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Keywords:

  • Mosquito;
  • ecology;
  • resting sites;
  • Costa Rica

ABSTRACT:

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

The resting sites of tropical American mosquitoes are poorly documented, and the few reports that do exist are largely from opportunistic collections. Since blood-engorged females (used in determining host associations) are more efficiently collected from resting sites than attractive traps, information on resting site utilization has practical value. To investigate differences in the resting sites utilized by tropical mosquitoes, we collected and identified female mosquitoes from one man-made (resting shelter) and three natural (buttress tree roots, hollow trees, and understory vegetation) resting environments at a tropical dry forest location in western Costa Rica. All of the most common species collected demonstrated associations with one or more resting environments. Females of five species (blood-engorged Anopheles albimanus, Uranotaenia apicalis, Uranotaenia lowii, Uranotaenia orthodoxa, and blood-engorged Mansonia titillans) were collected in significantly greater numbers from understory vegetation than other resting environments. Culex erraticus and other members of the subgenus Melanoconion were encountered more often in resting shelters, hollow trees, and buttress roots, while Culex restrictor (blood-engorged) females were associated with hollow trees. Similarity indices indicate that buttress tree roots, hollow trees, and resting shelters are similar with respect to the mosquito communities that utilize them as resting sites, while understory vegetation has a resting fauna that is different than the other environments surveyed here. These results add to the body of information regarding resting sites utilized by tropical American mosquitoes.


INTRODUCTION

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

Resting sites of adult mosquitoes are under-documented, yet important, components of mosquito ecology. Information on the resting sites of various mosquitoes is indispensible for studies investigating patterns of host use, since greater numbers of blood-engorged females (required for such studies) are collected from resting sites than by conventional traps (Komar et al. 1995). In Africa, resting site selection by Anopheles mosquitoes that transmit malaria (Plasmodium) parasites has been a matter of particular importance to malaria control efforts, which rely heavily upon indoor residual insecticide sprays (World Health Organization 2009). Malaria vectors differ in their preference for resting and feeding indoors (endophilic) vs outdoors (exophilic), affecting their contact with residual pesticides (Haridi 1972, Pates and Curtis 2005, White 1974). Rates of outdoor biting may increase if indoor residual sprays selectively kill indoor resting mosquitoes (Pates and Curtis 2005, White 1974), which can lead to a decrease in the effectiveness of indoor residual sprays for controlling malaria vectors (Sharma and Mehrotra 1986). Apart from practical considerations, data from resting site collections often provide a different representation of the mosquito community than do light traps, which primarily collect host-seeking females (Mullen 1971, Service 1977).

Despite its importance, little information is available concerning the resting sites utilized by different mosquito species, especially in tropical American locations. Much of the literature concerning the resting sites of tropical mosquitoes is anecdotal, and very few studies systematically compare collections from different resting environments. The current study compared natural and artificial resting sites of various types to (1) investigate resting sites utilized by Costa Rican mosquitoes and (2) evaluate artificial resting shelters as a tool for collecting an abundance and diversity of mosquitoes in a tropical American location.

MATERIALS AND METHODS

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

The study was conducted at Palo Verde Biological Station, Guanacaste, Costa Rica. The station, located within Palo Verde National Park, is in the Pacific lowlands and is characterized by deciduous tropical dry forest bordered by a large freshwater marsh and associated wetlands. All collecting sites were located within a dry forest/open rural mosaic and were within 1 km of the freshwater marsh. The site receives most rain during a six-month wet season (May-October). Tropical dry forests within Palo Verde National Park are mostly composed of trees and shrubs in the families Fabaceae, Rubiaceae, Euphorbiaceae, Anacardiaceae, and Flacourtiaceae. There is a modest component of lianas, mostly of the family Bignoniaceae. The four most common forest plant species (stems per 0.1 ha) are (in descending order): Allophyllus occidentalis, Astronium graveolens, Bauhinia glabra, and Tabebuia ochracea (Gillespie et al. 2000). The freshwater marsh is associated with the floodplain of the Rio Tempisque and is composed of a diversity of semi-aquatic herbaceous species, including the dominants Hymenachyme amplexicaulis, Neptunia natans, Nymphaea amazonum, Thalia geniculata, and the introduced Typha domingensis (Trama et al. 2009). Scattered trees within and along the edge of the marsh include Parkinsonia aculeata (Palo Verde, the namesake of the National Park), and Pithecellobium lanceolatum (Trama et al. 2009), and the cactus Acanthocereus tetragonus.

