Oviposition in many insects appears non-random with respect to both abiotic and biotic factors of the environment. Females may gather information about environmental quality, and make oviposition decisions based upon that information. Egg-laying decisions can ultimately influence the success of a female's offspring (Butkewich, Prokopy & Green 1987; Quiring & McNeil 1987; Crump 1991). Oviposition substrates differ in numerous ways that can affect larval growth and survivorship; these differences may provide reliable cues allowing for discrimination between favourable and unfavourable sites. Presence of competitors and predators and resource quality have all been implicated as factors assessed by egg-laying insects (see reviews in Prokopy, Roitberg & Averill 1984; Roitberg & Prokopy 1987; Thompson 1988). Many insects use oviposition-deterring pheromones (Quiring & McNeil 1984) to signal that suitable hosts are already occupied (e.g. small plants, Thompson 1988; fruits, Prokopy 1981; Butkewich et al. 1987; seeds, Messina & Renwick 1985). Chemicals emanating from feeding larvae or other by-products of occupied sites can also act as epidiectic cues (see Prokopy et al. 1984; Roitberg & Prokopy 1987). Correlations have been discovered between oviposition preference and offspring performance for a number of insect species in which larvae cannot disperse (e.g. specialized herbivores and fruit feeders, parasites, and leaf and stem miners; Craig, Itami & Price 1989). This latter finding suggests that environmental cues play an important role in female choice of oviposition site. As in many herbivores and parasitoids, treehole mosquitoes (Aedes spp.) are dependent on restricted resources that differ in presence of intraspecific and intercohort competitors (Livdahl 1982; Edgerly & Livdahl 1992) and/or food sources (Léonard & Juliano 1995). Therefore, we expect that treehole mosquitoes will exhibit similarly choosy oviposition behaviour.
Aedes triseriatus (Say), a common treehole mosquito in the eastern United States, oviposits throughout the summer months. In the laboratory, egg-laying females are attracted to containers of water, particularly those with horizontal openings containing darkly coloured water and a high organic content (Wilton 1968). These characteristics are consistent with qualities typical of treeholes used by them in the field (Scholl & DeFoliart 1977; Sinsko & Grimstad 1977). Further laboratory studies have suggested that larva-produced compounds are also attractive to females (McDaniel et al. 1976). The response of A. triseriatus females to such cues may be species-specific; Bradshaw & Holzapfel (1988) found that water from treeholes occupied by conspecific larvae was more attractive than water from treeholes supporting other sympatric mosquitoes. Attractiveness of a treehole may be influenced further by conspecific eggs which become repellent as they accumulate in oviposition traps (Kitron, Webb & Novak 1989).
We generated hypotheses about egg-laying decisions by assuming that Aedes females will behave in a manner that maximizes the fitness of their offspring. These hypotheses reflect three main themes: females avoid competitive or predatory threats to their larvae; females judge larvae or eggs as cues to future permanence or productivity within a treehole; and females hedge their bets by scattering their eggs in multiple habitats (Table 1). The following sections will review predictions for each hypothesis.
