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A survey of adult anophelines in French Guiana: enhanced descriptions of species distribution and biting responses Isabelle Dusfour, Romuald Carinci, Jean Issaly, Pascal Gaborit, and Romain Girod Institut Pasteur de la Guyane, Unité d’entomologie médicale, B.P. 6010, 97306 Cayenne Cedex, French Guiana, [email protected] Received 28 November 2012; Accepted 12 April 2013 ABSTRACT: In French Guiana, Anopheles darlingi is considered the main malaria vector. However, several reports have hypothesized the implication of other anopheline species in malaria transmission for the territory. Data on the ecology of these other potential vectors is rare or even unexplored in French Guiana. The aim of this study was to describe the biting habits of several anopheline species in multiple localities in French Guiana. Six sampling sites yielded 1,083 anopheline adults. Results indicated the presence of An. darlingi in all study locations and it was the only species to be collected inside villages. Other anophelines collected included An. aquasalis, An. braziliensis, An. intermedius, An. mediopunctatus, An. nuneztovari, An. oswaldoi, and An. triannulatus, all of which were associated with open areas and forests. The environment and time, at which biting behavior was recorded, varied for each species. It was noted that An. oswaldoi showed a daytime rhythm in open areas. This study is the first to report on the biting habits of a range of anophelines in French Guiana that may play a role in malaria transmission. This information is vital to fully describe the risk of malaria transmission and thereby design appropriate vector control measures and malaria prevention programs. Journal of Vector Ecology 38 (2): 203-209. 2013. Keyword Index: Anopheles darlingi, Anopheles oswaldoi, secondary vectors, biting behavior, malaria, French Guiana.
INTRODUCTION In French Guiana, most malaria transmission occurs inland adjacent to rivers, with sporadic cases regularly recorded in the coastal areas (Carme et al. 2009). Anopheline control strategy is based on deltamethrin indoor residual spraying and distribution of impregnated hammock/bed nets, targeting the main known malaria vector Anopheles darlingi in South America. While the majority of malaria transmission is correlated to Anopheles darlingi presence and density, this association is questionable in some places and during some periods of the year. Therefore, the potential role of a secondary species is often hypothesized to explain the transmission of the disease in these areas (Pajot et al. 1978, Girod et al. 2011, Stefani et al. 2011). The status of Anopheles darlingi as a primary vector is due to its species-wide distribution, anthropophilic behavior, population densities, and entomological inoculation rates (Girod et al. 2008, Hiwat et al. 2009, Fouque et al. 2010). T h e w i d e range of ecological characteristics and habits of Anopheles darlingi have been largely reviewed (Zimmerman 1992, Mouchet et al. 2004, Sinka et al. 2010, Hiwat and Bretas 2011). This adaptability led to the hypothesis of a species complex, but no evidence has yet been found (Hiwat and Bretas 2011). Apart from An. darlingi, other anophelines suspected to be primary or secondary vectors in different parts of South America (Mouchet et al. 2004) have been collected in French Guiana and their infection by Plasmodium species demonstrated (Dusfour et al. 2012a). Among them, An. nuneztovari is reported as a secondary vector in Brazil
and Venezuela (de Arruda et al. 1986, Tadei et al. 1998, Galardo et al. 2007) and is suspected to be responsible for local transmission in Suriname (Zimmerman 1992). A P. falciparum infected An. nuneztovari specimen has been collected in Saint Georges, French Guiana (Dusfour et al. 2012a). In addition, An. intermedius and An. oswaldoi s.l., often described as occasional vectors (Mouchet et al. 2004), were found infected with P. falciparum in different villages of French Guiana (Dusfour et al. 2012a). On the other hand, An.aquasalis, An. marajoara, and An. triannulatus s.l., also considered as vectors in South America, have been regularly collected in French Guiana but never found naturally infected (Deane 1988, Rozendaal 1990, Laubach et al. 2001, Galardo et al. 2007, Moreno et al. 2009). Descriptions of the basic ecology for these secondary vectors are rare or even unexplored in French Guiana and their epidemiological importance in malaria transmission remains unclear. The aim of this study was to describe the biting habits of several suspected malaria vectors to inform effective adjustments in anopheline mosquito control strategies. Mosquito collections were conducted in forests, open areas, and villages during day and night sampling periods in multiple localities throughout French Guiana. MATERIALS AND METHODS Study sites Mosquito collections took place in multiple localities throughout French Guiana. This French territory is located in northeastern South America bordered by Suriname to the west and Brazil to the south and east. Six villages located
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in coastal and inland areas and corresponding surrounding habitat were selected for this study (Figure 1): 1) Camopi (CAM), a remote Amerindian village situated in the middleOyapock region accessible only by dugout canoe or plane and surrounded by primary rainforest; 2) Saint Georges de l’Oyapock (SGO), a Brazilian community hamlet situated in the lower-Oyapock region close to the Oyapock River; 3) Régina (REG), an Amerindian hamlet situated along the Approuagues River (collections were conducted 1 km away from the river); 4) Cacao (CAC), characterized by a community of H’mong immigrants from Laos settled in French Guiana since 1977, located in one of the major farming areas in French Guiana along the Comté River; 5) Matoury (MAT), in the suburb of the main town Cayenne, where collections were conducted in an area with households and food-producing crops along a dust road called “piste Mogès”; and 6) Kourou (KOU), a village of Brazilian settlers along a dust road called “piste des compagnons réunis” in an area of frequently flooded savannah. Adult mosquito collections Human-landing captures (HLC) were performed during the short and long rainy seasons from December, 2007 to June, 2011. During this period the sun rises between 06:15 and 06:45 and sets between 18:39 and 18:42, respectively.
