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Keywords:

  • Aedes albopictus;
  • Juniperus virginiana;
  • Oklahoma;
  • density dependence;
  • container habitats

ABSTRACT:

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Invasive plants are common and may provide resources through litter for container mosquito larvae. Invasive plant reproductive parts can make up a substantial part of litter but have mostly been ignored as a resource for mosquito larvae. We hypothesized that the reproductive fruits of the invasive eastern red cedar, Juniperus virginiana, provide high quality resources for the invasive, container mosquito Aedes albopictus at the western margin of its invasive range in North America. To test this hypothesis, we performed two laboratory experiments. The first examined the response of individual larvae of Ae. albopictus to different amounts of J. virginiana leaf (fresh and senesced) and J. virginiana fruit (ripe and unripe), as well as to a control leaf (Quercus virginiana, live oak). The second experiment examined the response of different densities of Ae. albopictus larvae to each litter type. We found significant differences in response by individual larvae to different amounts of litter and litter types. We also found J. virginiana litter components could support positive population growth rates as a function of initial larval density where the control leaf could not. We conclude that invasive plants may provide high quality resources, and that the reproductive parts (fruits, flowers, cones) may be an important and overlooked component in provisioning larval habitats. Therefore, the expansion of J. virginiana into grassland areas may contribute to the expansion of Ae. albopictus westward in North America.


INTRODUCTION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Competition in mosquito larvae for resources is well known, particularly from mosquitoes that use natural or artificial containers for larval development (Juliano 2009). Consequently, resources that provide higher nutrients can alleviate competition and result in higher mosquito populations. The majority of resources that provision container habitats is, at least by weight, plant derived (Kitching 2001, Yee et al. 2007a, Kaufman et al. 2010). There have been many studies on the role of plant material as a resource for larval mosquitoes, and most have used senesced leaves as the resource. Although senesced leaf material makes up the largest proportion of litter fall in most forests over the course of a year, plant reproductive parts may make up a total of 5% of biomass and can contribute a large percentage of litter for short periods of time depending on location (Bray and Gorham 1964). For example, in maple forests, reproductive fruits and flowers can make up to 34% of biomass (Pregitzer and Burton 1991), and fruits and flowers can be an important part of oak litter fall in Florida where, for short periods of time, flowers or fruits can make up the majority of litter fall (Lounibos et al. 1992).

Plant reproductive parts may be particularly important for container dwelling larval mosquitoes for several reasons. First, as noted, most studies focus on senesced leaves, the majority of which are dropped in the fall in temperate regions. Fall is not a productive period for mosquitoes, and if those senesced leaves get wet, they may not provide a high enough quality resource for larvae to develop the following spring or summer due to leaching (Pelz-Stelinski et al. 2010). Although plant reproductive parts do not make up a large percentage of overall plant litter biomass (Bray and Gorham 1964), flowers are often produced in the temperate spring and summer, and dehisce during periods of time when mosquito larvae are potentially abundant. Likewise, plant fruits may also be produced and dispersed during periods of high mosquito activity (e.g., summer). In spite of this, plant reproductive parts as a resource for larval mosquitoes have not been well described. Lounibos et al. (1993) found oak flowers to be a high quality larval resource for Aedes triseriatus and Kaufman et al. (2010) used stable isotopes to conclude that beech flowers were a major food stuff for Ae. triseriatus in Michigan. Barrera et al. (2006) found flowers and fruit to be linked with higher mosquito production in suburban environments in Puerto Rico and Yee et al. (2010) suggested seeds and fruits may explain differences in composition and abundance of larval mosquito assemblages in discarded tires in Illinois. However, there has not been scientific inquiry into the role of plant fruits as a resource for container mosquitoes.

Invasive plants can provide high quality resources for container mosquitoes through their leaves (Reiskind et al. 2010). They also input fruit and flowers into container habitats (Reiskind et al. 2010), although the importance of invasive fruits and flowers in aquatic environments has not been studied. Highly dispersive and abundant fruits are a characteristic of invasive plants (van Kleunen et al. 2010), suggesting that the reproductive parts of invasive plants may be an important input into aquatic environments, including container habitats.

