Sandfly Fauna (Diptera: Psychodidae, Phlebotominae) of São José Farm, Carmo District, State of Rio de Janeiro, Brazil

Abstract

Aiming to compare and update the sand fly fauna of São José farm, Carmo District, Rio de Janeiro State, Brazil, and considering the environmental changes occurred, the biology and ecology of the local sandfly species were examined twelve years later as a complementary study carried. Captures were made in the intra, peridomicile and in the woods, from 6 p.m. to 6 a.m. 1210 sandflies of fifteen species of the Lutzomyia were captured: L. intermedia, L. whitmani, L. lenti, L. aragaoi, L. cortelezzii, L. quinquefer, L. carrerai carrerai, L. davisi, L. lanei, L. fischeri, L. monticola, L. ayrozai, L. sordellii, L. lutziana, L. sp and two species of the Brumptomyia Kind: B. brumpti and B. cardosoi. In 1994 and 1995 were collected 4603 samples from six species of the former genus and three of the second. Lutzomyia intermedia was predominant, in the intra and in the peridomicile, in both periods. B. bumpti, collected only in the recent prevailed i n the woods. Six species implicated as vector of Leishmania: L. intermedia, L. whitmani, L. ayrozai, L. fischeri, L. davisi, L. carrerai carrerai and L. migonei have been collected in the area, however, this last only in the previous study.

Key words
Carmo; sandfly; São Jose farm; vector

INTRODUCTION

About 544 species of sandflies are found in the Americas, of which 527 presently exist and 17 are fossils (Galati 2018).

In Brazil, sandflies (Diptera: Psychodidae, Phlebotominae) of the genus Lutzomyia França, 1924 act as the invertebrate hosts for the species of the genus Leishmania Ross, 1903 (Kinetoplastida: Trypanosomatidae) that cause leishmaniasis in humans and other mammals (Young & Duncan 1994).

In the southeast region, 125 species of sandflies have been recorded so far. According to Carvalho et al. (2014), 65 species are present in the state of Rio de Janeiro. Lutzomyia (Nyssomyia) intermedia (Lutz and Neiva, 1912) is the main vector of Leishmania (Viannia) braziliensis Vianna, 1911 that causes American tegumentary leishmaniasis (ATL) in this State (Alves 2007).

According to the Ministério da Saúde (2019), 218.281 confirmed cases of ATL were registered in whole of Brazil from 2007 to 2017. Of these, 702 cases were reported in the State of Rio de Janeiro.

The prevalence of L. intermedia over other species of sandflies was registered in different regions of the State of Rio de Janeiro (Menezes et al. 2002, Aguiar & Vieira 2018).

Studies indicate that the shelters for domestic animals in rural areas help in the colonization of sandflies as they find food in these places (Alves 2007).

Studies on the impact of environmental, natural or those resulting from anthropic changes in the ecology of sandflies have been carried out in different regions of the country (Forattini 1960, Lima et al. 1988, Rangel et al. 1990, Menezes et al. 2002).

In the district of Carmo, nine cases of tegumentary leishmaniasis were notified from 2000 to 2006, eight of them occurred in the rural area. The occurrence of the first human case in the central area of district was recorded by Alves (2007), being L. intermedia the predominant species.

In 1994, one person, from a family of four, had cutaneous leishmaniasis (CL), worked at home and had no activity at night. The description of place was made by Alves (2007).

In 2006, only one couple the man worked on the farm and the woman elsewhere. The property had no shelters with pets except a dog. Thus, the anthropic actions have been reduced over the years.

In the peridomicile there are eight fruit trees. All these trees have been preserved since 1994, which was recorded by Alves (2007) (Figures 1 and 2).

Figure 1
The house and the peridomicile where the first autochthonous cases of leishmaniasis occurred in 1994.

Figure 2
The house of 1994 in 2006, when started the second period of research of sand flies fauna of São José farm, Carmo county, RJ, Brazil.

The inhabitants reported that animals such as anteaters, lizards, monkeys, armadillos and snakes occasionally appeared in the peridomicile, which was not the case with previous work.

The present study aimed to observe the changes in the sand fly fauna and in the of Leishmania spp. in a São José Farm, district of Carmo, considering the environmental changes where it took place. To do that, results of captures carried out in the 1994 and 1995 by Alves (2007) and those between 2006 and 2007 in the same district were compared.