Resting female mosquitoes were collected using a hand-held, battery-powered aspirator or sweep net (Burkett-Cadena et al. 2008). Collections were made on eleven mornings (07:00 – 09:00, every four days) during the month of August, 2010. Four resting environments were sampled, including wire-frame resting shelters (Burkett-Cadena 2011), hollow trees, buttress roots, and understory vegetation. Resting shelters (six total), made of a chicken wire loop (1m long × 0.32 m dia.) inside a black plastic trash bag, were placed in shaded locations, spaced evenly (∼40 m apart) along a forest trail than ran parallel to the shoreline of the adjacent marsh (Figure 1). A modified DustBuster® portable vacuum (Meek et al. 1985) was used to aspirate mosquitoes from inside the shelters. The vegetation growing along the same trail was sampled using an insect sweep net (Bioquip Products, Rancho Dominguez, CA, U.S.A.) in 10-m swaths (six total). The collector walked briskly along the trail, swinging the sweep net through low (0.5 m or less) vegetation (mostly dense growth of the forest grass Lasiascus spp.), until the end of the swath was reached, at which point contents of the net were aspirated using a modified DustBuster®. Lasiascus spp. was quite common throughout the lowland areas but was particularly dense at the forest edge and along paths. Hollow trees were somewhat scarce and interspersed throughout the sampling area (Figure 1). Six hollow trees were sampled using the modified DustBuster®. Trees with the buttress roots, Brosium alicastrum (Moraceae), were common and found throughout the forested areas. Six trees were selected at random and sampled using the modified DustBuster®. The collector walked around each tree, aspirating mosquitoes from protected recesses between the buttress roots and trunk. Mosquitoes were returned to the laboratory, where they were freeze-killed then identified using published keys (Clarke-Gil and Darsie 1983, Darsie 1983).

image

Figure 1. Map of a portion of Palo Verde Biological Station Guanacaste, Costa Rica, with mosquito sampling stations and dominant habitat types. BT = Buttress tree (Brosium), HT = Hollow tree, RT = Resting trap, V = Vegetation sweep.

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We used general linear models (SAS PROC GLM, SAS Institute, Cary NC, U.S.A.) to test for differences among different resting environments for each of the most commonly collected mosquito species. The proportion of total females collected from each resting environment each day of sampling was used as the dependent variable. Because different volumes of each habitat were sampled in our collecting protocol, raw proportions were corrected by total numbers caught per habitat type. Proportions were arcsine transformed prior to analysis (McDonald 2009). Significant differences among groups were determined using Tukey-Kramer adjustment for multiple comparisons (alpha = 0.05). Blood-engorged and non-engorged females were analyzed separately.

We explored relationships between mosquito abundance/diversity and resting habitat utilization using species accumulation curves and proportional index of community similarity. Species accumulation curves were calculated through the program EstimateS (Colwell 2005), using the Mao Tau function (Gotelli and Colwell 2001, Mao et al. 2005). Proportional similarities, indices of similarity among communities, were calculated for the species sampled from each combination of resting environments using formulas developed by Whittaker (1952).

RESULTS

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

A total of 1,691 female mosquitoes belonging to (at least) 18 species (Table 1), were collected from resting sites at Palo Verde Biological Station, Guanacaste, Costa Rica. Culex erraticus (Dyar and Knab) and Mansonia titillans (Walker) were the most commonly collected species, representing 32.1 and 29.0 of total collections, respectively. With the exception of Cx. erraticus, members of the subgenus Melanoconion (genus Culex) could not be identified to species and were thus treated as a group. Tropical species of Melanonconion are diverse but notoriously difficult to identify (Williams and Savage 2009). Male mosquitoes were not identified nor included in the analyses.