Juniperus virginiana is a native tree species in the eastern United States that has become invasive, expanding westward into former grassland areas, from Texas to North Dakota (DeSantis et al. 2010). Invasion of grasslands by J. virginiana has consequences on plant and animal communities and abiotic conditions, resulting in declines in plant biodiversity, a shift in bird communities from grassland birds to eastern woodland birds, and increases in humidity and soil moisture (Briggs et al. 2002, Horncastle et al. 2005, Linneman and Palmer 2006, Pierce and Reich 2010). There may also be consequences for mosquitoes in this region. In particular, the areas being invaded by J. virginiana are on the western edge of the invasive range of the Asian tiger mosquito, Aedes albopictus (Darsie and Ward 2005, Benedict et al. 2007). Some of these changes may directly affect adult Aedes albopictus by providing different, or greater or fewer blood hosts (e.g., different bird or mammal species) and conditions conducive to longer survival (e.g., higher humidity). In addition, if components of J. virginiana litter provide a high quality input to container habitats, this plant invasion may help the westward expansion of Ae. albopictus by providing both high quality adult and larval environments.

To determine the importance of invasive plant reproductive parts as a resource for container dwelling larvae, we hypothesized that the fruit of J. virginiana provides a good resource for larvae of the invasive mosquito Aedes albopictus. To test this, we performed two experiments. The first experiment examined the response of individual mosquito larvae in the absence of competition to green and senesced leaves and fruits of the invasive tree Juniperus viriginiana. The second experiment examined how these leaf litters affected intraspecific competition within cohorts of Ae. albopictus larvae at different initial densities.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Leaf litter

We conducted a preliminary survey of the components of leaf litter in five suburban sites in Stillwater, OK, by placing two tarps (152.4 cm × 243.8 cm) at each site. All litter that accumulated on these tarps from August 21–28, 2008 was brought back to the lab, partitioned to lowest possible taxonomic level and type (leaf, woody tissue, flower or fruit), dried at 50° C for 72 h, and weighed. All plant material was saved to be used in larval growth experiments. As a comparison to previous laboratory studies (Alto et al. 2008, Reiskind et al. 2009), live oak leaves, collected as litter fall from Vero Beach, FL in 2007 and kept dried, was also used in the larval growth experiments.

Mosquitoes

All mosquitoes used in this study were F1 mosquitoes from field populations collected in Tulsa, OK, during the summer of 2009 in conjunction with the Tulsa Department of Health. We collected, hatched, and reared over 3,000 F0 eggs in a nutrient broth containing 0.3 g of 1:1 yeast:albumin. We identified Ae. albopictus as pupae and then confirmed their identification at the adult stage to make the colony, kept at 95% RH, 26° C with a 14:10 L:D photoperiod. We fed this colony human blood from a volunteer (Oklahoma State University, Institutional Review Board exemption 8/25 /2008) to produce the F1 eggs used in the experiments.

Individual responses to components of cedar leaf litter

We measured the survival and growth of individual larvae in response to different components of cedar leaf litter. Using 50 ml conical tubes (VWR International, West Chester, PA), we placed 0.1 or 0.2 g of five types of leaf material (green J. virginiana leaf, senesced J. virginiana leaf, unripe J. virginiana fruit, ripe J. virginiana fruit, and live oak leaves) in each tube with 35 ml of tap water. Therefore, we created ten treatments (two amounts × five leaf types). We replicated each treatment 12 times, for a total of 120 replicates. We hatched F1 eggs in distilled water 36 h prior to the start of the experiment. A single, 1st instar larvae was added to each tube the same day. Tubes were kept under controlled conditions (26° C 14:10 L:D) in an incubator. We monitored the growth of these larvae, and we recorded the time from hatching to pupation, emergence, and death. Upon emergence, each mosquito was allowed to live for at least 24 h, and then killed in the drying oven for at least 48 h. We sexed and weighed each mosquito using an ultra micro balance (Sartorius MP 3 balance, Data Weighing Systems, Inc. Elk Grove, IL). We only present data for female mosquitoes as the patterns of males and females were similar, and females are more critical in determining the population level effects of these nutrients.

