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Journal of Medical Entomology, 53(5), 2016, 1002–1012 doi: 10.1093/jme/tjw046 Forum Advance Access Publication Date: 28 June 2016 Forum What Can Larval Ecology Tell Us About the Success of Aedes albopictus (Diptera: Culicidae) Within the United States? Donald A. Yee Department of Biological Sciences, University of Southern Mississippi, Hattiesburg, MS, 39460, Corresponding author, e-mail: [email protected] Received 23 January 2016; Accepted 17 March 2016 Abstract Aedes albopictus (Skuse) was introduced in the United States approximately 30 years ago, and since has become an important pest and vector of disease. This species uses small water-holding containers as sites for oviposition and larval development. Larvae can consume a wide range of detritus-based energy sources, including microorganisms, and as such the type and quantity of detritus that enters these systems have been studied for the effects on adult populations. This review examines the documented responses of Ae. albopictus to different larval environments within the United States, and some of its unique ecology that may lead to a better understanding of its spread and success. Field surveys generally find larvae in shaded containers with high amounts of organic detritus. Larvae have higher survival and population growth under high amounts of detritus and microorganisms, but they also can outcompete other species when nutrients are limiting. Allocation of time to feeding by larvae is greater and more focused compared with resident species. These latter two points also may explain differences in carbon and nitrogen composition (nutrient stoichiometry), which point to a lower need for nitrogen. Combined, these facts suggest that the Ae. albopictus is a species with a relatively wide niche that had been able to exploit container habitats in the United States better than resident species. After 30 yr of research, only a narrow range of detritus types and environmental conditions have been examined. Data on factors affecting the production of adults and its spread and apparent success are still needed. Key words: Aedes albopictus, container, carbon, detritus, feeding, nitrogen The Asian tiger mosquito, Aedes albopictus (Skuse), has been a widespread pest species for most of the 30 years it has been in the eastern United States (Yee 2016). During that time, as it extended its distribution from the initial entrance point near Galveston, Texas (Sprenger and Wuithiranyagool 1986), it has experienced a wide range of environments, from the tropical and semi-tropical locations in the south along the Gulf Coast and southern Florida, to temperate locations in the north stretching from southern New York west to Iowa (Rochlin et al. 2013, Kraemer et al. 2015). Along this wide eastern swath of the continent, larvae have been exposed to variation in detrital input based on the local plant and animal communities, experienced different microorganism communities, and have been affected by different temperatures and water chemistry values that have likely produced variation in local population sizes and temporal dynamics. This review summarizes how Ae. albopictus has responded to the different larval nutrient environments within the United States, and some of its unique larval ecology that may lead to a better understanding of its success in eastern North America. Herein, I show that larval resource environments in the United States generally have been conducive for Ae. albopictus establishment, that their feeding behavior allows for superior exploitation of container nutrients compared with many resident and other invasive species, and that their tolerances to low-nutrient environments may be a central factor explaining their establishment in the United States. Together, these attributes are helpful in understanding the success of this species in the United States. Although I have restricted my examination of the published literature to those studies emphasizing Ae. albopictus in the United States, some works that examined the general biology and life history from other continents also were included. Moreover, although other factors such as human density, container type, and adult behavior are known to affect populations of Ae. albopictus (Yee et al. 2010, 2015a), the focus of this review was on the influence of resources. Herein, I use the inclusive term “nutrients” in reference to the abiotic material (e.g., dissolved organic nutrients, fine and course particulate detritus, organic molecules) ingested by larvae that allows them to complete development, whereas I use “microorganisms” (including bacteria, protozoan, fungi) as the biotic portion of these same environments. I use the term “resources” to include both nutrients and microorganisms. I caution that even though environments in the United States C The Authors 2016. Published by Oxford University Press on behalf of Entomological Society of America. V All rights reserved. For Permissions, please email: [email protected] 1002 Journal of Medical Entomology, 2016, Vol. 53, No. 5 may be novel compared with other locations, it is difficult to know what ramifications there are for these differences without comparative data on populations elsewhere. The arrival of Ae. albopictus in the United States coincided with declines in the abundance of a well-established container species, Aedes aegypti (L.) (Yee 2016). This pattern is exactly opposite of one that was found in Asia during the 20th century, where Ae. aegypti populations underwent range expansion into locations where Ae. albopictus populations were declining (reviewed in Hawley 1988). The mechanism for displacement in Asia has many hypotheses, although under one scenario, niche differences between the species and concomitant changes in habitat features caused by humans may have changed the relative availability of those niches (Hawley 