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Four seasons are recognized in French Guiana: a short rainy season (December to January), a short dry season (February to mid-April), a long rainy season (mid-April to mid-July), and a long dry season (mid-July to November). Collections were conducted on two consecutive days at each site by one person at dawn (05:00-7:00), dusk and night (18:0022:00), and during the day (09:00-11:00; 15:00-17:00) in the outdoor environment. Collections were repeated at each study site two or three times. Mosquitoes were collected as they landed on local residents who were employed by the Pasteur Institute of French Guiana and carefully supervised by an entomologist. Mosquitoes landing on the exposed lower legs of the collectors were caught with mouth aspirators and transferred to collecting pots that were labelled with the type of environment and time of collection. Species collection environments at each locality were categorized into three distinct types: open, forest, and village. Open was defined as deforested cultivated or uncultivated land without houses; the forest type included primary and secondary growths; and village corresponded to a group of houses. Mosquito handling and species identification All captured anopheline specimens were individually stored in 1.5 ml microtubes filled with dessicant and transported from the field to the laboratory in Cayenne where morphological identification was performed using standard keys for the region (Floch and Abonnenc 1951, Forattini 1962, Faran and Linthicum 1981). Statistical analysis In order to control effort bias, the human biting rate (HBR), corresponding to the number of mosquitoes per person-hour of collections (i.e., the number of mosquitoes divided by the time spent and the number of people collecting), was computed for each data set prior to analysis. Associations between Anopheles species with environmental class (forest, open area, village) and time (05:00-07:00, 09:00-11:00, 15:00-17:00, 18:00-22:00) were investigated by using correspondence analysis (CA), which displays multidimensional representation of the association between row and column categories in a two-way contingency table. This technique fixes scores for row and column categories which account for the greatest proportion for association between the row and column categories. The lower the χ² value is, the more associated the categories are. All analyses were performed using PROC CORRESP procedure in SAS version 9.1 (SAS Institute Inc., Cary, NC, U.S.A.). RESULTS
Figure 1. Map indicating anopheline collection localities in French Guiana. CAC: Cacao; CAM: Camopi; KOU Kourou; MAT: Matoury; REG: Régina; SGO: Saint Georges de l’Oyapock.
A total of 1,083 anopheline adults were collected from all study localities during 2,456 person-hour collections giving an overall HBR of 0.44 bites per personhour. Ten species were identified (Table 1), eight of them known to be primary vectors (An. aquasalis, An. darlingi, An. nuneztovari) or secondary/occasional vectors (An. braziliensis, An. intermedius, An. mediopunctatus, An. oswaldoi, An. triannulatus) in South America. Among
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Table 1. The mean anopheline density (mosquitoes per person-hour) per species by collection site CAC: Cacao, CAM: Camopi, KOU: Kourou, MAT: Matoury, REG: Régina, SGO: Saint Georges de l’Oyapock. *Number of different species. N
CAC
CAM
KOU
MAT
An. darlingi
624
0.165
0.411
0.144
0.283
An. braziliensis
171
0.010
-
0.344
An. intermedius
59
0.077
0.036
-
An. triannulatus
58
0.069
-
An. nuneztovari
49
0.044
0.044
An. oswaldoi
44
-
0.070
An. acanthotorhynus/nimbus
27
-
-
An. mediopunctatus
22
-
-
An. aquasalis
10
-
-
An. argyritarsis
1
0.002
Anopheles spp.
18
Overall
REG
SGO
0.342
0.054
0.033
-
0.107
-
-
-
0.014
0.017
0.008
0.039
0.003
-
-
-
-
-
0.003
-
0.042
0.008
0.003
0.029
0.006
0.003
0.006
0.061
0.017
0.011
-
-
-
-
-
-
-
0.002
-
0.011
0.022
0.008
0.007
0.369
0.560
0.581
0.378
0.369
0.296
7
4
8
7
6
6
Species Richness*
Table 2. The mean anopheline density (mosquitoes per person-hour) per species by collection environment. *Number of different species. N
Open area
Forest
Village
An. darlingi
624
0.378
0.063
0.304
An. braziliensis
171
0.189
0.009
0.029
An. intermedius
59
0.065
0.016
0.001
An. triannulatus
58
0.021
0.057
0.004
An. nuneztovari
49
0.057
0.006
0.004
An. oswaldoi
44
0.053
0.001
0.005
An. acantothorhynus/nimbus
27
-
0.040
-
An. mediopunctatus
22
0.003
0.029
-
An.aquasalis
10
0.010
0.001
0.002
An. argyritarsis
1
0.001
-
-
0.788
0.229
0.354
9
9
7
Overall Species Richness*
Table 3. The mean anopheline density (mosquito per person-hour) per species by collection time. *Number of different species.