Cohort responses to components of cedar leaf litter

We also assessed the effects of variation in leaf litter type with varying densities of mosquito larvae to determine whether the differences in individual response would have an effect on the productivity of mosquitoes under more natural, competitive conditions. We used the same leaf types as in the previous experiment (green leaf, senesced leaf, green fruit, ripe fruit, and oak leaf), at 1 g in 250 ml of tap water in 500 ml food grade, plastic containers (Newspring Industrial Corporation, Kearney, NJ). As opposed to varying the amount of food, we varied the density of 1st instar mosquitoes in each container: 10, 20, or 30 1st instar containers, for a total of 15 treatments (three densities by five leaf types). We replicated each treatment seven times. These densities and leaf amounts were chosen based upon field data and previous experiments (O'Meara et al. 1995, Reiskind et al. 2010). Containers were kept under controlled conditions (26° C, 14:10 L:D photoperiod) in an incubator. We checked containers daily for pupation. We removed pupae from each container and treated them as in the previous experiment. We collected total survival (male and female), average weight, average days to emergence, and average wing length data for each replicate.

Statistical analysis

As we could not reject the null hypothesis of normality using Shapiro-Wilk's test for normality (Sokal and Rohlf 1995) for our outcomes of survival, days to emergence, weight, or wing length, we concluded our data were normally distributed and used a generalized linear model (PROC GLM, SAS 9.2, SAS Inc., Cary, NC). We measured multiple outcomes (time to emergence and adult weight) on replicates, therefore we analyzed the individual data with a multivariate analysis of variance model (MANOVA). This approach allowed us to examine correlations between the outcome variables and gain a better understanding of how leaf type or amount affected all outcomes simultaneously (Scheiner and Gurevitch 2001). In addition, the MANOVA approach has become common practice among studies of mosquito larval response and allows meaningful comparisons across studies with different larval environmental factors or different species (Alto et al. 2005, Yee et al. 2007a,b, Alto et al. 2008, Reiskind and Wilson 2008, Juliano 2009, Reiskind et al. 2009). After significant MANOVA, we performed a priori planned contrasts to determine the differences among cedar litter type (fruit or leaf) and among cedar litter condition (fresh or senesced) for time to emergence and final weight.

For the cohort study, we focused on an aggregate measurement of population performance, the estimated finite rate of increase, λ′. Following Juliano (1998), we determined λ′ for each replicated cohort using the following equation:

  • image

where N0 is the initial number of females in a cohort (assumed to be half of the larvae added), Ax is the number of females emerging on day x, wx is a measure of mean female size on day x, f(wx) is a function relating fecundity to female size, and D is the time required, in days, for a female to mate. This measurement has been commonly employed in experiments with container mosquitoes (Juliano 1998), and we used the equations and parameters for Ae. albopictus fecundity described in Lounibos et al. (2002). A λ′ above 1 estimates a positive population growth, while a λ′ of less than 1 suggests population decline under those given conditions. As this outcome was not normally distributed by Shapiro-Wilk's test for normality, and no transformations helped normalize λ′, we used a distribution free randomization ANOVA to determine the significance of litter type and density using the program RT using 5,000 randomizations (Manly 1998). After a significant full model, we ran pair-wise comparisons using the same randomization ANOVA under the same conditions to determine differences between fruit and leaf of J. virginiana and between senesced and fresh material. We have data on survival, growth rate, and final adult size for each individual in the cohort study, and these data are available as supplemental data from the corresponding author upon request but are not shown in the interest of space.

