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Though researchers have advocated a more direct, mechanistic link between individual- and population-level processes (Wiens et al. 1993; Lima & Zollner 1996; Sutherland 1996; Lidicker 2002; Zollner & Lima 2005), translating the behaviour of individuals to the spatial distribution of populations has remained a major challenge in ecology (Morales & Ellner 2002; Biro, Post & Parkinson 2003). There remain few empirical studies attempting this integration (Levin et al. 2000), particularly studies that monitor the behaviour of individuals at the whole-system scale (Biro et al. 2003) and that test alternative mechanisms generating population phenomena (Jones 2001). Small-scale studies are useful for understanding the behaviour of individuals, but the scale at which they are conducted limits our understanding of the importance of behaviours in determining population processes (Lowe 2003; McMahon & Matter 2006). For example, studies have tested the effects of competitor and predator cues on the oviposition preferences of insects in a laboratory setting; however, it is unclear how important observed behaviours are in a natural setting where insects are exposed to a variety of different cues (Munga et al. 2006). Field studies, on the other hand, can be conducted at scales that are relevant to populations, but often they do not examine the actual behaviour of individuals (Jones 2001; Lidicker 2002) (e.g. field studies of the distribution of mosquito offspring: Lounibos 1981; Barker et al. 2003b). For this reason, field studies often cannot distinguish patterns generated by behaviour (e.g. habitat or oviposition preferences) from patterns generated by other processes (e.g. spatial differences in mortality) (Jones 2001).
One situation where the empirical link between behavioural and spatial population distribution is often assumed but rarely demonstrated is the influence of oviposition-site selection on the distribution of insect offspring. The link between oviposition and population distribution is presumably strong because the manner in which females distribute their offspring across a heterogeneous environment has direct consequences for population distribution, offspring survival and individual fitness (Reiskind & Wilson 2004; Rudolf & Rodel 2005). Empirical studies have examined oviposition and its consequences for offspring performance in several insects including galling sawflies, wasps, and aphids (reviewed in Jaenike 1990; Price 1994), grass and leaf miners (e.g. Scheirs, De Bruyn & Verhagen 2000), and butterflies (e.g. Bossart 2003; Ladner & Altizer 2005). However, most of these studies have been performed in controlled laboratory conditions and may not therefore be relevant to the behaviours and performance of organisms in natural settings. Other studies have examined the consequences of oviposition preference for spatial population distribution in the field by documenting the distribution of offspring among habitats (mosquitoes, Lounibos 1981; aquatic beetles, Binckley & Resetarits 2005; tree frogs, Rudolf & Rodel 2005). However, these field studies rarely study the pre-oviposition behaviour of adults and often assume that offspring distribution reflects adult oviposition preferences (e.g. Barker, Brewster & Paulson 2003a; Barker et al. 2003b; Rapley, Allen & Potts 2004; Heisswolf, Obermaier & Poethke 2005). This is despite the fact that several processes other than oviposition preference can generate spatial patterns of offspring density, such as dispersal limitations or spatial differences in mortality.
Previous work has demonstrated that the spatial distribution of offspring (eggs and larvae) of the eastern tree hole mosquito Ochlerotatus triseriatus (Say) is aggregated in the north-eastern USA (Ellis 2007). Within a 0·02 km2 area that included three adjacent habitats (open field, deciduous forest with dense understory vegetation, evergreen forest with little understory vegetation) of approximately equal size (c. 0·006 km2), more eggs and higher larval densities were found in the deciduous forest stands (Ellis 2007). The correlation between oviposition pattern and offspring distribution observed in the study suggests that aggregated distributions of offspring may result from (Hypothesis 1) preferences for habitats with particular vegetation characteristics by ovipositing females. However, several mechanisms in addition to habitat selection could generate the previously observed aggregated distribution of O. triseriatus offspring. First, mosquitoes may actually distribute their eggs randomly or evenly throughout their environment, but there may be spatial differences in egg mortality or hatching success (Hypothesis 2). Second, mosquitoes may randomly colonize particular areas but have limited dispersal capability (Hypothesis 3) causing them to distribute offspring in a relatively small area where founder populations were established. Third, mosquitoes may passively aggregate in particular habitats due to environmental factors such as wind turbulence (Hypothesis 4). Finally, spatial heterogeneity in adult mortality (Hypothesis 5) may generate clumped distributions of adults and, subsequently, their offspring. These hypotheses are not mutually exclusive, and certain aspects of them may operate simultaneously. However, incorrectly assuming that offspring distributions are generated primarily by oviposition preferences may not only compromise our ability to understand the mechanisms determining population dynamics, but may have important implications for our understanding of the evolutionary relationships among life-history traits (e.g. oviposition preference and offspring performance).