1988). Specifically, increased urbanization aided the more peridomestic Ae. aegypti, while at the same time, reductions of forest or rural habitats, which are favored by Ae. albopictus, disappeared. Thus, one might ask if a similar niche shift could explain the expansion of Ae. albopictus and the decline of Ae. aegypti in the United States. The answer to that is unknown, given the lack of details on the pre- and post-Ae. albopictus introduction niches for Ae. aegypti. However, given how rapidly Ae. albopictus spread in the United States, it appears unlikely that dramatic changes in the niche spaces for these species occurred. More likely is the possibility that Ae. albopictus was able to occupy otherwise underexploited niche space upon arrival to the United States, that Ae. albopictus was able to outcompete Ae. aegypti in otherwise marginal niche space for Ae. aegypti (Juliano 1998), or both. I have chosen to examine evidence for these hypotheses via the larval ecology of Ae. albopictus in the United States, especially as it relates to the use of habitats under different nutrient environments. The exact nature of the interactions between Ae. albopictus and Ae. aegypti will be discussed elsewhere in this set of papers (Fader 2016); however, how Ae. albopictus has responded to the nutrient environments in the United States may offer some evidence for its successful establishment. The material for this review was amassed from the published literature on Ae. albopictus within the United States. Because there are few studies specifically investigating the sole effect(s) of detritus on aspects of larval growth or survival, I included studies that focused on factors such as temperature, photoperiod, and geographic variation on life-history traits to understand responses to a wider set of nutrient sources. Reviews of species interactions between Ae. albopictus and other resident mosquito species do include some details of resource types used in those experiments (Juliano 2009, 2010); however, the goal of those reviews was not to examine performance (e.g., growth, adult size, survival) on different resources per se, but instead focused on the outcomes of those interactions. Therefore, in this review, I specifically examined the types of resources used in the assessment of both laboratory and field investigations of Ae. albopictus in the United States. Even if only one type of resource was investigated and the focus of the work was on something besides resources, the outcomes of the study when examined within the context of other work could still assist in understanding how nutrients affect Ae. albopictus. Nutrient Environments Aedes albopictus is a container specialist that has its origins in eastern Asia (Hawley et al. 1987). Adult females select small, often dark, water-holding containers in which to lay their eggs (Hawley 1988, Yap et al. 1995). Man-made containers include tires (Yee 2008), cemetery vases (Vezzani 2007), and down spout extensions (Unlu et al. 2014), whereas natural containers include tree holes 1003 (Hawley 1988). In the United States, Ae. albopictus is the most common species found in tires in the southeast (Yee 2008). Eggs are laid singly above the water line or, in limited instances, directly on the water surface (Hawley 1988, Rey and O’Connell 2014). This former habit takes advantage of future environmental conditions, as eggs won’t hatch until a precipitation event has occurred and rising water levels cover the eggs, thus maximizing the time for larval development. Once eggs hatch, larvae in containers primarily feed on heterotrophic microorganisms and nutrients (Merritt et al 1992, see the role of algae, below). Growth of larvae as well as the phenotypic characteristics of adults, such as body size, are affected by the quality and quantity of these food sources. Several studies within the United States have correlated the abundance of Ae. albopictus larvae with aspects of the resource environments in field containers. In surveys of tires from six sites among four counties in spring and summer in Illinois, Yee et al. (2010) found that abundance of Ae. albopictus larvae was correlated with the presence of detritus (leaf, seed, and fine detritus in spring; seeds in summer). Bacterial productivity (production of new bacterial cells hr-1) was important for larval presence in summer, but not in spring. Using a similar approach in Mississippi, Yee et al. (2015a) examined tires in six counties during spring and summer. Abundance of Ae. albopictus larvae was predicted by detritus amounts, here responding to pine needles and reproductive parts (seeds, fruits). In both of these studies, Ae. albopictus larvae were often found in tires associated with low human densities (Yee et al. 2010, 2015a), which is consistent with its preference for more rural habitats (Hawley 1988). Murrell et al. (2011) surveyed cemetery vases across Florida to understand dynamics between detritus, fine particulate organic matter, dissolved nutrients (carbon, nitrogen, phosphorus, CNP), and the abundance of Ae. albopictus and Ae. aegypti. They found that the relative abundance of both species relied on inputs of detritus and the resulting CNP environment, and concluded that nutrients and detritus in general contributed to the distributions of these species across the state (Murrell et al. 2011). In surveys of five tree hole and six tire sites in and around Washington, DC (Maryland), in late summer and fall, Freed and Leisnham (2014) found that Ae. albopictus abundance was positively related to detritus amounts and to total nitrogen concentrations; container volume also affected abundance. Moreover, they found the abundance of Ae. albopictus to be significantly higher in tires compared with tree holes. Although these authors did not sort detritus by type, the consistent effect of detritus seen in their work in conjunction with other studies provided