MATERIALS AND METHODS

Study area

The district of Carmo is located at 21º 56` 04`` S and of 42º 36` 31`` W in the physiographic zone of the Rio Paraiba do Sul marginal, bordering the districts of Cantagalo, Duas Barras, Sapucaia, Sumidouro and the State of Minas Gerais (Fig. 3).

Figure 3
Localization of Rio de Janeiro State, Brazil and Carmo County with its neighboring municipalities.

According to Köppen-GeIger classification (2016), adapted to Brazil, the region of Carmo is Aw (high temperatures rains in the summer), with an average temperature between 19°C and 28°C and the average of rainfall inferior to 2000 mm/per year. The vegetation which covers the district is likewise those found in Mata Atlântica (INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA, [IBGE] 2016).

Collection of specimens

Sandflies were collected at São José farm, at the same location as that in the first study (1994/1995), and the same methodology was used in both studies by Alves (2007). For clarification and mounting of the specimens, the technique of Young & Perkins (1984), modified by Aguiar et al. (1993), was used. The identification of the species of the Lutzomyia França, 1924 and Brumptomyia França & Parrot, genera was undertaken in accordance with Young & Duncan (1994) and Forattini (1973), respectively.

Statistical analysis

We used the diversity indexes of Shannon and Simpson and applied the tests to identify significant differences between the two study periods (Rodrigues 2014). The analysis of the data was performed using the (ISA) and the standardized species abundance index (SISA), (Roberts & Hsi 1979) to classification based on the absolute abundance ISA and SISA were calculated using Microsoft Excel 2013 (Microsoft Corp., Redmond, WA, USA) and converted values between 0 and 1 (SISA), based on the following equations:

$$ISA=(a+RI)/k$$

$$SISA=(c-ISA)/(c-1)\text{where:}K=\text{capture number}$$

a = value obtained by multiplying the species absence number (NAE) in k catches per c.

c = value of the highest position of the species in k catches plus 1.

RJ = sum of classifications in each species

The species were considered highly abundant when the SISA value was near to 1.0. This calculation was applied to all captured sandflies and to each type of collection performed in both periods.

RESULTS

From August 2006 to July 2007, 17 sandfly species were captured at São José farm, of which 15 belonged to the genus Lutzomyia and 2 species were from the genus Brumptomyia. The species list was published by Carreira-Alves (2008).

L. intermedia was the predominant species in all of the locations (93.3%). The manual aspiration, 38.6% of the specimens were collected in the intradomicile and 61.4% in the peridomicile (22.3% from the external of the residence, 39.1% in the tree trunks). In the forest, where the number of female specimens were slightly higher than of males, only four. In the collections with Castro aspirator, in both periods, the male was predominant. In 1994/95, the proportion of male / female specimens was 1.9: 0.52 and 1.14: 0.87 in 2006/07. It is observed that the number of males was more significant in the first period, while that of females was in the second period. In relation to the peridomicile, we found the highest value among males 17.7, while the lowest was among females (0.06) in 1994/95. In 2006/07, the ration between, the female / male ratio was higher (0.19) and the male / female ratio, lower (5.28) (Table I).

Table I
Number of sand flies species collected with Castro captor and CDC light trap on São José farm, District of Carmo, State of Rio de Janeiro, Brazil, from August to July in the periods of 1994/1995 and 2006/2007.

Species	Manual Gathering *				CDC Trap *					Manual Gathering **				CDC Trap **
	Intradomicile		Peridomicile		Peridomicile		Woods		M/F	Intradomicile		Peridomicile		Peridomicile		Woods		M/F
	M	F	M	F	M	F	M	F	%	M	F	M	F	M	F	M	F	%
Lutzomyia intermedia	480	248	2871	162	406	341	24	22	98.9	105	92	264	50	362	232	9	15	93.3
Brumptomyia brumpti														1		15	14	2.5
L. aragaoi																8	7	1.2
L. cortelezzii															3		4	0.6
L. whitmani	2		10		3		4		0.4	1				2		2		0.4
L. . ayrozai				1					0.02							2	2	0.3
L. davisi																4		0.3
L. fischeri																	3	0.2
L. monticola														1		2		0.2
L. lanei																	2	0.2
L. quinquefer			1						0.02						2			0.2
L. carrerai carrerai														1				0.1
L. lenti		3	2	1	4	2			0.3						1			0.1
L. lutziana																1		0.1
L. sordellii																1		0.1
L. migonei.			2		4	1		1	0.2
Lutzomyia sp.																	1	0.1
B. avellari					2		4		0.13
B. cardosoi																1		0.1
B. guimaraesi								1	0.02
B. nitzulescui							1		0.02
Total	482	251	2886	164	419	344	33	24	100	106	92	264	50	367	238	45	48	100