An. darlingi An. braziliensis An. intermedius An. triannulatus An. nuneztovari An. oswaldoi An. acantothorhynus/nimbus An. mediopunctatus An.aquasalis An. argyritarsis Overall Species Richness*
N
5-7am
9-11am
3-5pm
624 171 59 58 49 44 27 22 10 1
0.444 0.151 0.024 0.016 0.038 0.012 0.004 0.006 0.002 0.002 0.706 10
0.022 0.002 0.002 0.015 0.015 0.058 5
0.009 0.002 0.004 0.009 0.013 0.011 0.002 0.054 7
6-10pm 0.393 0.096 0.044 0.045 0.030 0.025 0.013 0.019 0.008 0.686 9
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collection sites, the HBR varied from 0.296 to 0.581 bites per person-hour, with KOU indicating highest and SGO lowest. Species richness from varied 4 to 8, with KOU indicating highest and CAM lowest (Table 1). Regarding the type of environment in which anopheline were collected, open areas captured the highest overall density (0.788 bites per person-hour), whereas forest and village categories accounted for 0.229 and 0.354 bites per person-hour, respectively (Table 2). However, both forest and open areas captured a broader number of anopheline species (N=9) as compared to the villages (N=6). The Correspondence Analysis showed that An. darlingi was the only species t h a t w a s strongly associated with the village environment category, although it was also collected in high density in the open areas (Table 2, Figure 2). This analysis also demonstrated that Anopheles aquasalis, An. braziliensis, An. intermedius, An. nuneztovari, and An. oswaldoi were all associated with open areas. An. acanthotorhynus/nimbus, An. mediopunctatus s.l., and An. triannulatus s.l. were strongly associated with forest (Table 2, Figure 2). The majority of all anopheline species collected were captured during the 05:00-7:00 and 18:00-22:00 time periods (0.706 and 0.686 bites per person-hour, respectively) (Table 3). However, even with lower densities, the range of anopheline species collected during the day was non-negligible, with five to seven species collected for the 09:00-11:00 and 15:00-17:00 ranges, compared to nine and ten species for the 05:00-07:00 and 18:00-22:00 ranges, respectively (Table 3). Anopheles aquasalis, An. intermedius, An. mediopunctatus, and An. triannulatus were highly associated with the dusk-nighttime collection periods, whereas An. darlingi, An. nuneztovari, and An. braziliensis were collected during both dusk-nighttime and dawn sampling periods. Anopheles aquasalis, An. braziliensis, An. darlingi, and An. triannulatus were also collected in low numbers during the day (09:00-11:00; 15:00-17:00) (Table 3, Figure 3). There was a strong association of An. acanthotorhynus/nimbus and
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especially An. oswaldoi to daytime biting (09:00-11:00; 15:0017:00) (Table 3, Figure 3). DISCUSSION This study is the first to report on the biting habits of a range of anophelines that may play a role in malaria transmission from six localities throughout French Guiana. Sampling performed in three types of environments yielded ten species out of the 25 listed for the territory (Floch and Abonnenc 1951, Degallier and Claustre 1980) (www. mosquitocatalog.org). Anopheles darlingi was the most abundant and widely distributed, being collected at each study locality, confirming its range from coastal areas to deep forest environments. This result is not unexpected as previous papers have also described a wide range of breeding habitat types for this species. Anopheles darlingi presence is often related to rivers and forests (Mouchet et al. 2004, Sinka et al. 2010, Hiwat and Bretas 2011) but has also been recorded i n savannahs and swamps (Pajot et al. 1977, Claustre et al. 2001, Povoa et al. 2006, Girod et al. 2011) as well as humanaltered environments (Tadei et al. 1998, Vittor et al. 2006). Ecological data on the other anopheline species are still scarce but our observations agree with what is known a b o u t t h e ecology of these mosquitoes. Indeed, An. aquasalis, whose breeding sites are mainly characterized by brackish water (Mouchet et al. 2004), was found on the coastal collection sites of Kourou and Matoury. Anopheles nuneztovari is well known to breed in sunlit small to medium-sized pools in flooded areas filled with vegetation (de Barros et al. 2007, Montoya-Lerma et al. 2011). This typology is encountered in many localities in French Guiana, from coastal to riparian and inland collection sites explaining the wide distribution of An. nuneztovari across the territory (Pajot et al. 1978, Girod et al. 2008, Berger et al. 2011, Dusfour et al. 2012a, 2012b). Anopheles oswaldoi was mainly found in Camopi, the most forested site, which Figure 2. Two-dimensional ordinations of the two-dimensional correspondence analysis showing the relationship between collected anopheline species (raw categories. bold. square dots) and the ecology of collection sites (column categories. circle dots). The smaller the distances between points, the “stronger” their associate with points of a certain category positioned close to each other are similar with regard to the pattern of relative frequencies across the other category. DAR: An. darlingi, BRA: An. braziliensis, INT: An. intermedius, TRI: An. triannulatus, NUN: An. nuneztovari, OSW: An. oswaldoi, ACA: An. acantothorhynus/nimbus, MED: An. mediopunctatus, AQU: An.aquasalis, ARG: An. argyritarsis.
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207 Figure 3. Two-dimensional ordinations of the three-dimensional correspondence analysis showing the relationship between collected anopheline species (raw categories, bold, square dots) and the time of sites (column categories, circle dots). Dimension 1 plus 2 display 98.59% of the variance. The smaller the distances between points, the “stronger” their associate, with points of a certain category positioned close to each other similar with regard to the pattern of relative frequencies across the other category. DAR: An. darlingi, BRA: An. braziliensis, INT: An. intermedius, TRI: An. triannulatus, NUN: An. nuneztovari, OSW: An. oswaldoi, ACA: An. acantothorhynus/ nimbus, MED: An. mediopunctatus, AQU: An. aquasalis, ARG: An. argyritarsis.