|1.||Potential biotic interactions|
|1a.||Females avoid predators of larvae||Females will not lay eggs near Anopheles larvae|
|1b.||Females avoid habitats with high |
larval densities because of competition between larvae
|Females will lay eggs in less crowded habitats|
|1b1.||Response to larval density is |
influenced by timing of egg diapause
|If eggs are able to hatch immediately, females will avoid competitive |
|1c.||Females avoid eggs which reflect |
potential competition in the future
|Females will avoid laying eggs in habitats containing a relatively large |
number of eggs
|2a.||Presence of larvae indicates treehole |
|When larvae are present, females will lay eggs into the habitat|
|2b.||Eggs indicate that treehole |
held water in recent past
|Eggs attract and/or stimulate egg-laying females|
|2c.||Larval density reflects treehole |
|Females will be differentially attracted to treeholes with more larvae|
|3a.||Catastrophes within individual |
habitats occur asynchronously, and
risk of movement among habitats is low
|Females will lay eggs in multiple habitats; minimum batch size < |
potential batch size
|3b.||Catastrophes are uncommon, or |
occur synchronously within a
region; risk of movement among habitats is high
|Females will lay all eggs within a single habitat; |
minimum batch size = potential batch size
Potential biotic interactions
Egg-laying mosquitoes should avoid ovipositing in sites where aquatic predators are abundant (Chesson 1984; Tietze & Mulla 1991; Blaustein & Kotler 1993). Late instar Anopheles barberi larvae are voracious predators of young mosquito larvae (Petersen, Chapman & Willis 1969; Livdahl 1982; Copeland & Craig 1992; Willey 1993). We predict that A. triseriatus females will avoid ovipositing in treeholes that contain these predators (Table 1; hypothesis 1a).
The presence of older conspecific larvae may be unfavourable to a cohort of newly hatched larvae. Laboratory studies suggest that many A. triseriatus eggs hatch upon inundation with rainwater in the spring, while others delay hatching until repeated immersions have occurred (Livdahl & Koenekoop 1985). The resulting multiple cohort structure of A. triseriatus larval populations leads to complex and often detrimental interactions. For example, in simulated treeholes placed in the field, younger cohorts suffered adverse consequences of competition, increasing in severity as larval density increased (Livdahl 1982; Edgerly & Livdahl 1992). In these studies, detrimental effects of density were reflected in decreased sizes of adults, delayed development, and increased mortality. Of note is that the experimental densities were based on naturally occurring densities of 28, 44 and 60 larvae per 100 mL (see Livdahl 1982; Edgerly & Livdahl 1992). Newly hatched larvae may also risk cannibalism by older larvae (Koenekoop & Livdahl 1986; but see Edgerly & Livdahl 1992). We suggested that A. triseriatus eggs delay hatching under conditions of high larval density to avoid such competitive penalties (Livdahl, Koenekoop & Futterweit 1984; Livdahl & Edgerly 1987; Edgerly, Willey & Livdahl 1993). The inhibition appears to result from larvae grazing micro-organisms from the egg surfaces, thereby removing agents of oxygen consumption, which would otherwise promote egg hatching (Edgerly & Marvier 1992). Another possible mechanism for avoiding potentially competitive habitats, tested in the present study, is selective oviposition in response to larval density (Table 1: hypothesis 1b).
The repercussions of delayed hatching may depend on the time of year. If ovipositing females do respond to larvae, it seems also likely that their response could vary with season. During June and July, a female deposits eggs that can hatch and reach adulthood during that growing season. However, in northern areas, eggs enter diapause in response to a short photophase later in the summer, and hatch the following spring (Shroyer & Craig 1980). Females ovipositing in late summer may therefore face constraints different from those ovipositing early in the season. If a female in early summer oviposits into a crowded habitat, her eggs may delay hatch long enough to enter diapause, and delay development for nearly a year. If she rejects crowded habitats and instead oviposits into less populated treeholes, her eggs may hatch, thereby increasing her fitness in two ways: generation time of her offspring will be reduced, and by avoiding winter mortality, survivorship of her offspring will be increased. Although the former advantage applies specifically to growing populations, the second should apply to all populations that experience mortality during an extended period of dormancy. In contrast, a female in late summer may not reject crowded habitats, especially if the presence of larvae reflects a treehole's qualities of permanence or nutrition as argued below. Competition, while imminent early in the season, will not occur between a late summer female's progeny and those presently in the treehole because the former enter diapause, while the latter emerge as adults or die at the onset of freezing weather. Based on this logic, we predict a negative relationship between the number of eggs added during the trial and the number of larvae already present in early summer. In contrast, late summer females should not discriminate between the artificial treeholes based on number of larvae present (Table 1: hypothesis 1b and 1b1).