• M = Male; F = Female.
  * = 1994/1995; ** = 2006/2007.

In the collections with CDC trap in the peridomicile the highest male / female ratio occurred in 2006/07 (1.56), while the lowest (0.6) occurred in the forest in this same period, when the females were more numerous than males, while for B. brumpti the most collected species was 1.07: .69. In total, the forest collections were balanced (0.9: 1.0). In the intradomicile, L. intermedia was the most common species with a frequency of 99 % which reached a peak in March 1995 and August 2006, when the temperature was of 25°C and 24°C, respectively (Fig. 4). The second L. intermedia peak occurred in September, from both periods, with 30 and 18 sandflies collected in each of them, with a temperature of 21º C and 20º C. In 1994/95, there was a higher frequency in the hot and wet period (January, February and March) with 158 sandflies, representing 63.7 % of the total and the lowest occurred in cold and dry months (June, July and August) with 16 sandflies (6.45%). In 2006/07, the highest frequency was recorded in the cold and dry period, with 53 sandflies (57.6%) and the lowest in the warmer and wetter months, with only 12 (13%) specimens. B. brumpti was the second most common species, with a recorded of 2.5%, when all the sites of capture were observed. In the frequency of this species was of 31.2%, followed by L. intermedia with 25.8%.

Figure 4
Total of females’ specimens of L. intermedia collected with Castro captor, in relation to the temperature from August to July 1994/95 and 2006/07 on the São José farm, Carmo county, RJ, Brazil.

Comparing the years 1994/95 and 2006/07, it was found that L. intermedia remained with the largest number of specimens, which in previous years was even higher 98.9%. L. migonei representing 0.2% was not found in this posterior phase study (Table II).

Table II
Quantitative comparison and composition of the sandfly fauna of São José farm, District of Carmo, State of Rio de Janeiro, Brazil, from August 1994 to July 1995 and August 2006 to July 2007.

Species/Year	1994/1995	%	2006/2007	%
Lutzomyia intermedia	4554	98.9	1129	93.3
Brumptomyia brumpti			30	2.5
L. aragaoi			15	1.2
L. whitmani	19	0.4	5	0.4
L. lenti	12	0.3	1	0.1
L. migonei	8	0.2
L. cortelezzii			7	0.6
B. avellari	6	0.1
L. ayrozai	1	0.02	4	0.3
L. davisi			4	0.3
L. fischeri			3	0.2
L. monticola			3	0.2
L. quinquefer	1	0.02	2	0.2
L. lanei			2	0.2
L. carrerai carrerai			1	0.1
L. lutziana			1	0.1
L. sordellii			1	0.1
B. guimaraesi	1	0.02
B. nitzulescui	1	0.02
Lutzomyia sp.			1	0.1
B. cardosoi			1	0.1
Total	4603		1210

As seen in Table III, a total of specimens were collected in 1994/95 and 2006/07 using a Castro aspirator, presenting a SISA of 0.875 and specimens collected in 1994/95 and banana tree with an abundance of 200 specimens being captured in 2006/07, followed by L. whitmani, which was only collected in 2006/07 inside the house, with a very low index (0.021) and only one specimen collected. L. intermedia was predominant in all locations and periods of collection, but was more abundant in 1994/95 than in 2006/07.

Table III
Total (T) of sand flies by places of captures with Castro captor in inner and outer wall of the house, in tree trunk, banana tree and sty. Standartized index of species Abundance (SISA) and Rank (R) in São José farm, municipality of Carmo, State of Rio de Janeiro, Brazil, from August to July in the periods of 1994/1995 and 2006/2007.