corroborates its preference for primary forest (Floch and Abonnenc 1947, de Barros et al. 2007, Hiwat et al. 2009). Anopheles intermedius has been described as sylvatic or perisylvatic and zoophilic (Floch and Abonnenc 1951, Forattini 1962, Zimmerman et al. 2006, Galardo et al. 2007). Its distribution is known to be territory-wide in French Guiana and was encountered only in the two inland localities Cacao and Camopi during the current study. Its zoophilic behavior may be explain by sampling bias as collections were only made by human landing method. Anopheles triannulatus breeding sites have been linked to large sunlit stagnant water ponds containing floating vegetation corresponding to fish ponds, natural depressions (Floch and Abonnenc 1951, de Barros et al. 2007), or flooded areas in riverine sites (Hiwat et al. 2009). The range of potential breeding sites explains its presence in many sites where permanent or temporary flooded areas are recorded and in Cacao where fish breeding is well developed. Beyond species presence, the current study also investigated the biting patterns of anophelines within each collection site. Results showed An. darlingi to bite mainly at dusk-night and dawn sampling periods in both open and village settings. This report supports previous characterizations of An. darlingi biting preferences such that early evening through morning periods had the highest abundance with specific biting modalities according to location and time of year (Pajot et al. 1977, Voorham 2002). Daytime activity has also been previously reported in forest camps by Floch (1954). Nighttime biting and preference for village settings increase its contact with humans and favors malaria transmission, but also supports the use of mosquito nets and indoor residual spraying as effective control strategies where An. darlingi occurs (Hiwat et al. 2012, Martins-Campos et al. 2012). The observation of daytime biting activity is interesting since some malaria transmission patterns are far from clear. For example, two annual malaria transmission peaks are recorded in Camopi. One is related to both Plasmodium
falciparum and P. vivax in the early rainy season (January) and the other one linked to P. vivax infection at the end of the rainy season (June) (Stefani et al. 2011). Whereas the peak in June in the rainy season corresponds to the presence of An. darlingi in the village, the second does not correlate with the presence of this main suspected vector (Girod et al. 2011). This observation suggests transmission by other anopheline species such as An. nuneztovari (Stefani et al. 2011) or An. neivai (Pajot et al. 1978), or that transmission occurs outside the village, in crop fields, or in the forest where people are hunting or fishing (this study). Those hypotheses are even reinforced by the presence of P. falciparum positive specimens in Camopi (An. oswaldoi s.l.) and also in Saint Georges de l’Oyapock (An. nuneztovari and An. intermedius) and Cacao (An. intermedius) (Dusfour et al. 2012a). Anopheles aquasalis, An. intermedius, and An. nuneztovari were all strongly associated with collections from open areas, whereas An. triannulatus was associated with forest settings. All species were collected during the day sampling period except An. nuneztovari which was strictly collected at the dusk-night and dawn times. The roles of these species in pathogen transmission depends upon the behavior of t h e human population in the surrounding area that brings them in contact with the adult mosquitoes. Human population behaviors and malaria prevention measures vary in French Guiana as the territory is composed of multicultural communities whose differences are characterized by habitat, behavior, and socio-economic status. All current malaria prevention and vector control measures in French Guiana are based on the presumption that An. darlingi is a primary vector throughout the country and the presumptive nocturnal biting activity of anophelines. Little consideration has been given to other potential vectors and their roles in malaria transmission on the habits of people at risk. Our study represents a general survey of adult anophelines throughout French Guiana and
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has confirmed the presence of several mosquito species that exhibit human biting and therefore could play a role in malaria transmission. This also complements a previous work demonstrating that An. intermedius, An. nuneztovari, and An. oswaldoi are able to transmit P. falciparum parasites in the same study localities (Dusfour et al. 2012a). Additionnal investigation will be required to better describe human behaviors and to fully determine which anopheline species are responsible for disease in a given locality. Findings reported here highlight that not only presence but also biting patterns within different environments must be characterized to design effective vector control measures and malaria prevention programs. Acknowledgments Funds for this study were provided by the local health agency in French Guiana. The authors wish to thank Sarah C. Chaney and other reviewers for proofreading the manuscript and providing valuable comments. REFERENCES CITED Berger, F., C. Flamand, L. Musset, F. Djossou, J. Rosine, M.A. Sanquer, I. Dusfour, E. Legrand, V. Ardillon, P. Rabarison, C. Grenier, and R. Girod. 2011. Investigation of a sudden malaria outbreak in the isolated Amazonian village of Saul, French Guiana, January-April 2009. Am. J. Trop. Med. Hyg. 86: 591-597. Carme, B., V. Ardillon, R. Girod, C. Grenier, M. Joubert, F. Djossou, and F. Ravachol. 2009. [Update on the epidemiology of malaria in French Guiana]. Med. Trop. 69: 19-25. Claustre, J., C. Venturin, M. Nadire, and P. Fauran. 2001. [Malarial vectors in French Guiana: study in an epidemic focus near Cayenne (1989-1998)]. Bull. Soc. Pathol. Exot. 94: 353-357. de Arruda, M., M.B. Carvalho, R. S. Nussenzweig, M. Maracic, A.W. Ferreira, and A.H. Cochrane. 1986. Potential vectors of malaria and their different susceptibility to Plasmodium falciparum and Plasmodium vivax in northern Brazil identified by immunoassay. Am. J. Trop. Med. Hyg. 35: 873-881. de Barros, F.S., D.B. de Aguiar, M.G. Rosa-Freitas, J.F. Luitgards-Moura, H. Gurgel da Costa, N.A. Honorio, M.E. de Arruda, P. Tsouris, and S.D. Vasconcelos. 2007. Distribution summaries of malaria vectors in the northern Brazilian Amazon. J. Vector Ecol. 32: 161-167. Deane, L.M. 1988. Malaria studies and control in Brazil. Am. J. Trop. Med. Hyg. 38: 223-230. Degallier, N. and J. Claustre. 1980. [Culicidae (Diptera, Nematocera) de Guyane Française: notes faunistiques et taxonomiques]. Rev. Fr. Entomol. 2: 138-146. Dusfour, I., J. Issaly, R. Carinci, P. Gaborit, and R. Girod. 2012a. Incrimination of Anopheles (Anopheles) intermedius Peryassu, An. (Nyssorhynchus) nuneztovari Gabaldon, An. (Nys.) oswaldoi Peryassu as natural vectors of Plasmodium falciparum in French Guiana. Mem. Inst.
