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Mycologia, 96(6), 2004, pp. 1233-1235.
© 2004 by The Mycological Society of America

Temporal distribution of Smittium culisetae in a wild population of Wyeomyia smithii from pitcher plants


W.K. Reeves 1

     Department of Entomology, Soils and Plant Sciences, 114 Long Hall, Clemson University, Clemson, South Carolina 29634

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

The fungus Smittium culisetae is a trichomycete that develops in the hindguts of larval aquatic Diptera. This is the first report of S. culisetae from the pitcher plant mosquito, Wyeomyia smithii. Larvae of the mosquito were collected from the purple pitcher plant, Sarracenia purpurea, from a bog in Jackson County, North Carolina. The lowest proportions of colonized larvae occurred in December, January and July. The greatest proportions of colonized larvae occurred in October and March. The distribution of colonized larvae among pitchers did not differ significantly from a random distribution.

Key words: Diptera, Culicidae, endosymbiotes, Harpellales, Sarracenia purpurea, Trichomycetes


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Trichomycetes are obligate fungal endosymbionts that live in the alimentary tracts of arthropods. Species of Smittium (Harpellales) often colonize the hindguts of mosquito larvae (Culicidae) (Misra and Lichtwardt 2000Go). Potential mosquito hosts are found in a wide range of habitats including artificial containers, tree holes, rock pools, lakes and ponds, puddles and the margins of rivers and streams. Even mosquitoes in ephemeral habitats, such as the water retaining leaves and flowers of plants, are colonized by trichomycetes (Lichtwardt 1994Go). Trichomycetes are transmitted from larva to larva by direct consumption of trichospores shed in contaminated feces (Lichtwardt 1986Go). Neither mosquito larvae nor available habitats are randomly distributed in the environment. Both host populations and the external environment probably influence the distributions of Smittium species. If the horizontal transmission of Smittium species between larvae is not random, then the mosquito lar vae with trichomycetes should be clumped in distribution and in seasonality.

To test this hypothesis I needed a mosquito with a relatively long-lived larval stage that allows for horizontal transmission and a restricted larval habitat that does not allow larvae to migrate between sites. The pitcher plant mosquito, Wyeomyia smithii (Coquillett), is an ideal experimental organism to examine the distribution of Smittium in wild mosquitoes. Wyeomyia smithii is the only mosquito known to develop in the pitchers of the purple pitcher plant, Sarracenia purpurea L. (Miller et al 1994Go, Nastase et al 1995Go). Female mosquitoes oviposit directly on the water surface in a pitcher (Nastase et al 1995Go). Neither the pitcher plant fluid nor the larvae can move between pitchers. The discovery of S. culiseta Lichtwardt in a wild population of W. smithii allowed examination of occurrence, distribution and seasonality of this harpellid species. The larval development of W. smithii, which can last for months (Bradshaw et al 1998Go), would permit horizontal transmission between mosquitoes in the individual pitchers.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
On each collection date larvae of W. smithii were collected with a 50 mL pipette from all pitchers of S. purpurea in a randomly chosen 2 m2 plot at Bullpen Bog, Jackson County, North Carolina, United States, (35.0313°N, 83.0638°W). The contents of each pitcher were stored alive in independent vials for 1 h and transported to the laboratory. All Wyeomia larvae were dissected on microscope slides in distilled water, and their hindguts were removed and examined with a compound microscope at 400x using phase contrast microscopy. The number of colonized and uncolonized larvae in each pitcher was recorded. Larvae were collected on 28 Jun, 3 Jul, 14 Aug, 15 Nov, and 10 Dec 2001; 4 and 31 Oct 2002; and 3 Jan, 19 Feb, 17 Mar and 21 May 2003.

The hindguts of Metriocnemus knabi (Coquillett) (Diptera: Chironomidae) also were examined to determine if this sympatric midge is a reservoir host for trichomycetes. Fifty larvae of M. knabi from different dates were dissected during the course of the experiment.

The proportions of colonized larvae and pitchers with uncolonized larvae were tested statistically to determine if significant differences existed between collection dates. A Monte Carlo simulation was used to determine whether the proportion of colonized larvae on each date was statistically different from what was expected if larvae were drawn from pools of all collected larvae. A Chi-square test was used to determine if the proportion of pitchers with colonized larvae deviated from the expected proportion of colonizations.

A culture of S. culisetae was deposited in the USDA-ARS Collection of Entomopathogenic Fungal Cultures in Ithaca, New York. Voucher specimens of W. smithii were deposited in the Clemson University Arthropod Collection.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Smittium culisetae was found in the hindguts of W. smithii but not in M. knabi, indicating the specificity of S. culisetae to mosquitoes in the pitcher plant environment. Overall 689 larvae from 165 pitchers were collected and dissected and the average colonization rate was 32%. Not all larvae in a pitcher were colonized. The prevalence of S. culisetae colonizations is reported in TABLE IGo. The proportions of colonized larvae collected on 3 Jul and 10 Dec 2001 and 3 Jan 2003 was statistically less than the expected colonization rate (P < 0.05). Conversely, the proportions of colonized larvae collected 31 Oct 2002 and 17 Mar 2003 were statistically higher than expected (P < 0.05). The Chi-square test indicated that there was no significant deviation from the expected proportion of pitchers with Trichomycetes (P > 0.05).


