Biting Rates and Developmental Substrates for Biting Midges (Diptera: Ceratopogonidae) in Iquitos, Peru
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POPULATION AND COMMUNITY ECOLOGY Biting Rates and Developmental Substrates for Biting Midges (Diptera: Ceratopogonidae) in Iquitos, Peru 1 2 3 DAVID R. MERCER, GUSTAVO R. SPINELLI, DOUGLAS M. WATTS, AND ROBERT B. TESH Department of Pathology, University of Texas Medical Branch, Center for Tropical Diseases, 301 University Boulevard, Galveston, TX 77555Ð0609 Downloaded from https://academic.oup.com/jme/article-abstract/40/6/807/834903/ by guest on 03 October 2019 J. Med. Entomol. 40(6): 807Ð812 (2003) ABSTRACT Biting midges (Diptera: Ceratopogonidae) were collected at 16 periurban and rural sites around Iquitos, Peru, between 17 October 1996 and 26 May 1997. Culicoides paraensis (Goeldi), the principal vector of Oropouche virus, was the most commonly collected species (9,086 ßies) with Culicoides insinuatus Wirth & Blanton second (7,229 ßies). Although both species were collected at all sampling sites (linear distance surveyed '25 km), C. paraensis dominated at northern collection sites (.90%), whereas C. insinuatus prevailed at southern collection sites (.60%). C. paraensis were collected from human sentinels at a constant rate throughout daylight hours, at similar rates during wet and dry months, and regardless of rainfall. Larval developmental substrates for C. paraensis included decaying platano (Musa 3 paradisiaca L. [Musaceae]) stems, stumps, ßowers, fruits, and debris beneath platano trees as well as from soil beneath a fruiting mamay (Syzygium malaccense Merr. & Perry [Myrtaceae]) tree and organic-rich mud along a lake shoreline. C. insinuatus adults likewise emerged from decaying platano and organic-rich mud along a lake shoreline, but also from debris accumulated in the axils of aguaje (Mauritia flexuosa L. [Palmae]) fronds and decaying citrus fruit. Despite high numbers of biting adults near putative substrates, adults of neither species emerged from other decomposing plant material, soil, phytotelmata, or artiÞcial containers. Because both species of biting midges emerged in high numbers from all parts of platano (ubiquitous in Iquitos), it will be challenging to control them through sanitation. KEY WORDS Oropouche virus, arbovirus, host-seeking, biting rates, developmental substrates OROPOUCHE FEVER IS THE most important emerging hu- (1989) and Peru (1992), with .400,000 estimated man viral disease vectored by ceratopogonid biting cases worldwide between 1961 and 1995 (Tesh 1994). midges in the Western Hemisphere. The causative Additional outbreaks of ORO are likely in other re- agent, Oropouche (ORO) virus, is a member of the gions of the Caribbean, Central America, and tropical Simbu serogroup in the family Bunyaviridae. ORO South America as human populations grow, especially virus causes a self-limited, dengue-like illness, char- as they alter natural landscapes (Tesh 1994). acterized by fever, headache, myalgia, arthralgia, diz- Culicoides paraensis (Goeldi) (Diptera: Cerato- ziness, anorexia, and prostration of 2- to 5-d duration pogonidae) is the principal vector of ORO in periur- (LeDuc et al. 1981). One to several recurrences of ban cycles (Dixon et al. 1981, LeDuc et al. 1981, Rob- fever and chills occur in some patients after recovery. erts et al. 1981, Hoch et al. 1986, Wirth and Felippe- Effects upon fetal development have not been sufÞ- Bauer 1989) and a possible vector of Þlarial worms ciently studied, although other Simbu serogroup vi- (Shelley and Coscaro´n 2001) to humans in part of its ruses cause abortions and teratogenic effects in ani- range. The species is distributed from northern Ar- mals (Linley et al. 1983). gentina to north central United States (Wirth and ORO was Þrst isolated from a charcoal maker in Blanton 1973, Wirth and Felippe-Bauer 1989). Larvae Trinidad in 1955 (Anderson et al. 1961); the Þrst out- have been collected from decaying plant tissue (pla- break was documented in Bele´m, Para State (Brazil), tano [Musa 3 paradisiaca L. (Musaceae)] stems and in 1961 (Pinheiro et al. 1976). Subsequently, other cacao [Theobroma cacao (L.) (Sterculiaceae)] hulls) outbreaks have also been reported from Panama and phytotelmata (Linley et al. 1983, Hoch et al. 1986, Wirth and Felippe-Bauer 1989, Hoch et al. 1990). 1 Current address and corresponding author: Department of Biol- Therefore, adults may be numerous in periurban set- ogy, University of Northern Iowa, Cedar Falls, IA 50614Ð0421 (e-mail: tings with backyard gardens. Hoch et al. (1990) re- [email protected]). ported the daily biting activity of C. paraensis in 2 Cosejo Nacional de Investigaciones CientiÞcas y Tecnicas, Insti- Belem, Brazil; biting was highest during crepuscular tuto de Limnologia, La Plata, Argentina. ´ 3 United States Naval Medical Research Institute Detachment, Unit periods in houses and sun-exposed sites, but peaked at 3800, Lima, Peru. midday in shaded peridomestic sites. Linley et al. 0022-2585/03/0807Ð0812$04.00/0 q 2003 Entomological Society of America 808 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 40, no. 6 Table 1. Collection sites of biting