strong evidence of the importance of allochthonous energy inputs in explaining Ae. albopictus population distributions. Moreover, these studies span >10 of latitude and encompass a wide variety of detritus types, suggesting that Ae. albopictus are capable of successfully utilizing almost any detrital environment across its current U.S. range. Yee et al. (2012a) also compared container types and detrital composition and found Ae. albopictus larvae to be 48 times more abundant in tires compared with tree holes during both survey times. This fact was consistent with the finding that Ae. albopictus was more susceptible to predation by Toxorhynchites rutilus (Coquillett) compared with some native species (Kesavaraju and Juliano 2004), and that tree holes harbored more of this predator than other systems (Yee et al. 2012b, Freed and Leisnham 2014). It also provided evidence for the influence of detritus type and amount in affecting populations of Ae. albopictus in containers, but suggested that container type was not in and of itself an impediment to success. Besides field evaluations of how natural inputs of detritus affect Ae. albopictus populations, there are 39 published papers that 1004 experimentally evaluated how resource variation affects the biology and ecology of Ae. albopictus in the United States (Table 1). The majority (n ¼ 25) of these used some sort of leaf litter as one resource base, and of those, most (n ¼ 17) used a species of oak (Quercus sp.), often live oak (n ¼ 9, Quercus virginiana Miller). Maple (n ¼ 4) and elm (n ¼ 4) leaves were the next most common types used. Dead invertebrates were used as an energy base in 10 studies, whereas 19 studies included an artificial diet source (Table 1). For animal diets, almost all used dead tropical house crickets (Gryllodes sigillatus Walker), pomace flies (Drosophila melanogaster Meigen), or both. For artificial diets, high protein sources like dried ground mammalian liver power or albumin power were used. The rationale for using many of these detritus types was based on either known detrital patterns in the field (Kesavaraju et al. 2014) or were used to isolate other factors of interest (e.g., interspecific density; Juliano 1998). As mentioned, there have been broader examinations of the effect of detritus on Ae. albopictus competitive interactions with other species (Juliano 2010); however, the emphasis on effects of different detritus types on Ae. albopictus performance has not been reviewed. In a subset of the studies mentioned earlier (Table 1), authors compared the effect of different types or different ratios of detritus on performance (e.g., survival, growth, development time, population growth) of Ae. albopictus. The data generally support higher overall performance for Ae. albopictus in animal- versus plant-derived diets (Daugherty et al. 2000, Yee et al. 2007a, Murrell and Juliano 2008, Winters and Yee 2012, Bara et al. 2014,Yee and Skiff 2014, Yee et al. 2015b); however, Barrera (1996) found that Ae. albopictus survived longer when grown on leaves versus an artificial diet of bovine liver powder and yeast. Animal detritus seems to support greater microorganism populations and productivity (Yee and Juliano 2006, Murrell and Juliano 2008) and may provide greater amounts of limiting nutrients (e.g., nitrogen) compared with some leaf types. Animal detritus may also be more readily available for feeding compared with leaves, as it decomposes faster and could therefore be directly ingested by larvae (Yee and Juliano 2006, Yee et al. 2007b). Even though Ae. albopictus appears to do better on animal-based diets, it is quite capable of using a wide range of detritus types, and generally shows positive population growth under a suite of single and mixed diets (Yee et al. 2007a, Murrell and Juliano 2008). Growth and development of Ae. albopictus are affected by different leaf types under laboratory situations (Table 1). For example, Costanzo et al. (2011) investigated the effect of ratios of leaves of American elm (Ulmus americana L.) and giant foxtail grass (Setaria faberi Hermm.) on Ae. albopictus success (and in competition with Culex pipiens L.). Generally, population growth estimates were positive, but declined as less grass was added to elm leaves. Elm leaves decompose slower compared with grass (Murrell and Juliano 2008), and grass may supplement nutrients to an otherwise poor nutrient environment. In a study meant to examine resource environments in the far northern limit of Ae. albopictus in the United States, leaves of common persimmon (Diospyros virginiana L.) led to lower survival and longer development times for Ae. albopictus compared with American elm, red oak (Quercus rubra L.), or maple (Acer sp.) (Kesavaraju et al. 2009). Resikind et al. (2009) examined the effect of four leaf species on aspects of growth and oviposition of Ae. albopictus from southern Florida. Adults had greater survival, were larger, and had shorter development times when grown using leaves of Boston fern (Nephrolepis exaltata Schott) and live oak (Quercus virginiana) compared with grape (Vitis aestivalis Michaux) or wild coffee (Psychotria nervosa) (Resikind et al. 2009). Leaf mixtures Journal of Medical Entomology, 2016, Vol. 53, No. 5 produced differences in population growth estimates, with those mixtures containing live oak, Boston fern, or a mixture of those and others appearing to promote greater mosquito population growth. One explanation for the differences in performance in Ae. albopictus across leaf types is secondary plant compounds, like tannins, which may be higher in some lead species and which are known to negatively affect the performance (e.g., size, growth rates) of Ae. albopictus and other mosquito species (Rey et al. 1999). Tannins have been identified as a critical factor explaining larval performance on different leaf types. Specifically, Murrell and Juliano (2008) found tannin concentrations greatest in live oak leaves, which showed lower larval survival and population growth compared with other lower tannin-producing leaf types (e.g., grass). Kesavaraju et al. (2009) hypothesized that higher concentrations of tannins in common persimmon could have inhibited larvae development compared with other leaf types. It should be noted that Resikind et al. (2009) used fresh leaves, a fact that could have affected the composition and concentration of secondary plant compounds. To date, most examinations of leaves in Ae. albopictus habitats have used senescent leaves, as this is the most common way for leaves to enter containers. From these various studies, it appears that Ae. albopictus can tolerate and, in some cases, thrive under vastly different detrital environments. This may point to a relatively large niche breadth for this species, which could be the mechanism for its invasion across the United States, where it has encountered substantial variation in habitats and thus detrital types. Niche shifts based on models between the native range and the North American populations have been identified for Ae. albopictus in the United States and elsewhere (Medley 2010); however, we lack strong empirical evidence to document this shift. Moreover, although animal detritus and leaves were studied extensively, the relatively narrow range of detrital environments that have been explored for Ae. albopictus in the United States is striking, given the myriad of detritus types that enter containers in the field, with many including flowers, pollen, twigs, bark, seeds, and many other leaf genera having never been examined under controlled experiments. Assessing the response of Ae. albopictus to a greater range of detritus types could provide additional evidence about the niche of this species, a finding that would help explain its successful invasion. Larval Microorganism Food Sources Mosquito larvae consume fine detritus, dissolved organic nutrients, and microorganisms, with the latter types consisting of a complex food web of bacteria, fungi, and protozoans (Walker et al. 1991, Merritt et al. 1992). There have been few investigations into the effects of specific microorganism groups on Ae. albopictus in the United States; however, there have been investigations for other container taxa. As discussed above, detritus type and amount can affect the performance of Ae. albopictus; however, larvae benefit from the combined contributions of nutrients from the consumption of detritus and microorganisms. Specifically, adults were smaller and females took longer to develop when microorganisms were reduced via flushing compared with no flushing situations (Yee et al. 2007c). Microorganism productivity generally correlates with high-quality detritus environments and has had significant positive effects on Ae. albopictus growth and survival (Yee et al. 2007a, c; Murrell and Juliano 2008). Bacteria specifically have been shown to be predictive of Ae. albopictus populations in tires in Illinois (Yee et al. 2010) and Mississippi (Yee et al. 2015a); however, Yee et al. (2012a) found Live oak American elm, Ulmus americana Slippery elm, Ulmus rubra Foxtail grass, Setaria sp. American elm Pin oak, Quercus palustris Live oak, grass, Zoysia sp. Slash pine, Pinus elliotti Tuchman et al. 2003 Yee et al. 2004a Costanzo et al. 2005 Murrell and Juliano 2012 Costanzo et al. 2011 Resikind et al. 2009 Leisnham et al. 2009 Kesavaraju et al. 2009 Murrell and Juliano 2008 Crickets, Gryllodes sigillatus þ Drosophila sp. D. melanogaster Drosophila melanogaster Animals Live oak American elm Red oak, Quercus rubra Norway maple, Acer platanoides American persimmon, Diospyrios virgiana Summer grape, Vitis aestivalis, live oak, wild coffee, Psychotria nervosa, Boston fern, Nephrolepis exaltata American elm, Giant foxtail grass, Setaria faberi White oak, Quercus alba Crickets Trembling aspen, Populus tremuloides Lounibos et al. 2002 Teng and Apperson 2000 Yee et al. 2007a Armistead et al. 2008 Live oak Quercus sp. Juliano 1998 Comiskey et al. 1999 Daugherty et al. 2000 Leaves Nutrient source Live oak, Quercus virginiana Live oak Hackberry, Celtis sp. Live oak Barrera 1996 Citation Tree hole water – Stem flow Tire water Albumin:yeast: rabbit chow Bovine liver powder: yeast Other Lab Lab Lab Lab Lab Lab Field Lab Lab Lab Lab Lab Field Lab Lab Lab Venue Florida Illinois Florida Florida, Illinois New Jersey Florida Illinois Virginia Florida Illinois Florida North Carolina Florida Louisiana Florida, Illinois Florida Location Cx. pipiens Ae. triseriatus Ae. aegypti – Ae. aegypti Ae. triseriatus Ae. japonicus Ae. aegypti Culex pipiens – Ae. aegypti Ae. triseriatus Aedes aegypti – Ae. aegypti – Interacting species 25 25 28 28 25 28 27 18.8 "Room temp."Not specified 25 25 24, 30 15, 23, 31 Ambient 27 27 24.5–25.5 Temp ( C) 14:10 16:8 14:10 14:10 16:8 14:10 14:10 Natural 14:10 16:8 12:12 16:8 Natural 16:8 16:8 14:10 Photoperiod (L:D) (continued) Ae. albopictus lab strain used Exp. 1 only Notes Table 1. Summary of specific nutrient environments and localities examined for effects on various measures of performance of Aedes albopictus within the United States since its introduction in 1985 Journal of Medical Entomology, 2016, Vol. 53, No. 5 1005 Shumard oak, Quercus shumardii White oak White oak Red maple, Acer rubrum White oak Red maple Bara et al. 2014 Freed and Leisnham 2014 Kesavaraju et al. 2014 Yee and Skiff 2014 Smith et al. 2015 Yee et al. 2015b Yee et al. 2007c Black et al. 1989 Walsh et al. 2012 Leisnham et al 2011 Alto et al. 2008 Bevins 2007b Bevins 2007a Briegel and Timmermann 2001 Juliano et al. 2004 Novak et al. 1993 Livdahl and Willey 1991 Ho et al. 1989 Red maple Live oak Leaves Nutrient source Winters and Yee 2012 Allgood and Yee 2014 Citation Table 1. continued Crickets D. melanogaster Crickets D. melanogaster Crickets þ Drosophila sp. Dead