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insecticide-treated nets (ITNs); malaria down to near elimination level. 86: 649-655. Laubach, H. E., L. Validum, J. A. Bonilla, A. Agar, R. Cummings, C. Mitchell, R. R. Cuadrado, and C. J. Palmer. 2001. Identification of Anopheles aquasalis as a possible vector of malaria in Guyana, South America. West Indian Med. J. 50: 319-321. Martins-Campos, K. M., W. D. Pinheiro, S. Vitor-Silva, A. M. Siqueira, G. C. Melo, I. C. Rodrigues, N. F. Fe, M. Barbosa, W. P. Tadei, C. Guinovart, Q. Bassat, P. L. Alonso, M. V. Lacerda, and W. M. Monteiro. 2012. Integrated vector management targeting Anopheles darlingi populations decreases malaria incidence in an unstable transmission area, in the rural Brazilian Amazon. Malar. J. 11: 351. Montoya-Lerma, J., Y.A. Solarte, G.I. Giraldo-Calderon, M.L. Quinones, F. Ruiz-Lopez, R.C. Wilkerson, and R. Gonzalez. 2011. Malaria vector species in Colombia: a review. Mem. Inst. Oswaldo Cruz. 106 Suppl. 1: 223-238. Moreno, J.E., Y. Rubio-Palis, E. Paez, E. Perez, V. Sanchez, and E. Vaccari. 2009. Malaria entomological inoculation rates in gold mining areas of Southern Venezuela. Mem. Inst. Oswaldo Cruz 104: 764-768. Mouchet, J., P. Carnevale, M. Coosemans, J. Julvez, S. Manguin, D. Richard-Lenoble, and J. Sircoulon. 2004. [Biodiversité du paludisme dans le monde]. John Libbey, Eurotext, Paris. Pajot, F.X., F. Le Pont, J.F. Molez, and N. Degallier. 1977. [Agressivité d’Anopheles (Nyssorhynchus) darlingi Root, 1926 (Diptera, Culicidae) en Guyane Française]. Cah. ORSTOM Sér. Entomol. Méd. Parasitol. XV: 15-22. Pajot, F.X., J.F. Molez, and F. Le Pont. 1978. [Anophèles et paludisme sur le Haut- Oyapock (Guyane Française)]. Cah. ORSTOM Sér. Entomol. Méd. Parasitol. XVI: 105111. Povoa, M.M., R.T. de Souza, R.N. Lacerda, E.S. Rosa, D. Galiza, J.R. de Souza, R.A. Wirtz, C.D. Schlichting, and J.E. Conn. 2006. The importance of Anopheles albitarsis E and An. darlingi in human malaria transmission in Boa Vista, state of Roraima, Brazil. Mem. Inst. Oswaldo Cruz 101: 163-168.
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Rozendaal, J.A. 1990. Observations on the distribution of anophelines in Suriname with particular reference to the malaria vector Anopheles darlingi. Mem. Inst. Oswaldo Cruz 85: 221-234. Sinka, M.E., Y. Rubio-Palis, S. Manguin, A.P. Patil, W.H. Temperley, P.W. Gething, T. Van Boeckel, C.W. Kabaria, R.E. Harbach, and S.I. Hay. 2010. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic precis. Parasit. Vectors 3: 72. Stefani, A., M. Hanf, M. Nacher, R. Girod, and B. Carme. 2011. Environmental, entomological, socioeconomic and behavioural risk factors for malaria attacks in Amerindian children of Camopi, French Guiana. Malar. J. 10: 246. Tadei, W.P., B.D. Thatcher, J.M. Santos, V.M. Scarpassa, I.B. Rodrigues, and M.S. Rafael. 1998. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am. J. Trop. Med. Hyg. 59: 325-335. Vittor, A.Y., R.H. Gilman, J. Tielsch, G. Glass, T. Shields, W.S. Lozano, V. Pinedo- Cancino, and J.A. Patz. 2006. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am. J. Trop. Med. Hyg. 74: 3-11. Voorham, J. 2002. Intra-population plasticity of Anopheles darlingi’s (Diptera, Culicidae) biting activity patterns in the state of Amapa, Brazil. Rev. Saude Publica. 36: 75-80. Zimmerman, R.H. 1992. Ecology of malaria vectors in the Americas and future direction. Mem. Inst. Oswaldo Cruz 87 Suppl 3: 371-383. Zimmerman, R.H., A.K. Galardo, L.P. Lounibos, M. Arruda, and R. Wirtz. 2006. Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon. J. Med. Entomol. 43: 947-956.
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A survey of adult anophelines in French Guiana: enhanced descriptions of species distribution and biting responses Isabelle Dusfour, Romuald Carinci, Jean Issaly, Pascal Gaborit, and Romain Girod Institut Pasteur de la Guyane, Unité d’entomologie médicale, B.P. 6010, 97306 Cayenne Cedex, French Guiana, [email protected] Received 28 November 2012; Accepted 12 April 2013 ABSTRACT: In French Guiana, Anopheles darlingi is considered the main malaria vector. However, several reports have hypothesized the implication of other anopheline species in malaria transmission for the territory. Data on the ecology of these other potential vectors is rare or even unexplored in French Guiana. The aim of this study was to describe the biting habits of several anopheline species in multiple localities in French Guiana. Six sampling sites yielded 1,083 anopheline adults. Results indicated the presence of An. darlingi in all study locations and it was the only species to be collected inside villages. Other anophelines collected included An. aquasalis, An. braziliensis, An. intermedius, An. mediopunctatus, An. nuneztovari, An. oswaldoi, and An. triannulatus, all of which were associated with open areas and forests. The environment and time, at which biting behavior was recorded, varied for each species. It was noted that An. oswaldoi showed a daytime rhythm in open areas. This study is the first to report on the biting habits of a range of anophelines in French Guiana that may play a role in malaria transmission. This information is vital to fully describe the risk of malaria transmission and thereby design appropriate vector control measures and malaria prevention programs. Journal of Vector Ecology 38 (2): 203-209. 2013. Keyword Index: Anopheles darlingi, Anopheles oswaldoi, secondary vectors, biting behavior, malaria, French Guiana.