	Inner of the house*			Outer of the house*			Tree trunk*			Sty*
Species	T	SISA	R	T	SISA	R	T	SISA	R	T	SISA	R
L. intermedia	728	0.833	1	258	0.604	1	1432	0.875	1	1343	0.771	1
L. lenti	3	0.042	2	1	0.021	2	2	0.042	3	1	0.042	2
L. whitmani	2	0.021	3	1	0.021	2	9	0.083	2	´´	´´	´´
L. migonei	´´	´´	´´	´´	´´	´´	1	0.028	4	1	0.021	3
L. ayrozai	´´	´´	´´	´´	´´	´´	´´	´´	´´	1	0.021	3
Total	733			260			1444			1346
	Inner of the house**			Outer of the house**			Banana Tree**
Species	T	SISA	R	T	SISA	R	T	SISA	R
L. intermedia	197	0.167	1	114	0.542	1	200	0.667	1
L. whitmani	1	0.021	2	´´	´´	´´	´´	´´	´´
	931			374			1644
* =1994/1995; ** = 2006/2007.

Analyzing the statistical results of internal and external walls of the residence, we observed that L. intermedia was more abundant in the interior of the wall (0.833) and in the external (0.604) in 1994/95.

In Table IV, a total of 1.511 specimens were collected using light traps. L. intermedia was the more abundant species in all locations of collection, especially in the peridomicile and stye (0.701 and 0.618, respectively), followed by B. brumpti (0.324). L. aragaoi (0.167) and L. davisi (0.106) in the forest. L. migonei, which was collected in 1994/95 in the stye and forest, 0.014.

Table IV
Total (T) of sand flies by places of captures with CDC light traps in Sty, Forest and Peridomicile. Standarsed Index of species abundance (SISA) and Rank (R) in São José farm, municipality of Carmo, State of Rio de Janeiro, Brazil, from August to July in the periods of 1994/1995 and 2006/2007.

	CDC light Sty*				CDC light Forest*				CDC light Peridomicile**				CDC light Forest**
Species	T	SISA	R		T	SISA	R		T	SISA	R		T	SISA	R
L. intermedia	747	0.618	1		46	0.25	1		585	0.701	1		24	0.394	1
L. lenti	6	0.049	4		´´	´´	´´		1	0.035	5		´´	´´	´´
L. migonei	5	0.103	2		1	0.014	6		´´	´´	´´		´´	´´	´´
L. whitmani	3	0.028	6		4	0.056	4		2	0.049	4		2	0.032	11
L. cortellezzii	´´	´´	´´		´´	´´	´´		3	0.063	3		4	0.065	6
L. quinquefer	´´	´´	´´		´´	´´	´´		2	0.049	4		´´	´´	´´
L. carrerai carrerai	´´	´´	´´		´´	´´	´´		1	0.021	7		´´	´´	´´
L. monticola	´´	´´	´´		´´	´´	´´		1	0.083	2		2	0.032	11
B. brumpti	´´	´´	´´		´´	´´	´´		1	0.028	6		29	0.324	2
B. avellari	2	0.083	3		4	0.083	2		´´	´´	´´		´´	´´	´´
B. guimaraesi	1	0.033	5		2	0.075	3		´´	´´	´´		´´	´´	´´
B. nitzulescui	´´	´´	´´		1	0.035	5		´´	´´	´´		´´	´´	´´
L. aragaoi	´´	´´	´´		´´	´´	´´		´´	´´	´´		15	0.167	3
L. davisi	´´	´´	´´		´´	´´	´´		´´	´´	´´		4	0.106	4
L. fischeri	´´	´´	´´		´´	´´	´´		´´	´´	´´		4	0.074	5
L. lanei	´´	´´	´´		´´	´´	´´		´´	´´	´´		2	0.046	7
L. ayrozai	´´	´´	´´		´´	´´	´´		´´	´´	´´		4	0.042	8
L. lutziana	´´	´´	´´		´´	´´	´´		´´	´´	´´		1	0.042	8
L. sordellii	´´	´´	´´		´´	´´	´´		´´	´´	´´		1	0.042	8
B. cardosoi	´´	´´	´´		´´	´´	´´		´´	´´	´´		1	0.023	13
Total	764				58				596				93
* = 1994/1995; ** = 2006/2007; L. = Lutzomyia; B.= Brumptomyia.