RESULTS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Leaf litter survey

We found cedar (Juniperus viriginiana) litter made up a large proportion of leaf litter in late summer (Figure 1). Cedar litter collected from this preliminary survey was more green leaf (35.14%) than senesced leaf (11.94%), and more ripe fruits (29.64%) than green fruits (23.29%). Other plant material was primarily leaves, although Carya illinoisensis, Lagerstroemia indica, and Magnolia grandifolia all contributed flowers or seeds to the collected litter.

image

Figure 1. Summed plant litter biomass (fruits, flowers, woody tissue, and leaves) from five litter collecting sites in suburban Stillwater, OK. Abbreviations: Juvi: Juniperus virginiana; Unid: unidentifiable (includes most woody tissue); Magr: Magnolia grandifolia; Cail: Carya illinoisensis; Qupa: Quercus palustris; Lain: Lagerstroemia indica; Quma: Quercus marylandica; Ploc: Planus occidentalis; Ulam: Ulmus americanum; Ulru: Ulmus rubra; Ceoc: Celtis occidentalis; Casp: Catalpa speciosa.; Visp: Vitus spp.; Busp: Buxus spp.. Total dry weight of each category is given above each bar. Weight is given on a log10 scale for visualization purposes.

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Individual responses

Individual female larvae showed significant differences in both growth rate and total growth between plant materials depending upon the amount of material provided (Table 1 and Figure 2). Increased plant material increased the final weight across all leaf treatments, and reduced development time in live oak, but had little effect on development time when provisioned with components of J. virginiana litter. Different plant material also significantly affected growth. Larvae reared with J. virginiana material grew bigger at both leaf amounts compared to live oak leaves. Ignoring the oak control, larvae provided with senesced material were not significantly different in final weight or rate of development than those with green material (leaves and fruits)(GLM: time to emergence: F1,48= 1.82 p=0.1853; weight: GLM, F1,48= 0.34 p=0.5620). Larvae provided fruits (green or ripe) grew heavier than those given leaf material (green or senesced) (GLM: weight: F1,48= 7.91 p<0.01) but did not develop significantly faster (GLM: time to emergence: F1,48= 0.23 p=0.6340).

Table 1.  Results of the MANOVA of individual female larval responses to different components of Juniperus viginiana litter (green leaf, green fruit, ripe fruit, and senesced leaf) and live oak at two amounts (0.1 and 0.2 g).
     Standardized Canonical Coefficients
SourcePillai's traceDF (num,den)F-valuePvalueWeightTime to Emerge
Leaf0.6138,965.30<0.00011.4830.0242
Amount0.37232,4713.94<0.00011.352–0.481
Leaf* Amount error0.30738,962.180.0355–0.3061.137
image

Figure 2. A) Centroids for female mosquitoes of average time to emergence and average dry weight reared in five different leaf treatments (green fruit, ripe fruit, green leaf, sensesced leaf of Juniperus virginiana and oak) at 0.2 g of material. Error bars are +/-1 standard error of the mean. Legend applies to panels A and B. B) Centroids for female mosquitoes of average time to emergence and average dry weight reared in five different leaf treatments (green fruit, ripe fruit, green leaf, sensesced leaf of Juniperus virginiana, and oak) at 0.1 g of material. Error bars are +/- 1 standard error of the mean.

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Cohort responses

Estimated finite rate of increase of Ae. albopictus grown on all types of J. virginiana litter and oak leaves showed a decline with increasing initial larval density (Table 2 and Figure 3). At all densities, populations of Ae. albopictus were estimated to grow faster on any type of J. virginiana litter than live oak leaves. In general, these mosquitoes performed well on J. virginiana fruit, with positive population growth (λ’ > 1) at all densities on both ripe and green fruits. Indeed, populations of larvae performed better on fruit than on leaf material from J. virginiana (randomization ANOVA, fruit vs leaf material: F1= 3.93, p<0.0002). Likewise, there was an average λ’ above one for all densities when given senesced leaf, while the average λ’ for green leaf at the highest density estimates population decline, and senesced leaf material resulted in a significantly higher λ’ (randomization ANOVA, green vs senesced leaf: F1=2.02, p<0.05). At high and medium density for oak leaves there was an average estimated finite rate of increase of less than one, or negative population growth.

Table 2.  Results of a randomization ANOVA on the estimated finite rate of increase.
SourceDFF-valuep-value
Leaf416.210.0002
Density29.420.0002
Leaf* Density83.960.0014
Error90..
image

Figure 3. Average λ’ estimates for each litter type at high (30 larvae), medium (20 larvae), and low (ten larvae) initial larval densities. Point estimates are given above each bar. Error bars are +/- 1 standard error of the mean.