Clusters of eggs may portend a future, rather than immediate, competitive environment (Table 1: hypothesis 1c). Potential competition among emerging larvae may explain why abundant eggs apparently repelled females searching for oviposition sites at an Illinois field site (Kitron et al. 1989). Egg density may be a more important signal of future competition than present larval density, and we predict that the number of eggs added to ovitraps will be an inverse function of the number of eggs already present.
Females should choose treeholes with water-holding ability (Table 1: hypotheses 2a, 2b). If so, then early and late summer females should choose treeholes with older larvae, regardless of density. The presence of these older larvae indicates relative habitat permanence. We would expect significantly more eggs in habitats with larvae than without, regardless of density if habitat permanence underlies a female's response to larvae.
Eggs may accumulate over time in a treehole and their numbers may reflect relative permanence. Despite the report that eggs repel ovipositing females (Kitron et al. 1989), we predict that females could use relatively high numbers of eggs as a reflection of past water-holding capabilites of the treehole. Females are known to lay their eggs into water-filled cavities (Wilton 1968). The possibility exists that if they locate a dry treehole with eggs along the inner wall of a treehole, the eggs reflect a conspecific's response to water that evaporated in the recent past. Eggs might then be a reliable cue to water-holding. Therefore, eggs might accumulate at a higher rate in habitats that already have eggs (Table 1: hypothesis 2b). This prediction is the opposite of that predicted by the competiton hypothesis 1c.
In addition to variation in tendency to desiccate, treeholes also vary in quantity and quality of stemflow, a source of water and nutrients, and organic matter necessary for development of larvae (Walker & Merritt 1988; Léonard & Juliano 1995). If a nutrient-rich habitat is key to the survival of larvae, then egg-laying females may select treeholes occupied by larvae, particularly in late instars (Table 1: hypothesis 2c). By this hypothesis, we would expect the number of eggs to increase linearly as number of larvae increases, independent of seasonal variation.
In a risky habitat, we may expect females to adopt different strategies of oviposition, depending on when the risks are most intense during the life cycle, and whether the risks are spatially distributed in a patchy or homogeneous manner. The possible evolutionary outcomes include at least two conditions in which eggs should accumulate without regard to the presence or abundance of larvae. We set forth the following hypotheses to account for the possible observation of no response to larvae.
A bet-hedging approach, which might be anticipated in a low-risk environment for adults and a high-risk environment for larvae, is to scatter their offspring among as many habitats as possible, thereby minimizing the likelihood of losing all offspring due to a catastrophe in the larval habitat. This strategy should be most advantageous in situations when the larval habitats vary greatly in their permanence, or when catastrophes occur asynchrously among larval habitats, and when the females have no reliable means of discriminating between temporary and permament habitats or anticipating future catastrophes (Table 1: hypothesis 3a). This approach may also prevent a detectable response to larval density. However, bet-hedging females are more likely to encounter multiple habitats during repeated searches, and are therefore more likely to be able to make choices among them. Therefore, if bet-hedging occurs within an ovarian cycle, some response to cues about habitat quality might be anticipated.
A contrasting approach is more likely if females travel in a low-risk environment, when they may have much to gain by inspecting a variety of habitats before finalizing their decision about where to oviposit. In this instance, a response of females to larval density may be advantageous. However, if there is substantial risk of mortality during additional searching, or of not finding another suitable habitat, oviposition of all eggs into the first suitable larval habitat discovered, independently of larval abundance, may be the most successful strategy (Table 1: hypothesis 3b).
Adult female Aedes triseriatus experience a moderate risk of dying while searching for oviposition sites and blood-meals (daily survival ranges from 0·78 to 0·95; references in Pumpuni & Walker 1989); risk of pre-reproductive death may have led to the evolution of less choosy oviposition behaviour than that exhibited in laboratory tests, where alternative sites are nearby (references in Bentley & Day 1989).