Table 1.  Total female mosquitoes collected from four different resting environments at Palo Verde Biological Station, Guanacaste, Costa Rica. Eleven collections were made over a period of 20 days, August, 2010.
MosquitoButtress rootsVegetation sweepHollow treeResting shelter
Non-engorgedBlood engorgedNon-engorgedBlood engorgedNon-engorgedBlood engorgedNon-engorgedBlood engorged
Ae. (Och.) euplocamus 00000010
Ae. (Och.) taeniorhynchus 00100000
An. (Ano.) pseudopunctipennis 20100100
An. (Nys.) albimanus 5326142022
Cq. (Rhy.) nigricans 00011023
Cx. (Ano.) conservator 00100000
Cx. (Ano.) restrictor 521110380
Cx. (Cux.) nigripalpus 00000010
Cx. (Mel.) erraticus 1093811311730441
Cx. (Mel.) spp.144224116514737
Cx. (Neo.) derivator 00100000
Limatus durhamii 10000000
Ma. (Man.) titillans 95086272712512
Ur. (Ura.) apicalis 22823610105
Ur. (Ura.) geometricus 00100000
Ur. (Ura.) lowii 102630010
Ur. (Ura.) orthodoxa 00660000
Ur. (Ura.) socialis 00000010
Total3646723790882772890

In general, little difference was observed in resting sites utilized by blood-engorged and non-engorged mosquitoes of each species (Figure 2), with one exception. A far greater proportion of blood-fed Ma. titillans females were encountered in vegetation (90.0%), compared to non-engorged females (19%).

image

Figure 2. Resting site utilization by blood-engorged (blood-fed) and non-engorged (not blood-fed) female mosquitoes in a tropical dry forest, Guanacaste, Costa Rica, 2010. Only the most commonly encountered species are presented. Cx. (Mel.) spp. refers to undetermined species of the subgenus Melanoconion (genus Culex). Data are normalized by total mosquitoes collected per habitat type.

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Statistically speaking, each mosquito species (blood-engorged, non-engorged, or both) was collected in greater numbers from one or more resting environments. More blood-engorged females of Anopheles albimanus Wiedemann were collected from vegetation (F3,24= 8.31, P < 0.001) than other habitat types. Culex erraticus females were collected in greater numbers from resting shelters, hollow trees, and buttressed roots (blood-engorged: F3,28= 9.5, P < 0.001; non-engorged: F3,40= 35.65, P < 0.001). Other, unidentified members of the subgenus Melanoconion were collected in greater numbers from resting shelters, buttress roots, and hollow trees (blood-engorged: F3,32= 9.07, P < 0.001; non-engorged: F3,40= 10.81, P < 0.001). Non-engorged females of Cx. restrictor were collected in greater numbers from hollow trees (F3,32= 52.15, P < 0.001). Blood-engorged females of Ma. titillans were collected in greater numbers from vegetation (F3,24= 8.18, P < 0.001) over other resting environments, whereas non-engorged females were not significantly associated with any resting environment. Uranotaenia apicalis Theobald (non-engorged: F3,24= 74.82, P < 0.001), Uranotaenia lowii Theobald (blood-engorged: F3,4=∞, P < 0.001; non-engorged: F3,16= 38.61, P < 0.001), and Uranotaenia orthodoxa Dyar (blood-engorged: F3,4=∞, P < 0.001; non-engorged: F3,8=∞, P < 0.001) were collected in greater numbers from understory vegetation than other resting environments.

Accumulation curves (Figure 3) indicate that more mosquito species are likely to be encountered with additional sampling in all four resting environments, especially understory vegetation. The trajectory of the curves of buttress roots, hollow trees, and resting shelters are quite similar, despite differences in the total numbers and diversity of mosquitoes encountered in the three environments.

image

Figure 3. Accumulation curves of mosquito species sampled from four resting environments in a tropical dry forest, Guanacaste, Costa Rica, August, 2010. Species observed (Mao Tau formula) were calculated using the program EstimateS (Colwell 2005).

