Oviposition habitat selection by container-dwelling mosquitoes: responses to cues of larval and detritus abundances in the field.

Insects’ oviposition responses to resource and larval densities can be important factors determining distributions and competitive interactions of larvae. Aedes albopictus (Skuse) and Aedes aegypti (L.) (Diptera: Culicidae) show aggregated distributions of larvae in the field, larval interactions that are affected by detritus resources, and oviposition responses to resource and density cues in the laboratory. We conducted field experiments testing whether these species choose oviposition sites in response to chemical cues indicating detritus resource quantity and quality or larval abundances. In experiment 1, both species showed interactive responses to water conditioned with high or low quantities of senescent live oak leaves and density combinations of A. albopictus and A. aegypti larvae. Aedes aegypti preferred high-detritus containers when conspecifics were absent. Aedes albopictus tended to prefer high-detritus containers when larval density was low. We found no evidence of interspecific differences in oviposition preferences. In experiment 2, A. albopictus preferred high detritus over low or no detritus, and rapidly-decaying, high-quality detritus over low-quality detritus. Oviposition choices by these Aedes are mainly determined by resource quantity and quality, with larval densities having minor, variable effects. Oviposition responses of these species are unlikely to lead to resource partitioning. Aggregated distributions of these species in the field are unlikely to be products of oviposition choices based on larval densities. Keywords: oviposition choice, resource abundance, larval density, Aedes aegypti, Aedes albopictus, aggregation, resource partitioning Introduction Habitat selection theory predicts that organisms will disperse and colonize habitats in a way that maximizes expected fitness (Resetarits 1996, Binckley & Resetarits 2005, 2008, Resetarits & Binckley 2009). For species that provide no parental care to offspring deposited in discrete patches, selection on the ability to discriminate favorable and unfavorable patches should be particularly strong because offspring are confined to a patch until some developmental milestone is reached (Resetarits & Wilbur 1989). In many patchy-systems such as Drosophila-colonized fruits and mushrooms (e.g., Atkinson 1985) and aquatic container communities (e.g., Juliano 1998), resource competition within a patch is important and may be a significant source of larval mortality, hence female oviposition decisions should minimize the future experience of competition by her larvae. Container-dwelling mosquitoes seem particularly capable of responding to volatile chemical cues that may reflect current or future intensity of larval competition. For example, the presence of con- and heterospecific competitors (Zahiri et al. 1997, Edgerly et al. 1999) or the quantity and type of resources present in a container (Ponnusamy et al. 2008, Reiskind et al. 2009) can influence oviposition choices in these systems. Aedes aegypti and Aedes albopictus are container-dwelling mosquitoes that inhabit human-dominated landscapes throughout the world. Both are competent vectors of multiple arboviruses and thus their reproductive and oviposition behaviours have received much attention (e.g., Sucharit et al. 1980, Allan & Kline 1998, Sharma et al. 2008). Aedes aegypti responds to cues from eggs and larvae of both conspecifics and heterospecifics, including A. albopictus (Zahiri et al. 1997, Allan & Kline 1998). Behavioural assays often test the response of gravid females to water conditioned by larvae or eggs although specific chemical cues have also been isolated and assayed in oviposition trials (Zahiri et al. 1997, Ganesan et al. 2006, Seenivasagan et al. 2009). Aedes aegypti females respond positively to chemical cues derived from well-fed and healthy larvae, but may be repelled by chemical cues from larvae at very high densities or from starved larvae (Zahiri et al. 1997, Allan & Kline 1998, Zahiri & Rau 1998, Seenivasagan et al. 2009). Cues indicating resource availability in a container also elicit oviposition responses from these species. Chemical cues associated with microorganisms from decaying organic matter elicit positive oviposition responses from both A. albopictus (Trexler et al. 2003) and A. aegypti (Benzon & Apperson 1988, Ponnusamy et al. 2008). Reiskind et al. (2009) reported oviposition preference of A. albopictus for containers with oak leaves over containers with grape leaves or plain water. In larval competition experiments oak leaves are a superior resource compared to grape leaves, suggesting that A. albopictus selects oviposition sites that will reduce larval competition and maximize expected fitness (Reiskind et al. 2009). These observations suggest that ovipositing container-dwelling Aedes accurately respond to container conditions, including larval density and resources, as predicted by habitat selection theory. However, most studies have tested oviposition behaviour in the laboratory, under carefully controlled conditions. For example, oviposition assays have been conducted on multi-well plates with water volumes of only a few ml, and water treatments separated by several centimeters or less (Zahiri et al. 1997). Others have used electroantennogram techniques and Y-maze olfactometers to assess the mechanisms eliciting attraction to cues (i.e., behavioural orientation vs. stimulation to oviposit; Seenivasagan et al. 2009). These are effective methods for understanding the proximate causes of these behaviours and the range and strength of responses that can be expected in these species. These studies, as well as a select few field studies (e.g., Trexler et al. 1998), have been largely motivated by the goal of developing attractants or repellents for mosquito control and monitoring, important goals given the human health importance of these species. However, relatively little is known about the importance of such chemical cues in the presence of natural variability, and how they might influence distributions of mosquito eggs across oviposition sites and resulting ecological interactions among larvae. The strong and species-specific responses observed in laboratory experiments may be important drivers of species distributions in wild populations, particularly as they affect densities of individuals relative to local resource availability, and spatial variation of competitive interactions. Understanding responses to these cues in the field and their potential for affecting actual distributions of species, is the goal of this paper. Aedes albopictus and A. aegypti coexist in some areas of the southern United States (O’Meara et al. 1995) despite competitive asymmetry usually favoring A. albopictus (Juliano 1998, 2009, 2010). A leading hypothesis to account for this pattern is condition-specific competition which suggests that the outcome of competition depends on the conditions within larval containers (Juliano 2009, 2010). For example the abundance of rapidly decaying detritus releases A. aegypti from interspecific resource competition with A. albopictus (Daugherty et al. 2000, Murrell & Juliano 2008, Juliano 2010, O’Neal & Juliano 2013). Based on the oviposition experiments discussed above, one hypothesis for coexistence of these species postulates that A. aegypti females select container habitats with higher levels of high-quality resources, stabilizing coexistence via resource partitioning (Shorrocks & Sevenster 1995, Adler et al. 2007). This hypothesis predicts that the two species will show different oviposition responses to detritus resource quantity and quality in the field, and negative correlations of egg numbers. Another coexistence hypothesis in this system is the ‘aggregation model’ of coexistence (Atkinson 1985, Ives 1991) that postulates that intraspecifically aggregated or clumped distributions of larvae among containers will increase intraspecific competition relative to interspecific competition, facilitating coexistence (Ives 1991, Shorrocks & Sevenster 1995, Fader & Juliano 2013). This hypothesis predicts that one or both species preferentially oviposit in containers containing conspecifics in the field. Both A. aegypti and A. albopictus preferentially oviposit in laboratory containers with conspecific larvae or eggs (Allan & Kline 1998) and if this behaviour is prevalent in nature this would directly increase intraspecific aggregation in the field and the likelihood of coexistence (Ives 1991). Aggregated spatial distributions of these species have been observed in the field suggesting aggregation may affect interspecific competition and coexistence (Leisnham & Juliano 2009, Fader & Juliano 2013). These predictions center on oviposition behaviour in response to ecologically realistic cues from detritus or conspecifics at relevant spatial scales in the field. In this paper we describe two experiments testing these hypotheses about oviposition responses of naturally-occurring A. albopictus and A. aegypti females to larval abundance and detritus resource quantity and quality cues at levels likely to be encountered in nature.