INTRODUCTION In French Guiana, most malaria transmission occurs inland adjacent to rivers, with sporadic cases regularly recorded in the coastal areas (Carme et al. 2009). Anopheline control strategy is based on deltamethrin indoor residual spraying and distribution of impregnated hammock/bed nets, targeting the main known malaria vector Anopheles darlingi in South America. While the majority of malaria transmission is correlated to Anopheles darlingi presence and density, this association is questionable in some places and during some periods of the year. Therefore, the potential role of a secondary species is often hypothesized to explain the transmission of the disease in these areas (Pajot et al. 1978, Girod et al. 2011, Stefani et al. 2011). The status of Anopheles darlingi as a primary vector is due to its species-wide distribution, anthropophilic behavior, population densities, and entomological inoculation rates (Girod et al. 2008, Hiwat et al. 2009, Fouque et al. 2010). T h e w i d e range of ecological characteristics and habits of Anopheles darlingi have been largely reviewed (Zimmerman 1992, Mouchet et al. 2004, Sinka et al. 2010, Hiwat and Bretas 2011). This adaptability led to the hypothesis of a species complex, but no evidence has yet been found (Hiwat and Bretas 2011). Apart from An. darlingi, other anophelines suspected to be primary or secondary vectors in different parts of South America (Mouchet et al. 2004) have been collected in French Guiana and their infection by Plasmodium species demonstrated (Dusfour et al. 2012a). Among them, An. nuneztovari is reported as a secondary vector in Brazil
and Venezuela (de Arruda et al. 1986, Tadei et al. 1998, Galardo et al. 2007) and is suspected to be responsible for local transmission in Suriname (Zimmerman 1992). A P. falciparum infected An. nuneztovari specimen has been collected in Saint Georges, French Guiana (Dusfour et al. 2012a). In addition, An. intermedius and An. oswaldoi s.l., often described as occasional vectors (Mouchet et al. 2004), were found infected with P. falciparum in different villages of French Guiana (Dusfour et al. 2012a). On the other hand, An.aquasalis, An. marajoara, and An. triannulatus s.l., also considered as vectors in South America, have been regularly collected in French Guiana but never found naturally infected (Deane 1988, Rozendaal 1990, Laubach et al. 2001, Galardo et al. 2007, Moreno et al. 2009). Descriptions of the basic ecology for these secondary vectors are rare or even unexplored in French Guiana and their epidemiological importance in malaria transmission remains unclear. The aim of this study was to describe the biting habits of several suspected malaria vectors to inform effective adjustments in anopheline mosquito control strategies. Mosquito collections were conducted in forests, open areas, and villages during day and night sampling periods in multiple localities throughout French Guiana. MATERIALS AND METHODS Study sites Mosquito collections took place in multiple localities throughout French Guiana. This French territory is located in northeastern South America bordered by Suriname to the west and Brazil to the south and east. Six villages located
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in coastal and inland areas and corresponding surrounding habitat were selected for this study (Figure 1): 1) Camopi (CAM), a remote Amerindian village situated in the middleOyapock region accessible only by dugout canoe or plane and surrounded by primary rainforest; 2) Saint Georges de l’Oyapock (SGO), a Brazilian community hamlet situated in the lower-Oyapock region close to the Oyapock River; 3) Régina (REG), an Amerindian hamlet situated along the Approuagues River (collections were conducted 1 km away from the river); 4) Cacao (CAC), characterized by a community of H’mong immigrants from Laos settled in French Guiana since 1977, located in one of the major farming areas in French Guiana along the Comté River; 5) Matoury (MAT), in the suburb of the main town Cayenne, where collections were conducted in an area with households and food-producing crops along a dust road called “piste Mogès”; and 6) Kourou (KOU), a village of Brazilian settlers along a dust road called “piste des compagnons réunis” in an area of frequently flooded savannah. Adult mosquito collections Human-landing captures (HLC) were performed during the short and long rainy seasons from December, 2007 to June, 2011. During this period the sun rises between 06:15 and 06:45 and sets between 18:39 and 18:42, respectively.
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Four seasons are recognized in French Guiana: a short rainy season (December to January), a short dry season (February to mid-April), a long rainy season (mid-April to mid-July), and a long dry season (mid-July to November). Collections were conducted on two consecutive days at each site by one person at dawn (05:00-7:00), dusk and night (18:0022:00), and during the day (09:00-11:00; 15:00-17:00) in the outdoor environment. Collections were repeated at each study site two or three times. Mosquitoes were collected as they landed on local residents who were employed by the Pasteur Institute of French Guiana and carefully supervised by an entomologist. Mosquitoes landing on the exposed lower legs of the collectors were caught with mouth aspirators and transferred to collecting pots that were labelled with the type of environment and time of collection. Species collection environments at each locality were categorized into three distinct types: open, forest, and village. Open was defined as deforested cultivated or uncultivated land without houses; the forest type included primary and secondary growths; and village corresponded to a group of houses. Mosquito handling and species identification All captured anopheline specimens were individually stored in 1.5 ml microtubes filled with dessicant and transported from the field to the laboratory in Cayenne where morphological identification was performed using standard keys for the region (Floch and Abonnenc 1951, Forattini 1962, Faran and Linthicum 1981). Statistical analysis In order to control effort bias, the human biting rate (HBR), corresponding to the number of mosquitoes per person-hour of collections (i.e., the number of mosquitoes divided by the time spent and the number of people collecting), was computed for each data set prior to analysis. Associations between Anopheles species with environmental class (forest, open area, village) and time (05:00-07:00, 09:00-11:00, 15:00-17:00, 18:00-22:00) were investigated by using correspondence analysis (CA), which displays multidimensional representation of the association between row and column categories in a two-way contingency table. This technique fixes scores for row and column categories which account for the greatest proportion for association between the row and column categories. The lower the χ² value is, the more associated the categories are. All analyses were performed using PROC CORRESP procedure in SAS version 9.1 (SAS Institute Inc., Cary, NC, U.S.A.). RESULTS
Figure 1. Map indicating anopheline collection localities in French Guiana. CAC: Cacao; CAM: Camopi; KOU Kourou; MAT: Matoury; REG: Régina; SGO: Saint Georges de l’Oyapock.