When we compare the diversity of the phlebotomine fauna captured in the forest, we can establish that: In 1994 and 1995, sand flies were collected during four months, totalizing five species. In October, a peak of L. whitmani occurred with four specimens, followed by L. migonei in a unique way, at a temperature of 23º C. We were struck by the fact that during the other three months only phlebotomines of the genus Brumptomyia were collected. In September and May B. avellari were collected, with one specimen, in the first month and three in the other, with 21º C and 20º C in both months respectively, while in July, B. nitzulescui and B. guimaraesi were collected with a single specimen of each and with the lowest temperature (19º C) during all four months. This demonstrates a preference for cold and dry weather for species of this genus. It is also observed that in August at a temperature of 15º C, no phlebotomes were captured.

In 2006 and 2007, phlebotomes were registered during nine months, with a finding of twelve species, being ten of them of the genus Lutzomyia and two of them of Brumptomyia. It is worth pointing the fact that B. brumpti and L. aragaoi were found in eight and five months each species. Besides, B. brumpti presented two peaks, both with eight phlebotomes, in February and June, at a temperature of 27º C and 18º C respectively, in the hot and humid as well as cold and dry periods, followed by a third peak, with six specimens, in April, with a temperature of 24º C. It was also recorded that in January and November (28ºC) was the highest temperature of this period, and two specimens of B. brumpti, were captured in both months.

L. aragaoi showed a peak in April, with eight phlebotomes and in February with three phlebotomes, with 24º C and 27º C, in each month. It was captured uniquely in January, when the highest temperature (28ºC) was recorded. In September, at the lowest temperature (20ºC), two specimens of L. aragaoi were captured. It is suggested this species is adapted to low and high temperature in the forest environment of the studied area.

In order to continue evaluating the diversities collected in the peridomicile with CDC trap in 1994/1995 and 2006/2007 on the São José farm, we highlight that:

In 1994/95, the CDC trap was placed in the pig pen for seven months, L. lenti, L. migonei, L. whitmani and B. avellari were collected. L. lenti was the most abundant species of all, with a peak in January, when the highest temperature (27º C) of the period was recorded. This species was ticked in February, too. In this month, the predominant species was L. migonei, being recorded the temperature of 25º C.

L. whitmani was also collected in January, but with two specimens. During the months of March, August, September, October and November, only one species of each was collected. In August and September, the coldest and dryest ones with 15º C and 21º C, respectively, B. avellari were collected, while L. migonei occurred in March and November, with one and two phlebotomes in each month, at 25º C and 26º C. In October, at a cooler temperature, 23° C, L. whitmani was collected.

In 2006/2007, in the peridomicile and with CDC trap four species were collected, two of them in the cold and dry period (June and August), another during the hot and humid period (February) and the last one in November.

In February, three species were collected: L. lenti, L. cortelezzii and L. whitmani, being one specimen of the first and two of the latter, in November it was one specimen of L. carrerai carrerai and two of L. quinquefer, while in June and August one of B. brumpti and L. monticola in each. L. lenti was caught in both periods and in February, as so was L. whitmani, however in January and October at that time. Considering the temperature, the lowest one was 18º C registered in June, being B. brumpt to be collected and the highest 28 ° C in November with L. carrerai carrerai and L. quinquefer collected (Fig. 5).

Figure 5
Total of diversity of species collected with CDC traps, in relation to the temperature, in peridomicile and in the forest from August to July 1994/95 and 2006/07 on the São José farm, Carmo county, RJ, Brazil.

The index of total abundance showed that L. intermedia was the most abundant species in 1994/95 (0.917) and 2006/07 (0.906) (Fig. 6).

Figure 6
Comparation of Standarsed Index Species Abundance (SISA) for L. intermedia captured with Castro captor, CDC trap in the forest and the total of all collection in São José farm, in the periods of 1994/95 and 2006/07.

The student test revealed significant differences between the predominance of L. intermedia in 1994/95 and 2006/07 in all locations of collection, except for the external wall (t = 2.014; p = 0.050042; v (GL) = 45).