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The communities that rest in buttress roots, hollow trees, and resting shelters were quite similar (Figure 4), with 84.6 to 93.8% proportional similarities among samples. The mosquito communities resting in understory vegetation were most dissimilar from other resting habitats (Figure 4), with proportional similarities ranging from 34.8 to 41.4%.

image

Figure 4. Similarities among mosquito (species) communities sampled from four resting environments in a tropical dry forest, Guanacaste, Costa Rica, August, 2010. Size of arrow is proportional to the degree of similarity (value) between each resting environment.

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Aspirating from resting shelters was an effective means of sampling a fair abundance and diversity of tropical mosquitoes. Ten mosquito species were collected using this method, more than were collected from buttress roots (eight species) and hollow trees (seven species). Only vegetation sweeps (14 species) produced a greater variety of mosquito species. Resting shelter aspiration was the most productive collection method, in terms of total mosquitoes collected (Table 1). Using this method, 818 female mosquitoes were collected (728 non-engorged, 90 blood-engorged), which is 1.9, 2.5, and 7.1 times more females than collected from buttress roots, vegetation sweeps, and hollow trees, respectively.

In addition to mosquitoes, 49 female sand flies (Diptera: Psychodidae: Phlebotominae) were collected from resting sites, 46 of which (14 blood-engorged, 32 non-engorged) were from hollow trees.

DISCUSSION

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

In the first synoptic work treating the mosquito fauna of Costa Rica, Kumm et al. (1940) reported only two collections of resting adults (Table 2). Later, as part of their extensive studies on mosquitoes of Middle America, Heinemann and Belkin (1977) reported on opportunistic collections of resting adult mosquitoes throughout Costa Rica. Their 43 (sites) records of resting adults were mostly from crab holes and included specimens of nine different species (Table 2). Of the 22 species-resting site collections listed by Kumm et al. (1940) and Heinemann and Belkin (1977), only Culex nigripalpus Theobald was recovered during the current study. Previous surveys of Costa Rican mosquitoes (Kumm et al. 1940, Heinemann and Belkin 1977) were from a wider range of habitats and seasons than the current study and may explain why so few species that were reported earlier were also encountered presently. Nonetheless, the results of the current study help to further characterize the biology of the mosquitoes of this region.

Table 2.  Summary of mosquitoes (Diptera: Culicidae) collected from resting sites in Costa Rica. Data from published sources. K =Kumm et al. (1940), HB =Heinemann and Belkin (1977).
Mosquito speciesIn bromeliadIn crab holesIn cut bamboo internodeIn fallen monkey podIn a parked vehicleIn roomsIn tree holesOn leaves, stemsOn rockWater tank
Aedes           
Ae. (How.) allotecnon HB         
Ae. (How.) quadrivittatus HB         
Ae. (Och.) serratus  HB        
Ae. (Och.) taeniorhynchus      HB    
Culex           
Cx. (And.) conservator       HB   
Cx. (Car.) secundus    HB      
Cx. (Cux.) corniger         HB 
Cx. (Cux.) inflictus (group) HB        
Cx. (Cux.) nigripalpus  HB     K  
Cx. (Cux.) quinquefasciatus     HBHB    
Cx. (Lut.) allostigma          K
Cx. (Mel.) spp.HBHB        
Cx. (Tin.) latisquama       HB   
Deinocerites           
De. costaricensis  HB        
De. epitedeus  HB        
De. nicoyae  HB        
De. pseudes  HB   HBHB   
Haemagogus (Hag.) chalcospilans       HB   
Psorophora           
Ps. (Jan.) albipes      HB    
Ps. (Jan.) ferox  HB        
Trichoprosopon (Trc.) digitatum   HB    HB  
Wyeomyia (Wyo.) pertinans (group)HB         