A total of 1,083 anopheline adults were collected from all study localities during 2,456 person-hour collections giving an overall HBR of 0.44 bites per personhour. Ten species were identified (Table 1), eight of them known to be primary vectors (An. aquasalis, An. darlingi, An. nuneztovari) or secondary/occasional vectors (An. braziliensis, An. intermedius, An. mediopunctatus, An. oswaldoi, An. triannulatus) in South America. Among
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Table 1. The mean anopheline density (mosquitoes per person-hour) per species by collection site CAC: Cacao, CAM: Camopi, KOU: Kourou, MAT: Matoury, REG: Régina, SGO: Saint Georges de l’Oyapock. *Number of different species. N
CAC
CAM
KOU
MAT
An. darlingi
624
0.165
0.411
0.144
0.283
An. braziliensis
171
0.010
-
0.344
An. intermedius
59
0.077
0.036
-
An. triannulatus
58
0.069
-
An. nuneztovari
49
0.044
0.044
An. oswaldoi
44
-
0.070
An. acanthotorhynus/nimbus
27
-
-
An. mediopunctatus
22
-
-
An. aquasalis
10
-
-
An. argyritarsis
1
0.002
Anopheles spp.
18
Overall
REG
SGO
0.342
0.054
0.033
-
0.107
-
-
-
0.014
0.017
0.008
0.039
0.003
-
-
-
-
-
0.003
-
0.042
0.008
0.003
0.029
0.006
0.003
0.006
0.061
0.017
0.011
-
-
-
-
-
-
-
0.002
-
0.011
0.022
0.008
0.007
0.369
0.560
0.581
0.378
0.369
0.296
7
4
8
7
6
6
Species Richness*
Table 2. The mean anopheline density (mosquitoes per person-hour) per species by collection environment. *Number of different species. N
Open area
Forest
Village
An. darlingi
624
0.378
0.063
0.304
An. braziliensis
171
0.189
0.009
0.029
An. intermedius
59
0.065
0.016
0.001
An. triannulatus
58
0.021
0.057
0.004
An. nuneztovari
49
0.057
0.006
0.004
An. oswaldoi
44
0.053
0.001
0.005
An. acantothorhynus/nimbus
27
-
0.040
-
An. mediopunctatus
22
0.003
0.029
-
An.aquasalis
10
0.010
0.001
0.002
An. argyritarsis
1
0.001
-
-
0.788
0.229
0.354
9
9
7
Overall Species Richness*
Table 3. The mean anopheline density (mosquito per person-hour) per species by collection time. *Number of different species.
An. darlingi An. braziliensis An. intermedius An. triannulatus An. nuneztovari An. oswaldoi An. acantothorhynus/nimbus An. mediopunctatus An.aquasalis An. argyritarsis Overall Species Richness*
N
5-7am
9-11am
3-5pm
624 171 59 58 49 44 27 22 10 1
0.444 0.151 0.024 0.016 0.038 0.012 0.004 0.006 0.002 0.002 0.706 10
0.022 0.002 0.002 0.015 0.015 0.058 5
0.009 0.002 0.004 0.009 0.013 0.011 0.002 0.054 7
6-10pm 0.393 0.096 0.044 0.045 0.030 0.025 0.013 0.019 0.008 0.686 9
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collection sites, the HBR varied from 0.296 to 0.581 bites per person-hour, with KOU indicating highest and SGO lowest. Species richness from varied 4 to 8, with KOU indicating highest and CAM lowest (Table 1). Regarding the type of environment in which anopheline were collected, open areas captured the highest overall density (0.788 bites per person-hour), whereas forest and village categories accounted for 0.229 and 0.354 bites per person-hour, respectively (Table 2). However, both forest and open areas captured a broader number of anopheline species (N=9) as compared to the villages (N=6). The Correspondence Analysis showed that An. darlingi was the only species t h a t w a s strongly associated with the village environment category, although it was also collected in high density in the open areas (Table 2, Figure 2). This analysis also demonstrated that Anopheles aquasalis, An. braziliensis, An. intermedius, An. nuneztovari, and An. oswaldoi were all associated with open areas. An. acanthotorhynus/nimbus, An. mediopunctatus s.l., and An. triannulatus s.l. were strongly associated with forest (Table 2, Figure 2). The majority of all anopheline species collected were captured during the 05:00-7:00 and 18:00-22:00 time periods (0.706 and 0.686 bites per person-hour, respectively) (Table 3). However, even with lower densities, the range of anopheline species collected during the day was non-negligible, with five to seven species collected for the 09:00-11:00 and 15:00-17:00 ranges, compared to nine and ten species for the 05:00-07:00 and 18:00-22:00 ranges, respectively (Table 3). Anopheles aquasalis, An. intermedius, An. mediopunctatus, and An. triannulatus were highly associated with the dusk-nighttime collection periods, whereas An. darlingi, An. nuneztovari, and An. braziliensis were collected during both dusk-nighttime and dawn sampling periods. Anopheles aquasalis, An. braziliensis, An. darlingi, and An. triannulatus were also collected in low numbers during the day (09:00-11:00; 15:00-17:00) (Table 3, Figure 3). There was a strong association of An. acanthotorhynus/nimbus and
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especially An. oswaldoi to daytime biting (09:00-11:00; 15:0017:00) (Table 3, Figure 3). DISCUSSION This study is the first to report on the biting habits of a range of anophelines that may play a role in malaria transmission from six localities throughout French Guiana. Sampling performed in three types of environments yielded ten species out of the 25 listed for the territory (Floch and Abonnenc 1951, Degallier and Claustre 1980) (www. mosquitocatalog.org). Anopheles darlingi was the most abundant and widely distributed, being collected at each study locality, confirming its range from coastal areas to deep forest environments. This result is not unexpected as previous papers have also described a wide range of breeding habitat types for this species. Anopheles darlingi presence is often related to rivers and forests (Mouchet et al. 2004, Sinka et al. 2010, Hiwat and Bretas 2011) but has also been recorded i n savannahs and swamps (Pajot et al. 1977, Claustre et al. 2001, Povoa et al. 2006, Girod et al. 2011) as well as humanaltered environments (Tadei et al. 1998, Vittor et al. 2006). Ecological data on the other anopheline species are still scarce but our observations agree with what is known a b o u t t h e ecology of these mosquitoes. Indeed, An. aquasalis, whose breeding sites are mainly characterized by brackish water (Mouchet et al. 2004), was found on the coastal collection sites of Kourou and Matoury. Anopheles nuneztovari is well known to breed in sunlit small to medium-sized pools in flooded areas filled with vegetation (de Barros et al. 2007, Montoya-Lerma et al. 2011). This typology is encountered in many localities in French Guiana, from coastal to riparian and inland collection sites explaining the wide distribution of An. nuneztovari across the territory (Pajot et al. 1978, Girod et al. 2008, Berger et al. 2011, Dusfour et al. 2012a, 2012b). Anopheles oswaldoi was mainly found in Camopi, the most forested site, which Figure 2. Two-dimensional ordinations of the two-dimensional correspondence analysis showing the relationship between collected anopheline species (raw categories. bold. square dots) and the ecology of collection sites (column categories. circle dots). The smaller the distances between points, the “stronger” their associate with points of a certain category positioned close to each other are similar with regard to the pattern of relative frequencies across the other category. DAR: An. darlingi, BRA: An. braziliensis, INT: An. intermedius, TRI: An. triannulatus, NUN: An. nuneztovari, OSW: An. oswaldoi, ACA: An. acantothorhynus/nimbus, MED: An. mediopunctatus, AQU: An.aquasalis, ARG: An. argyritarsis.