Accordingly, the purpose of this study was to evaluate at the whole-system scale the movement and oviposition behaviours of adult tree hole mosquitoes that may generate the previously observed aggregated distribution of their offspring. A mark–release–recapture experiment was performed to distinguish among the alternative hypotheses presented above. I predicted that: (1) the distributions of eggs and adults are clumped (not random or overdispersed) within a 0·01–0·02 km2 area; (2) dispersal is not passive or limiting within a 0·02 km2 area; and (3) the distribution of adults is associated with specific habitat characteristics. These results would provide support for the habitat selection hypothesis (Hypothesis 1).
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Theory predicts that females should distribute their offspring to maximize offspring performance (Rausher 1983; Schriber 1983; Thompson 1988; Valladares & Lawton 1991; Nufio & Papaj 2004). However, the distribution of offspring can be determined by a number of factors other than the oviposition preferences of adults (H1), such as spatial differences in egg mortality or hatching success (H2), dispersal limitations (H3), passive aggregation (H4), or spatial differences in adult mortality (H5). Here, a mark–release–recapture experiment was performed to distinguish among these alternative hypotheses.
Results were consistent with the hypothesis that tree hole mosquitoes exhibit some degree of habitat selection (H1), but did not rule out the possibility that observed distributions were influenced by passive physical aggregation (H4) or site-specific differences in adult mortality (H5). Clumped distributions of eggs and recaptures were not consistent with the hypothesis that aggregated offspring distributions are generated by random or overdispersed oviposition with spatial differences in egg hatch or success (H2). However, differences in the degree of clumping and differences in the amount of variability in environmental variables among the two sites suggest that differences in forest structure or the size of the forest patch may have been important in generating a more clumped distribution of adults and offspring in the Piermont site. This may have occurred because the Piermont site has more diverse microhabitats or because the forests differ in the spatial clustering of abiotic factors or the scale at which the forest structure changes.
The movement of tree hole mosquitoes also did not appear to be passive via prevailing wind or limiting in a 0·02 km2 patch of forest, which is not consistent with the hypothesis that aggregated offspring distributions are determined by random colonization followed by limited dispersal from founder populations (H3). Though the location of recaptures in this study did not appear to be related to the prevailing direction of wind, results cannot completely rule out the hypothesis of passive aggregation (H4). Vegetation within the forest can create turbulent wind flow (Clements 1999), which may have influenced movement on smaller spatial scales within each site. Mosquitoes may congregate in sites with more understory vegetation if, for example, sites with more vegetation tend to be the least windy (H4). Passive physical aggregation has been observed in other insects with weak flight capacity in sheltered areas (e.g. gall midges and moth flies, Lewis & Stephenson 1966); however, because vegetation also lowers wind speeds inside the forest, particularly at ground level (Clements 1999; Compton 2002) and because wind speeds tended to be low throughout the experiment (except for one short storm shortly after the first release), wind speeds were probably lower in the forest than the speed at which the flight of mosquitoes becomes depressed (c.3 m s−1 for mosquitoes, Clements 1999). Moreover, many studies indicate that small-bodied winged insects can control the degree to which movement is affected by wind (Johnson 1969; Isaacs & Byrne 1998; Loxdale & Lushai 1999). O. triseriatus and other mosquitoes, locusts, aphids, and other dipterans have been found to fly close to the ground where wind speeds are low (Taylor 1960, 1974; Isaacs & Byrne 1998), quickly stop flying when wind speeds increase (Johnson 1969; Clements 1999), and/or take flight only when winds are calm (Johnson 1969). Additionally, O. triseriatus and many other winged insects (e.g. mosquitoes, aphids, whiteflies and thrips) fly primarily at dusk and dawn when wind speeds are typically lower (Service 1971a; Clements 1999; Loxdale & Lushai 1999; Compton 2002), allowing them greater control over their flight (Southwood 1962; Taylor 1974; Loxdale & Lushai 1999). These behavioural processes greatly increase the opportunity for tree hole mosquitoes to have active and directed flight. In fact, when winds are low, it may be more likely that differences in wind speed are used as cues that mosquitoes use to select particular habitats. Future studies examining this issue in mosquitoes are clearly needed.