pupae/ larvae Animals Uncontrolled natural inputs Bovine liver powder Bovine liver powder Oak infusions, albumin:yeast Bovine liver powder Uncontrolled natural inputs Porcine liver powder Fish food Field Lab Lab Lab Florida, Illinois, Missouri North Carolina Florida Field Lab Louisiana Illinois Louisiana Texas Maryland Florida Florida Louisiana, Texas New Jersey, Maryland, Virginia Mississippi Maryland Kentucky Florida Mississippi Location Lab Lab Lab Lab Lab Lab Lab Lab Lab Lab Lab Lab Bovine liver powder Yeast:wheat Lab germ:baby Field cereal Tire and tree hole Lab water Other Venue – – Ae. aegypti Ae. triseriatus Ae. triseriatus – – Ae. triseriatus Ae. triseriatus Ae. aegypti Ae. triseriatus Ae. triseriatus – – – Cx. coronator Ae. sierrensis Ae. j. japonicus Ae. aegypti Ae. triseriatus, Cx. pipiens – Cx. quinquefasciatus Interacting species 16:8 16:8 10:14 14:10 12:12 14:10 Not specified 12:12 14:10 14:10 14:10 12:12 14:10 Photoperiod (L:D) Ambient 21 28 24 24 Ambient Natural 12:12, 15:9 14:10 16:8 16:8 Natural 12, 17, 27, 32 14:10 27 22 24–25 26 20 27 26 27 26 26 28–30 20 27 Temp ( C) (continued) Lab strains used Lab strains used Lab strains used Ae. triseriatus from Massachusetts Ae. triseriatus from Illinois Cx. coronator from Florida Ae. aegypti from Florida Ae. j. japonicus lab strain Ae. sierrensis from Utah Cx. pipiens from Illinois Notes 1006 Journal of Medical Entomology, 2016, Vol. 53, No. 5 Leaves Venue references the location where the work was conducted, but Location is where the detritus or Ae. albopictus populations originated unless noted. A colon between artificial diets under Other Nutrient Sources designates a ratio of diets (often 1:1). In cases of fluctuating temperatures, only means are presented. For specifics, see individual citations. 27 20 Ae. aegypti – Florida Mississippi Lacalbumin:yeast Lacalbumin:yeast Yee et al. 2014 Skiff and Yee 2015 Lab Lab Lacalbumin:yeast Yee et al. 2012b Citation Table 1. continued Nutrient source Animals Other Lab Venue Location Florida, New – Jersey, Virginia, North Carolina Interacting species 20 Temp ( C) Photoperiod (L:D) 10 hrs, 28 min:13 hrs 32 min and 13 hrs 49 min: 9 hrs 11 min 12:12 12:12 Notes Journal of Medical Entomology, 2016, Vol. 53, No. 5 1007 that bacterial productivity was significantly lower in tires in Mississippi (where Ae. albopictus populations were higher) compared with tree holes. A comparison of bronze versus nonbronze cemetery vases in Florida found that the former container type harbored higher bacterial abundance than the latter (Walker et al. 1996), suggesting a role for container type in affecting microorganism communities. Examination of bacterial communities in nature has revealed a complex community of potential food sources for Ae. albopictus. Using 16 S rDNA fragments, Ponnusamy et al. (2010) quantified bacterial communities in several container types (including tires, tree holes, and cemetery vases) in New Orleans, Louisiana. Their analysis identified known species within major bacterial groups (Alpha-, Beta-, and Gammaproteobacteria, and Actinobacteria, Bacteroidetes, Cyanobacteria, and Firmicutes) along with many unknown species. Some of these groups have been identified from other container habitats in the United States (Kaufman et al. 1999). From the perspective of Ae. albopictus, it was noteworthy that bacteria in tires exhibited a more consistent community structure compared with tree holes, although how certain types of containers structure bacterial communities or how bacterial communities influence the production of mosquitoes remains unknown. At present, the role of any single bacterial species or group of species on Ae. albopictus populations is unexplored. Aquatic fungi also are a critical source of energy for larvae developing in containers (Kaufman et al. 2001). However, in environments with leaves, fungi may be difficult for larvae to extricate from within the leaf tissue, and thus, most fungi remain unexploited by larvae (Kaufman et al. 2001). Container mosquitoes may rely on bacteria for energy for maintenance, whereas fungi and protozoan may be more important for growth (Kaufman et al. 2002). In fact, it has been suggested that Aedes triseriatus (Say) cannot meet their carbon demands when feeding on bacteria alone, making fungal tissue a potentially important source of micronutrients (Kaufman et al. 2001). No studies have investigated the role of fungi for production of Ae. albopictus, although Yee et al. (2012a) measured both fungal production and biomass (via the amount and rate of ergosterol and [1-14C]-acetate incorporation into ergosterol) in tires and tree holes in Mississippi. No significant differences in fungi were identified either between seasons or between container types; however, the data precluded directly relating the abundance of Ae. albopictus and measures of fungal production or biomass. The last major aquatic group of heterotrophic microorganisms in containers are the protozoans, which themselves represent a wide variety of trophic positions, including predators (Yee et al. 2010). Tires harbor at least three dozen species of protozoans (Yee et al. 2010, 2012a, 2015a) and they appear to be affected by the collective feeding of container inhabitants (Yee et al. 2007c). An assessment of the direct effects of protozoans from containers on Ae. albopictus larvae failed to find a significant role for these microorganisms in growth or survival of larvae (Skiff and Yee 2015). However, as mentioned for fungi, protozoans may be important for sequestering specific nutrients that are not available from other microorganism or detritus itself (Kaufman et al. 2001). Thus, although protozoans are prevalent in Ae. albopictus containers, they do not appear to have a direct role in growth or survival of Ae. albopictus. The indirect role of protozoans in providing specific nutrients has yet to be answered. Algae, which