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207 Figure 3. Two-dimensional ordinations of the three-dimensional correspondence analysis showing the relationship between collected anopheline species (raw categories, bold, square dots) and the time of sites (column categories, circle dots). Dimension 1 plus 2 display 98.59% of the variance. The smaller the distances between points, the “stronger” their associate, with points of a certain category positioned close to each other similar with regard to the pattern of relative frequencies across the other category. DAR: An. darlingi, BRA: An. braziliensis, INT: An. intermedius, TRI: An. triannulatus, NUN: An. nuneztovari, OSW: An. oswaldoi, ACA: An. acantothorhynus/ nimbus, MED: An. mediopunctatus, AQU: An. aquasalis, ARG: An. argyritarsis.
corroborates its preference for primary forest (Floch and Abonnenc 1947, de Barros et al. 2007, Hiwat et al. 2009). Anopheles intermedius has been described as sylvatic or perisylvatic and zoophilic (Floch and Abonnenc 1951, Forattini 1962, Zimmerman et al. 2006, Galardo et al. 2007). Its distribution is known to be territory-wide in French Guiana and was encountered only in the two inland localities Cacao and Camopi during the current study. Its zoophilic behavior may be explain by sampling bias as collections were only made by human landing method. Anopheles triannulatus breeding sites have been linked to large sunlit stagnant water ponds containing floating vegetation corresponding to fish ponds, natural depressions (Floch and Abonnenc 1951, de Barros et al. 2007), or flooded areas in riverine sites (Hiwat et al. 2009). The range of potential breeding sites explains its presence in many sites where permanent or temporary flooded areas are recorded and in Cacao where fish breeding is well developed. Beyond species presence, the current study also investigated the biting patterns of anophelines within each collection site. Results showed An. darlingi to bite mainly at dusk-night and dawn sampling periods in both open and village settings. This report supports previous characterizations of An. darlingi biting preferences such that early evening through morning periods had the highest abundance with specific biting modalities according to location and time of year (Pajot et al. 1977, Voorham 2002). Daytime activity has also been previously reported in forest camps by Floch (1954). Nighttime biting and preference for village settings increase its contact with humans and favors malaria transmission, but also supports the use of mosquito nets and indoor residual spraying as effective control strategies where An. darlingi occurs (Hiwat et al. 2012, Martins-Campos et al. 2012). The observation of daytime biting activity is interesting since some malaria transmission patterns are far from clear. For example, two annual malaria transmission peaks are recorded in Camopi. One is related to both Plasmodium
falciparum and P. vivax in the early rainy season (January) and the other one linked to P. vivax infection at the end of the rainy season (June) (Stefani et al. 2011). Whereas the peak in June in the rainy season corresponds to the presence of An. darlingi in the village, the second does not correlate with the presence of this main suspected vector (Girod et al. 2011). This observation suggests transmission by other anopheline species such as An. nuneztovari (Stefani et al. 2011) or An. neivai (Pajot et al. 1978), or that transmission occurs outside the village, in crop fields, or in the forest where people are hunting or fishing (this study). Those hypotheses are even reinforced by the presence of P. falciparum positive specimens in Camopi (An. oswaldoi s.l.) and also in Saint Georges de l’Oyapock (An. nuneztovari and An. intermedius) and Cacao (An. intermedius) (Dusfour et al. 2012a). Anopheles aquasalis, An. intermedius, and An. nuneztovari were all strongly associated with collections from open areas, whereas An. triannulatus was associated with forest settings. All species were collected during the day sampling period except An. nuneztovari which was strictly collected at the dusk-night and dawn times. The roles of these species in pathogen transmission depends upon the behavior of t h e human population in the surrounding area that brings them in contact with the adult mosquitoes. Human population behaviors and malaria prevention measures vary in French Guiana as the territory is composed of multicultural communities whose differences are characterized by habitat, behavior, and socio-economic status. All current malaria prevention and vector control measures in French Guiana are based on the presumption that An. darlingi is a primary vector throughout the country and the presumptive nocturnal biting activity of anophelines. Little consideration has been given to other potential vectors and their roles in malaria transmission on the habits of people at risk. Our study represents a general survey of adult anophelines throughout French Guiana and
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