Ceratopogonidae in Iquitos, Peru, between 17 October 1996 and 26 May 1997 Site Location Description Santa Maria S038 42.0019 W0738 14.3979 Small village, farms, backyard gardens, seasonal ßoodplain of Amazon River Punchana S038 43.1029 W0738 14.3619 River port, periurban, gardens, stilted homes on Amazon River ßoodplain Padre Isla S038 43.5239 W0738 13.7699 Island in Amazon River channel, rural with dense gardening and secondary forest Moronillo S038 43.7849 W0738 15.6539 Periurban, heavily residential surrounding seasonally ßooded lagoon Pradera S038 44.0359 W0738 16.1989 Edge of periurban settlement along lagoon of Nanay River Moronococha S038 44.6259 W0738 15.9389 Densely populated periurban neighborhood above lagoon of Nanay River Avenida Brasil S038 44.8309 W0738 15.4079 Periurban, heavily populated with drainage streams Aserradero S038 45.4229 W0738 16.3829 Private orchard with cement works adjacent to sawmill drainage stream Belen S038 45.9259 W0738 15.1399 Densely populated periurban stilted neighborhood seasonally ßooded by Itaya River Santa Clara S038 46.9379 W0738 20.4659 Isolated village along Nanay River, backyard gardens, surrounded by secondary forest Vihau S038 48.1319 W0738 18.5139 Small rural neighborhood, farms, less standing water Downloaded from https://academic.oup.com/jme/article-abstract/40/6/807/834903/ by guest on 03 October 2019 Finca de Sabino S038 49.1689 W0738 19.3169 Rural farm and orchard, limited standing water, surrounded by secondary forest Finca de Juan S038 49.6529 W0738 20.1059 Rural farm and palm plantation, surrounded by secondary forest Quistococha S038 49.7609 W0738 19.3109 Oxbow lake and tourist zoological center with sandy beach, secondary forest Correntillo S038 49.9359 W0738 21.7429 Dark water lagoon, surrounded with palm plantations, pasture, and secondary forest Morolillo S038 54.6269 W0738 20.3369 Isolated village, relatively recent, small farms with primary and secondary forest Sites are ordered from north to south. (1983) compiled data indicating peak biting activities landed, and all collecting was halted before sunset to during late afternoon. avoid malarial vectors. All biting ßies were aspirated Iquitos, Peru, a port city on the Amazon River be- by mouth, transferred to screened specimen cups, and tween the conßuences of the Nanay and Itaya Rivers provided with cotton moistened with sugar water. with .300,000 residents, was the site of a recent out- Biting midges were killed by freezing, counted, and break of ORO fever. Serological surveys in Iquitos identiÞed (by D.R.M.) using a dissecting stereomicro- have indicated high ORO antibody rates and annual scope according to published keys (Wirth and Blanton transmission among residents of Iquitos (Tesh 1994, 1973, Wirth et al. 1988, Wirth and Felippe-Bauer 1989) Watts et al. 1997, Baisley et al. 1998). Iquitos serves as and a reference collection of local species (provided a tourist, trade, and military center for the northern by G.R.S.). Rare individuals were identiÞed using part of Amazonian Peru. The region has also hosted wing patterns and genitalia dissection (by G.R.S.). numerous cooperative studies among Peruvian mili- During August 2000, a Garmin GPS III Plus (Garmin tary and public health agencies and United States Corporation, Olathe, KS) was used to estimate the researchers. Therefore, Iquitos not only serves as a latitude and longitude for each collection site. The locus for the spread of ORO, but it also presents a ratio (C. paraensis/[C. paraensis 1 C. insinuatus]) unique opportunity to study an emerging arbovirus captured was calculated for each collection site for all near its edge of expansion. dates. We investigated signiÞcant changes in the spe- The prevalence of ORO virus infection apparently cies ratio of biting ßies for each site along latitudinal increases with age-related exposure to bites from C. and longitudinal transects using PearsonÕs product- paraensis. A serological survey of ORO antibodies in moment correlation coefÞcients (Sokal and Rohlf Santa Clara (a small village near Iquitos) indicated a 1981). All statistical tests were performed with Statis- low incidence of infection for children (6Ð7%), but . 1 tica (1995). 50% incidence for adults (25 years, overall inci- Monthly Collections. Between January and May dence 34%, Baisley et al. 1998). Conversion of tropical 1997, monthly ceratopogonid collections were con- rain forest to agricultural use may favor the develop- ducted at 12 sites, a representative subset of the 16 ment of C. paraensis by providing more immature sites used. Two collectors at each site collected all developmental sites and human blood sources. As Iq- biting midges between 3:45 and 5:45 p.m. Three uitos expands and human colonizers clear the rain nearby sites were visited each day for each of 4 con- forest to build homes and plant gardens, they encoun- secutive days each month. Analysis of variance ter forest insects and novel pathogens. We studied (ANOVA) was used to test signiÞcant differences biting patterns and developmental substrates in peri- a 5 urban and rural sites around Iquitos to evaluate the ( 0.05) among months of collection and among vector potential of C.