is the only form of autochthonous energy in containers, has been measured in several studies in containers. Generally, there appears to be weak or absent effects of algae on growth rate or population sizes of container species (Kling et al. 2007, Lorenz et al. 2013) and Ae. albopictus specifically (Yee et al. 1008 2015a). A negative relationship was found between Ae. albopictus and algae in summer in tires from Illinois (Yee et al. 2015a). Marten (1986) found that pure cultures of algae would support growth and development of Ae. albopictus in Hawaii (this study preceded the introduction of Ae. albopictus into the mainland United States); however, it is not clear if the algae species used are common in containers. In addition, larvae died when they were fed individually on more than a dozen species of green and blue-green algae; death occurred largely owing to starvation (Marten 1986). Additions of yeast could allow larvae to complete development, implying low digestibility but nontoxicity for some algae (Marten 1986). Thus, the role of algae in supporting Ae. albopictus is unclear, but seems minor compared with other heterotrophic microorganism groups. Microorganisms are an important component of the container food web (Kaufman et al. 2001, Ponnusamy et al. 2010), Ae. albopictus larvae exhibit delayed growth under reduced microorganism communities (Yee et al. 2007c), and larval survival can be predicted by microorganism productivity (Yee et al 2010, 2015a; Murrell et al. 2011). However, the importance of certain microorganisms in directly affecting survival and population growth of Ae. albopictus appears limited, and thus, these groups don’t appear to be an integral part of the successful establishment and spread of Ae. albopictus. Larval Foraging Ecology Mosquito larvae consume both dead and living organic material (Merritt et al. 1992). Larvae rely on different forms of heterotrophic microorganisms (i.e., bacteria, fungi, protozoans), whose own energy comes from organic nutrients (Walker et al. 1988). These microorganisms grow on surfaces and float suspended within the water column (Merritt et al. 1992, Clements 1999), making understanding where and how larvae feed important for larval success. Larval feeding behavior is also important, as it both defines intra- and interspecific differences in species and can be an important tool to understand adult production. Larval feeding is categorized based on how species obtain their nutrients. Historically, categories of feeding include filtering, browsing, and predation (Surtees 1966), with more refined categories including collecting-gathering, collecting-filtering, scraping, shredding, and predation (Merritt et al. 1992, Clements 1999). Browsing, in which larvae make contact with a surface and remove microorganisms with their mouth parts, is common among container Aedes, whereas filtering, which involves rapid movement of mouthparts to remove microorganisms from the water column, is more common among Culex and Anopheles (Dahl et al. 1988); feeding behavior is not rigid and may vary with food type availability (Yee et al. 2004b). Thus, because it is so closely linked to production, the topic of larval feeding ecology has been studied extensively (reviewed in Merritt et al. 1992), including for Ae. albopictus. Aedes albopictus larvae feed using typical browsing and filtering behavioral modes, but often focus on browsing on surfaces when available (Yee et al. 2004b, Kesavaraju et al. 2007, O’Donnell and Armbruster 2007, Skiff and Yee 2014), especially when high-quality detritus types are offered (Kesavaraju et al. 2007). Specifically, when high-quality animal detritus was offered in conjunction with a similar-sized elm leaf segment, Ae. albopictus spent more time browsing on the animal detritus compared with another container species, Ae. triseriatus (Kesavaraju et al. 2007). As animal detritus led to faster larval development and to higher survival compared with leaves (Kesavaraju et al. 2007), Ae. albopictus larvae exhibit foraging behaviors that best exploit high-quality food types and a Journal of Medical Entomology, 2016, Vol. 53, No. 5 preference for those same food types. Obviously under food-limited conditions, which results in competition among larvae, feeding directly on available food and concentrating that activity on the bestquality food would be advantageous. Thus, it has been hypothesized that this behavior is precisely what could aid Ae. albopictus in its documented superior competitive ability over many resident container species in the United States (Yee et al. 2004b, Kesavaraju et al. 2007). Aedes albopictus does not appear to spend more time foraging compared with Aedes japonicus, a newly invasive species from Japan (Kaufman and Fonseca 2014). Specifically, O’Donnell and Armbruster (2007) examined foraging behavior of these two species across six food environments consisting of both liquid and solid forms. They found that Ae. j. japonicus showed greater foraging activity, especially under higher nutritive situations. The fact that Ae. j. japonicus is the weaker competitor, at least under the laboratory studies conducted thus far (reviewed in Kaufman and Fonseca 2014), seems to suggest that foraging behavior alone is insufficient to help explain the dominance of Ae. albopictus in containers in the United States. However, as has been noted, there are limited examinations of competition between Ae. j. japonicus and Ae. albopictus, they have used a narrow set of detrital environments, and most have used the same laboratory strain of Ae. j. japonicus (Kaufman and Fonseca 2014). Thus, these methodological shortcomings offer the need for a broader examination for how feeding behavior of these two invasives influences competitive interactions. Regardless of such shortcomings, it does appear that Ae. albopictus does forage in a more efficient way than resident species (e.g., Ae. triseriatus), and this foraging behavior plays a notable role in its success within containers. Moreover, because how larvae feed affects adult production based on the resource environment, it also has a notable role in helping to explain the successful invasion and expansion of this species in the United States. Nutrient Stoichiometry and Stable Isotopes The links among various ecological parameters, like nutrient inputs, microorganism communities, and larval performance, are often tested using a correlative approach, because it is difficult to find a common currency under which all linkages can be assessed equally. Thus, one might ask, “Are there any methods that could assist in understanding the direct links among resources, larvae, and adult populations?” A nutrient stoichiometry approach, where elements like nitrogen and carbon are measured both within the food and the consumer, has the potential to lead to a more complete understanding of mosquito ecology in general, and the success of Ae. albopictus specifically. As elements such as carbon cannot be created nor destroyed, they are simply recycled among the dead and living portions of food webs. After allochthonous detritus enters a container, it breaks down via the action of microorganisms and is transformed into new microorganism cells and waste products, which are then ingested by foraging larvae. Thus, an analysis of mosquito elemental composition and variation (i.e., stoichiometry) can inform not only of differences among species, but also where those elements come from (Kaufman et al. 2010, Winters and Yee 2012, Yee et al. 2015b). Besides stoichiometry, which deals specifically with nutrient composition and allocation patterns of elements like carbon, phosphorus, and nitrogen, stable isotopes, which use the rarer isotopic forms of common biological elements to assess diet and tropic position, also have the potential to lead to a deeper understanding of insect and mosquito ecology (Hood-Nowotny and Knols 2007). Stable isotopes can be used for both understanding natural variation in isotopes and in enrichment studies to assess movement of elements Journal of Medical Entomology, 2016, Vol. 53, No. 5 among resources and consumers (Hood-Nowotny and Knols 2007). Both stoichiometry and stable isotope analyses of mosquitoes are only now becoming an area of interest, and at present, there are a limited number of studies using either approach (Kaufman et al. 2010, Hood-Nowotny 2012, Winters and Yee 2012, Gilbreadth 2013, Young et al. 2014, Yee et al. 2015b), with only two published studies involving Ae. albopictus (Winters and Yee 2012, Yee et al. 2015b). Different types of detritus produce differences in the stoichiometry and isotopic signatures of container mosquitoes (Kaufman et al. 2010), including Ae. albopictus. Winters and Yee (2012) grew larval Ae. albopictus under different ratios of red maple (Acer rubrum L.) and Drosophila melanogaster in the lab. Adults had higher percent body carbon (61%) under animal detritus compared with leaves (45%), with body nitrogen showing the opposite response (8% N in pure animal, 11% in pure plant). Based on mixing models, which can assess the source(s) of specific nutrients, animal detritus was a higher source of mosquito body biomass carbon (69%) and nitrogen (67%) compared with leaf sources. The values for carbon and nitrogen are very similar to a more recent study by Yee et al. (2015) that separately compared the stoichiometry of males and females of three container species, including Ae. albopictus. Body carbon was 47% (mean of males and females) and nitrogen was 9.8% in pure plant for Ae. albopictus. Like Winters and Yee (2012), these relative amounts were reversed in pure animal, with carbon 55% and nitrogen 7%. Thus, both studies suggest that body nutrients can be altered in adult mosquitoes based on exposure to different detrital sources as larvae. Aedes albopictus also has showed higher carbon and nitrogen (C:N ratio) values that produce larger adults (Winters and Yee 2012), likely reflecting an increase in lipid and carbohydrate storage compounds (Fagan et al. 2002), compounds that would only increase after metabolic and development needs were met. Taken together, the ability to reach minimal protein (nitrogen) requirements and accumulate more carbon reserves (lipids) than other species may help explain A. albopictus’ advantage over others in the larval stage, especially under nutrient-limited scenarios. In addition to whole-body nutrient stoichiometry, both studies showed that male and female adults were larger and developed faster when given animal (lower body N, higher body C) versus plant detritus (higher body N, lower body C), and survival was generally higher under mixed detritus ratios. These nutrient environments clearly have ramifications for ecological interactions, as Juliano (2010) has pointed out that detritus from deciduous or coniferous trees led to competitive dominance of Ae. albopictus compared with resident species in the United States, whereas coexistence was more likely with those residents when detritus included animal material, yeast, or grass, the latter of which were deemed high-quality. At present, we lack knowledge of the natural variation in elements for adult Ae. albopictus from field containers, or a complete understanding of the detrital, and therefore the nutrient environment in nature. The superior competitive ability of Ae. albopictus may be reflective of the fact that its body nitrogen content is generally at the low end for insects in general and for other mosquitoes specifically (Fagan et al. 2002, Peck and Walton 2006). Variation in C, N, and P among some Ae. albopictus containers is documented (Murrell et al. 2011); however, these data have not been linked to the nutrient composition of adults, nor have any studies linked variation in stoichiometry to components of adult success (e.g., longevity) or the ability to transmit disease (e.g., vector competence). As elements are the basis for both structural components (e.g., chitin) and biological processes (e.g., metabolism), these seem 1009 like logical next steps for the use of stoichiometry in understanding the success of Ae. albopictus and other species. Besides examinations of body nutrient stoichiometry, stable isotope analysis may lead to some mechanistic understanding for how Ae. albopictus may gain a competitive advantage over other container species, specifically Culex. Values of d15N (the difference in the 15N isotope form compared with the more common 14N form) are higher in Ae. albopictus compared with Culex restuans Theobald (Winters and Yee 2012) and Culex quinquefasciatus Say (Yee et al. 2015b) under all detritus ratios tested. This suggests that although Ae. albopictus has a lower percentage of nitrogen in its tissue, it is obtaining it more efficiently compared with the other species (more enriched in detritus-derived N). This enhanced efficiency may come from either acquisition (pre-ingestion) or assimilation (post-ingestion), or both. As mentioned previously, the fact that Ae. albopictus feeds more and is drawn to higher-quality food sources (Yee et al. 2004a, Kesavaraju et al. 2007) seems to make the case for pre-ingestion mechanisms, although post-ingestion mechanisms, like gut clearance times and nutrient uptake pathways, have not been explored in this species. Collectively, these findings mentioned above suggest that Ae. albopictus is more efficient at obtaining nutrients required to complete development (Winters and Yee 2012, Yee et al. 2015b). Future Directions There have been numerous studies examining food environments for Ae. albopictus in the United States; however, the majority of these studies come from a small number of locations, especially Florida and Illinois (Table 1). This generally reflects the extremes of this species distribution (and the location of prominent Ae. albopictus researchers); however, it may not accurately reflect resource environments in other parts of its range. In addition, only one study has examined the resource environments from the far western part of the United States (Kesavaraju et al. 2014), perhaps owing to the lower occurrence of this species there. The resources used in that study were white oak, Quercus alba L., a species common in the western United States (Kesavaraju et al. 2014), but generally not studied elsewhere (Murrell and Juliano 2012, Freed and Leisnham 2014). Thus, as Ae. albopictus continues to spread, especially in western states like California, the lack of knowledge of how unique local detrital environments affect population dynamics hampers predictions about how this species will perform in these novel environments. The detritus types used in experiments also represent a narrow set of possibilities (Table 1). Even though field assessments of some containers have shown plant detritus, especially leaves, to be the dominant form (Lounibos et al. 1992, Kling et al. 2007), other forms or detritus, like flowers, are known to have significant effects on container mosquito production (Lounibos et al. 1993) and patterns of nutrients in tissue (Kaufman et al. 2010). Moreover, like plants, only a relatively narrow range of dead insects have been used for examinations of the effects of animal detritus (Table 1). Given the high diversity of insects and noninsects (especially spiders) in nature, the examination of nutrient content from these other forms of energy seems warranted. If there is a niche-based explanation for the successful invasion of Ae. albopictus in the United States (Hawley 1988, Juliano 1998), then a more complete picture of how this species responds to detrital environments will be required across its current and future range. The food web of container systems is complex, but because of methodological difficulties, the complete role of the heterotrophic 1010 microorganisms in affecting populations of Ae. albopictus, or any container mosquito, remains elusive. It is clear that bacteria can play a central role in the success of Ae. albopictus, either via providing food directly or assisting in the breakdown of detritus (Yee et al. 2007c). However, fungi and protozoans, both of which potentially provide unique nutrients to larvae growth, have received less attention than bacteria. Future studies involving how attributes of Ae. albopictus larvae are affected by changes in microorganism communities, especially changes in gut physiology responses, digestion rates, and how they may affect assimilation of nutrients, are especially needed. The establishment of Ae. albopictus in the United States has produced shifts in the communities of vectors in containers, including the widespread extinctions of Ae. aegypti and possible reductions of other residents. With its ability to consume a wide variety of detritus types and the nutrients and microorganisms that emanate from them, its feeding niche seems wider than most resident species, and this may be a major factor in its successful invasion. The research over the past 30 yr has narrowly focused on some, but not all, resource environments that Ae. albopictus has experienced. Studies in the future should concentrate on resource environments across the current and future range of this species, to both identify its current tolerances as well as the potential for spread under a changing climate. Acknowledgments I thank the many authors who provided summaries for this special feature, without whose generous time and participation this special feature could literally not have been possible. I thank an anonymous reviewer for constructive suggestions to an earlier draft of this manuscript. I also thank William Reisen for his enthusiasm, input, and patience with respect to this special feature. 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