber diapause frequency and duration in response to et al. 1986; Danks, 1987, 1992; Soula and Menu, uncertain environments (Bradford and Roff, 1993; 2003; Kostal, 2006). In insects, diapause is governed Soula and Menu, 2003). Thus, a single genotype may by reliable environmental signs preceding seasonal produce multiple phenotypes, some of which enter changes (Tauber et al. 1986). Duration of the seasons diapause whereas others continue to develop and influences the diapause period, which may range produce offspring (Hopper, 1999;Heet al. 2010). between days and months, or even years. Therefore, Whereas the variation of voltinism over a geographi- cal range as a result of local adaptation has been * Corresponding author: Departamento de Ecología widely described in insects (Tauber et al. 1986; Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. Sacramento s/n, La Cañada de Danks, 1987), the phenotypic plasticity of voltinism San Urbano, 04120 Almería, Spain. E-mail: amat@eeza. in a local population has been seldom reported and is csic.es poorly understood (He et al. 2010). Parasitology, Page 1 of 9. © Cambridge University Press 2012 doi:10.1017/S0031182012000534 M. Amat-Valero and others 2 Carnus hemapterus Nitzsch (1818) is a generalist Carnus hemapterus (Nitzsch 1818, Phylum parasite whose entire cycle, including diapause, takes Arthropoda, Class Insecta, Order Diptera, Family place in its host’s nest. It parasitizes a wide range of Carnidae) (hereafter Carnus) is a 2 mm long, highly bird species whose phenology varies considerably mobile ectoparasitic fly that colonizes nestling birds (Grimaldi, 1997). A degree of synchronicity has been (Grimaldi, 1997). It has a wide geographical distri- recorded between the appearance of the host and bution and parasitizes a variety of host species, its parasite’s emergence (Liker et al. 2001; Valera et al. although it shows some preference for birds nesting 2003). It has therefore been assumed that some in holes (troglodytic species) (Dawson and Bortolotti, environmental signs must exist to regulate such 1997; Grimaldi, 1997). Adult flies have a winged and synchronicity. Still poorly-known, the plasticity wingless phase. After their emergence, adults are of Carnus diapause seems to be remarkable: (i) 3 initially winged, but lose their wings as soon as they different types of diapause have been described, locate a suitable host (Roulin, 1998). Carnid flies do namely a short diapause (Guiguen et al. 1983), a not need a host for transmission because they actively winter diapause to resist the adverse environmental colonize hosts’ nests during the winged phase of conditions and food shortage (Guiguen et al. 1983; their life cycle (Grimaldi, 1997). Once emerged, the Grimaldi, 1997), and a long diapause that may imagines can survive for slightly less than 3 days prolong itself for years (Valera et al. 2006); (ii) without feeding. Carnid flies complete their cycle experiments have proved that temperature changes in their hosts’ nests. Adults mate in the nest, lay eggs at the end of the diapause influence the emergence which hatch approximately 5 days later, and the phenology of the parasite, which ultimately means larvae live on the organic matter in the nest (Capelle some plasticity in diapause termination in Carnus and Whitworth, 1973; Papp, 1998). The 3 larval (Calero-Torralbo and Valera, 2008). stages last 21 days (Guiguen et al. 1983) and pupation This paper examines variation in voltinism in a takes place in the nest. During the pupal stage, local population of Carnus hemapterus in southern Carnus undergoes a diapause that usually lasts for Spain. Resident bird species at temperate latitudes months. Carnus emergence is usually synchronized like ours start breeding early in the season and usually with the occurrence of the host (i.e. hatching) and produce several clutches. These species usually co- persists continuously throughout the whole nestling exist with migrant bird species, which start breeding period (Roulin, 1998; Liker et al. 2001; Valera et al. later and, therefore, produce a single brood. The 2003; Calero-Torralbo and Valera, 2008). Guiguen starting hypothesis is that the length of the breeding et al.(1983) described a short, 8-day diapause in season of bird species (i.e. Carnus’ hosts) influences spring in laboratory conditions, and Valera et al. diapause duration and that the co-occurrence of (2006) recorded a prolonged diapause that may last various host species with different breeding phenol- for years. ogy foster the co-existence of various life-cycle In southern Spain, the Spotless starling Sturnus strategies (multi- vs univoltinism). Flies which unicolor and the European roller Coracias garrulus are parasitize early breeding, multi-brooded bird species common avian breeders. These species readily use are expected to undergo short diapause and to be nest boxes and are commonly parasitized by Carnus multivoltine, while flies which parasitize late breed- (Liker et al. 2001; Václav et al. 2010). The Spotless ing, single-brooded bird species, like trans-Saharan starling is a resident species in the Iberian Peninsula. migrants, are expected to undergo long diapause and The breeding period begins in early March and some to be univoltine. To this end, we studied the pairs in our study area have a second clutch at the end emergence phenology of adult flies in nests of a bird of May. Incubation lasts for approximately 10 or 15 species with an early reproductive cycle as a model of a days, from the last laid egg until the first hatched egg multi-brooded species, the Spotless starling (Sturnus (Peris, 1984). European rollers are migratory birds unicolor), and also in nests of a bird species with a late that arrive at breeding grounds when resident and reproductive cycle as a model of a single-brooded secondary cavity-nesting birds are already settled. species, the European roller (Coracias garrulus). Rollers rear a single brood per year (Cramp, 1998). In our population incubation lasts for approximately 21 days and nestling rollers fledge about 20–22 days after MATERIALS AND METHODS hatching (R. Václav, unpublished data). European rollers are the latest breeders in our study area, with Study area and species the tardiest nestlings remaining in the nest until as The main study area (*50 km2) lies in the Desert late as the third week of July. of Tabernas (Almería, SE Spain, 37°05′ N, 2°21′ W). The climate in this area is semi-arid with high annual Experimental approach and seasonal rainfall variability (mean annual rainfall ca. 218 mm), and strong thermal oscillations with The number of generations per year and the existence inter-annual differences.
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