Download (Diptera: Culicidae) Within the United States?

Journal of Medical Entomology, 53(5), 2016, 1002–1012
doi: 10.1093/jme/tjw046
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Advance Access Publication Date: 28 June 2016
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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
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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
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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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