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  		TABLE I. Colonization of Wyeomia smithii with Smittium culisetae at Bull Pen Bog, Jackson County, North Carolina, 28 Jun 2001 to 21 May 2003
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The proportion of mosquito larvae colonized with S. culisetae fluctuated significantly throughout the year. This fluctuation could be the result of environmental factors or the life cycle of the larval mosquitoes. The two highest proportions of colonized larvae were found in March and at the end of October. These months correspond with the beginning and end of the period when the majority of the larvae are feeding (Bradshaw and Lounibos 1972Go). By November, air temperature can fall below freezing and mosquito larvae diapause. The high proportion of colonized larvae could result from increased larval feeding before diapause or could represent an increase in the number of colonized larvae as trichospores accumulate in the pitchers. March is the first warm month of the year during which freezing is unlikely to occur. Larval mosquitoes end diapause, become more active and feed on trichospores that accumulated over the winter. On the other hand, new spores could be introduced disproportionately into the pitchers during October and March, but no mechanism was determined for how new pitchers are inoculated with trichomycetes.

Two of the three collections with the lowest proportion of colonized larvae were from the winter months of December and January. Larvae of W. smithii diapause during the winter and usually do not feed (Bradshaw and Lounibos 1972Go); therefore, no new colonizations would be established. A collection from July also had a statistically smaller proportion of colonized larvae than expected. However, the collections from June and August of the same year were not statistically discernable from the expected proportion of colonized larvae if all colonizations were distributed randomly. I am unable to explain why the collections in July were disproportionally colonized less than larvae collected 10 d earlier. In other habitats Smittium culisetae colonizes a wide variety of Diptera, including chironomids, culicids, simulids, ceratopogonids and tipulids (Lichtwardt et al 1999Go). Beard and Adler (2002)Go reported on the seasonality of S. culisetae in Simuliidae of South Carolina. Their data indicate that this trichomycete was present sporadically in larval black flies, occurring in only one of their three collection streams in one of three years. Although it was most prevalent in the warmer months, only four colonized larvae were found, making determination of seasonality unreliable.

Several avenues are possible for the colonization of new pitchers by trichomycetes. Pitcher plants capture flying and crawling insects. These insects could be contaminated with trichospores or contain ovarian cysts. Taylor (1992)Go implied that some trichomycetes can invade the ovaries of their hosts and spread to new habitats when colonized females oviposit.

To date, trichomycetes had not been reported in the hindguts of W. smithii from similar bogs in North America. To make valid predictions about the occurrence and seasonality of S. culisetae in other populations of W. smithii, similar surveys must be undertaken in other bogs.


   ACKNOWLEDGMENTS
 
I thank J. Staeben and S.D. McCullough for their assistance with the fieldwork; C.E. Beard for identifying the trichomycete; and P.H. Adler, J.C. Morse, W. Wills, E. Ruppert, and G. Carner for reviewing drafts of this manuscript. This research was finaced partially by National Science Foundation DEB 0075269. This is Technical Contribution No. 4941 of the Clemson University Experiment Station.


   FOOTNOTES
 
Accepted for publication June 4, 2004.

1 Corresponding author. E-mail: cui8{at}cdc.gov


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Beard CE, Adler PH. 2002. Seasonality of trichomycetes in larval black flies from South Carolina, USA. Mycologia 94:200–209.[Abstract/Free Full Text]

Bradshaw WE, Holzapfel CM, Davison TE. 1998. Hourglass and rhythmic components of photoperiodic time measurement in the pitcher plant mosquito, Wyeomia smithii. Oecologia 117:486–495.

———, Lounibos LP. 1972. Photoperiodic control of development in the pitcher-plant mosquito, Wyeomyia smithii. Canadian Journal of Zoology 50:713–719.

Lichtwardt RW. 1986. The Trichomycetes: Fungal Associates of Arthropods. New York: Springer-Verlag. p 343.

———. 1994. Trichomycete fungi living in the guts of Costa Rican phytoelm larvae and other lentic dipterans. Revista de Biologia Tropical 42:31–48.

———, Ferrington LC Jr., Lopes Lastra C. 1999. Trichomycetes in Argentinean aquatic insect larvae. Mycologia 91:1060–1082.

Miller T, Cassill D, Johnson C, Kindell C, Leips J, Mcinnes D, Bevis T, Mehlman D, Richard B. 1994. Intraspecific and interspecific competition of Wyeomyia smithii (Coq.) in pitcher plant communities. American Midland Naturalist 131:136–145.

Misra JK, Lichtwardt RW. 2000. Illustrated Genera of Trichomycetes, Fungal Symbiotes of Insects and other Arthropods. Enfield, New Hampshire: Science Publishers Inc. p 155.

Nastase AJ, de la Rosa C, Newell SJ. 1995. Abundance of pitcher-plant mosquitoes, Wyeomyia smithii (Coq.) (Diptera: Culicidae) and midges, Metriocnemus knabi Coq. (Diptera: Chironomidae), in relation to pitcher characteristics of Sarracenia purpurea. American Midland Naturalist 133:44–51.

Taylor MR. 1992. Characterization of the microbial community within the digestive tracts of Simuliidae (Doctoral dissertation). United Kingdom: University of Portsmouth. p 313.




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