Reports of mosquito resting sites from neighboring countries allow us to compare our results to those from other tropical American locations. In El Salvador, Breeland (1972) encountered An. albimanus adults in greatest numbers in crevices and holes in rock walls and lava flows, while relatively few An. albimanus adults were found resting among tree roots, trunks, and hollow trees. In the current study, relatively few An. albimanus adults were found resting among buttress roots, and within hollow trees, affirming the findings of Breeland (1972) in this respect. However, nearly two-thirds (73.7% blood-engorged, 74.3% non-engorged) of An. albimanus females were collected from understory vegetation sweeps in the current study. Because Breeland (1972) did not include vegetation sweeps among his sampling techniques, and since rock walls and lava flows were not sampled in the current study, it is difficult to reconcile the differences between Breeland's findings and our own. In Guatemala, Cupp et al. (1986) found that Ma. titillans rested among high grasses around trees in fields. Our results partially support the findings of Cupp et al. (1986) in that 84% (corrected) of blood-engorged Ma. titillans females were collected in vegetation sweeps. However, non-blood-fed females were fairly evenly distributed among the four environments (Figure 2). Since Ma. titillans females were quite actively biting during collecting times (Burkett-Cadena, unpublished observations), it is likely that non-engorged females of Ma. titillans were not resting but were actively host-seeking and therefore randomly distributed in the environment as they searched for suitable hosts. Culex erraticus females were found most commonly in resting shelters, hollow trees, and among buttress roots. Combined, >99% (corrected data) of Cx. erraticus females were collected from these three resting environments. Results from studies in the southern U.S.A. found that Cx. erraticus females prefer artificial resting shelters and large tree cavities (Burkett-Cadena et al. 2008), generally supporting the results from this more tropical locale. Few records can be found concerning the preferred resting environments of Uranotaenia spp. from the American tropics. Pratt (1946) reported copulating adults of Ur. lowii resting among floating Lemna plants in Puerto Rico but provided no further observations. Therefore, our observations that Uranotaenia spp. females rest in understory vegetation, relative to all other resting environments, is an important contribution to our understanding of this group.

Proportional similarity indices suggest that buttress roots, hollow trees, and resting shelters are somewhat redundant as sampling sites for collecting resting mosquitoes. Since resting shelters had the greatest abundance and diversity of mosquitoes among these three resting environments, it is defensible to promote resting shelters as a reproducible means of collecting the mosquitoes that would naturally rest inside hollow trees and buttress roots. Furthermore, an optimal, yet efficient strategy for collecting the widest diversity and greatest abundance of resting mosquitoes would employ aspirating resting traps and vegetation sweeps. Although it is possible that the mosquito females sweep-netted from understory vegetation were not resting, but actually were flying within or hovering over the vegetation, this method of collection yielded species that were not regularly collected from buttress roots, hollow trees, or resting shelters. Collections from these two environments captured 17 of the 18 total species encountered, and 1,145 of the 1,691 total females collected (67.7%). The only mosquito species not collected by these two methods was a Limatus durhamii Theobald (a single female aspirated from buttress roots).

Despite the limited sampling in our study, we demonstrate that the mosquito species/groups are not evenly distributed among types of resting sites and that the mosquito communities vary among the different resting environments. Since several of the species included in this study are important vectors of human pathogens (An. albimanus (Warren et al. 1975), Cx. erraticus (Cupp et al. 2003), and Ma. titillans (Turell et al. 2000) this information may be useful for vector management applications. Studies of mosquito host preference can also benefit from this information, since large numbers of field-collected, blood-fed females are needed for such studies, and blood-fed females usually make up only a fraction of females collected using conventional methods, particularly light traps (Komar et al. 1995).

Acknowledgments

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

We thank Mahmood Sasa (Director) and other personnel of Palo Verde Biological Station for logistical support. This research was conducted under RESOLUCIÓN No 018-2009-ACAT (MINAET, Ministry of Environment, Energy and Telecommunications) while conducting research funded by the NSF IRES grant to the Organization for Tropical Studies.

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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