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DISCUSSION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Our results suggest that the reproductive parts of invasive plants are important in providing nutrients for mosquito larvae. Our leaf survey suggested that the invasive species Juniperus virginiana may be a significant contributor of plant material into container habitats in suburban environments in Oklahoma, and that fruits and leaves, senesced and green, likely get into aquatic, container environments used by Ae. albopictus. Our litter survey was not comprehensive in either geographic or temporal extent, and should not necessarily be extended to all locations in Oklahoma. Nevertheless, numerous other studies have shown J. virginiana to be a common and effective invader of grasslands, and it can be a dominant producer of litter in some areas (Coppedge et al. 2007, DeSantis et al. 2010). The preponderance of both fresh leaf and fruit in the J. virginiana material was surprising, as plants usually shed senesced leaves or ripe fruit. We did observe squirrels (Scirius carolinensis) eating green stems of J. virginiana twigs and discarding the green leaves and fruits (Reiskind, unpublished data), which may explain their large mass in our sample. The green components of leaf litter may therefore only be found when squirrels are actively foraging on cedar.

The individual response study demonstrated that J. virginiana leaf litter can provide a good resource for mosquito larvae, especially the fruits. The pattern of response at different amounts of leaf material is curious. Increasing the amount of material for all the J. virginiana litter types increased the final weight of each mosquito but also increased development time. This was different than the response to oak leaves, in which increased amounts increased weight and decreased development time, a pattern of outcomes that has been associated with better population performance through changes in initial larval density (Braks et al. 2004, Juliano 2009). The effects of increased J. virginiana litter is consistent with other studies comparing a diversity of leaf species in which final size varies between leaf species in a consistent way, but development time does not vary consistently (Sota 1993, Reiskind et al. 2009, Reiskind et al. 2010). This response to different amounts of leaf material, or different leaf species, is also different than the general response to variation in larval density (higher density equals longer development time and smaller adults) on a single resource (Juliano 2009). Other studies comparing leaf species have noted a consistent effect similar to changes in initial larval density, in which one leaf species results in quicker development and larger adults than a comparative species (Fish and Carpenter 1982, Dieng et al. 2002, Yee and Juliano 2006). Our results, taken in light of these other studies, suggest that increasing the amount or changing the type of leaf resource (whether that means different plant species or different components of the litterfall is not the same as decreasing initial larval density.

The cohort study demonstrated that the different components of J. virginiana litter could support high mosquito population growth, relative to the live oak control. More interestingly, the various components of that litter differed, with J. virginiana fruits outperforming leaf material. Although the differences were relatively small, even at high initial larval density, the exponential nature of the rate of increase means that small differences in the estimated finite rate of increase can represent big differences in population trajectory. As fruits made up a majority, by dry weight, of the J. virginiana leaf litter, the importance of plant fruits as a resource may be greater than previously considered in the scientific literature.

There are a plethora of studies focused on leaf material as a resource base for container mosquitoes, but very little on the reproductive parts of plants. The fruits and flowers of plants may be particularly important as a resource for mosquito larvae due to their high nutrient quality, as demonstrated by this and other studies (Lounibos et al. 1993, Barrera et al. 2006, Kaufman et al. 2010) and their propitious phenology, generally dehiscing in spring or summer (flowers) or summer or early fall (fruits). Furthermore, the presence of fruits or seeds may also contribute to differences in oviposition and habitat use, with concomitant epidemiological consequences, and may lead to higher populations of container mosquitoes.

Acknowledgments

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

The authors thank Talan Klein for assistance in the laboratory, Dr. George Opit and Dr. Carmen Greenwood for reading earlier versions of this manuscript, and two anonymous reviewers. This work was funded by the Oklahoma Agricultural Experiment Station (Oklahoma Hatch Project #2702 and Multistate Project NE-1014, Project #2712).

REFERENCES CITED

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED
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