Results also demonstrated that more marked females were recaptured in sites with dense understory vegetation (< 1 m), little foliage between 1 and 2·75 m, and a more open canopy providing support for the hypothesis that mosquitoes exercise some degree of habitat selection (H1). Though some studies have examined the movement of adult mosquitoes (e.g. Lounibos 1981; Beier et al. 1982; Barker et al. 2003a,b), very few have focused on the searching behaviours of gravid females prior to oviposition (Clements 1999). In fact, very few studies in general have examined the day-to-day trivial flight of adult winged-insects (Loxdale & Lushai 1999). Results presented here are consistent with increasing evidence that many woodland mosquito species such as O. triseriatus can be found in dense ground vegetation and may exhibit highly patchy distributions associated with vegetation type (Service 1971b; Beier et al. 1982; Clements 1999). Though mosquitoes may select habitats in part based on the density or diversity of blood meal hosts within them (Clements 1999), individuals in the current study were released after obtaining a blood meal in the laboratory. Because females remain unresponsive to hosts for c. 1–3 days after blood-feeding (Bentley & Day 1989; Clements 1999), host cues were probably not important in determining movement behaviours during the initial days following a release, but may have influenced movement after this refractory period.
The association of adult densities with vegetation characteristics does not, however, completely rule out the possibility that distribution patterns are also influenced by differential adult mortality in different parts of the forest (H4). Though predation is one obvious mechanism that could generate site-specific mortality, very little is known about the impact that predators may have on the densities of adult mosquitoes other winged forest insects. Studies have documented the potential for predation of mosquitoes by spiders (Roitberg, Mondor & Tyerman 2003; Jackson, Nelson & Sune 2005), but their influence in natural settings is unknown. Insectivorous bats in New Hampshire can consume up to half their weight in insects nightly; however, mosquitoes are typically only a small portion of their total insect diet (Anthony & Kunz 1977). Moreover, bats may tend to exploit only local mosquito swarms that can be spatially and temporally variable (Anthony & Kunz 1977). Thus, the effect of predation on insect density is probably highly localized, temporally variable and minor at a landscape scale. Moreover, results presented here demonstrate that tree hole mosquitoes have the ability to disperse quickly such that local effects of predation would be quickly masked unless predation rates are exceptionally high (i.e. greater than dispersal rates) and consistent at small spatial scales. More studies are clearly needed to determine the influence of predation on the distribution and abundance of mosquitoes and other winged insects in natural systems.
Based on theory (e.g. the preference–performance hypothesis) (Rausher 1983; Schriber 1983; Thompson 1988; Valladares & Lawton 1991; Nufio & Papaj 2004), a weak oviposition preference suggested by results of the current study should be an evolutionary consequence of differences in offspring fitness among habitats. In accord with these expectations, a previous study with tree hole mosquitoes in New Hampshire demonstrated differences in offspring fitness that would be consistent with the evolution of weak habitat preferences for habitats with little understory vegetation (Ellis 2007). At low densities, offspring performance did not differ among deciduous forest habitats with dense understory vegetation and evergreen habitats with little understory vegetation suggesting that when overall densities are low, no fitness differences exist between habitats. However, offspring performance was higher in habitats with more understory vegetation when larval densities were high. Thus, preferences for habitats with dense understory vegetation would be favoured when regional abundances are high, but would not be favoured when regional abundances are low. Temporal variability in abundance could therefore select for weak habitat preferences such as those suggested by the results of the current study.