DISCUSSION

The highest richness of species occurred in the woods, however, the greatest number of species occurred in the peridomicile. According to Ximenes et al. (2007), the greatest diversity of sandflies found in Alto Apodi in the State of Rio Grande do Norte, is probably due to the lowest level of environmental degradation in the mountain areas.

As observed by Alves (2007) and in the present study, L. intermedia is endowed with a great capacity of domiciliation and adaptation to the anthropic environment, at the same time that a smaller population continues to be present in a preserved area.

According to Teodoro et al. (2001a, b), the domestic animal shelters built close to the domicile and the absence of good hygiene conditions in the peridomicile, seem to favor the concentration of sandflies in this site of gathering. In our research, we observed that the frequency in both periods were basically the same, the data do not show there, because in the former period when there were animals in the peridomicile, L. intermedia was much more numerous.

In 1994/95, L. intermedia was more frequent in the summer and less frequent in winter. In 2006/07, we observed a higher frequency in winter and a lower frequency in the fall with featuring significant peaks in the months of February, August and November. This result suggests that L. intermedia managed to ideally adapt for its own reproduction, maintenance and survival.

Although L. intermedia had been collected in considerable amount and had been predominant during all the period, its frequency was not regular, corroborating observation of Forattini et al. (1976) and Santos-de-Marco et al. (2002).

It was evident that the seasonality did not represent a barrier to the adaptation and survival of L. intermedia to the anthropic place, this sandfly was more frequent in summer what increases the probability of the transmission had been occurred during this season.

Carreira-Alves et al. (1998) reported the finding of L. intermedia and L. migonei, in an area with occurrence of visceral leishmaniasis, in Barra da Tijuca, west of the city of Rio de Janeiro. L. intermedia was the predominant species. In addition, these authors called attention to the fact that L. longipalpis was not found. Species is the main vector of Le. (Leishmania) infantum chagasi, the etiologic agent of visceral leishmaniasis.

L. migonei was found naturally infected with Leishmania (V.) braziliensis in Jacarepagua, municipality of Rio de Janeiro by Pita-Pereira et al. (2005). Considering this and other literatures this species can be considered as secondary vector of cutaneous leishmaniasis in the State of Rio de Janeiro.

Alves (2007) registered the presenc of L. migonei in Carmo, except for the intradomicile, but with a low frequency. However, this sandfly was not found, abandonment by may have contributed to the migration of the population of L. migonei that existed there to a nearby secondary forest.

In this study, we have recorded the presence of armadillo burrows, an animal which is used as a source of feeding for some species of sandflies, among them, B. brumpti which was most of the time in the woods and next to armadillo burrows (Aguiar & Medeiros 2003).

B. brumpti occurred with an expressive quantity in summer, mainly in February. In this

month, it was recorded an average temperature of 27º C, which indicates a preference for a warm and humid period. It could be seen that a significant number of the sandflies captured in the woods belonged to Brumptomyia, confirming its sylvestral behavior (Aguiar & Soucasaux 1984).

The literature shows the occurrence of B. brumpti in domestic, in an endemic area of cutaneous leishmaniasis in the State of Paraná, where it was captured with light trap peridomicile as found Teodoro et al. (1993).

Aguiar & Vieira (2018) otherwise showed that B. avellari can be found in these ecotypes. In the study, this species was collected in the sty, which would explain the absence of this species in this study, because this shelter was not investigated. Additionally, in 1994 and 1995, there were B. guimaraesi and B. nitzulescui in the forest while B. cardosoi was found in this same location. Aguiar & Vieira (2018) did not report as one of the main habitats of this species.

In this study, among the species of Lutzomyia which have any relation with burrows of animals, namely armadillo, we can cite: L. aragaoi, L. ayrozai, L. davisi, L. lutziana, from these the second and third the are considered to be vectors Leishmania (Rangel & Lainson 2003, Aguiar & Vieira 2018).

L. aragaoi was the third species captured, and a preference for sylvestral environment is one of its characteristics. It is specifically found in burrows of wild animals (Dasypodidae), having an ample distribution in Brazil (Aguiar & Vieira 2018). On São José farm, this species was only collected in the woods and than 3 metres of burrows, leading us to believe that the dispersion of this species is superior to this distance. Presently, there is no record that L. aragaoi is taking part in a transmission cycle of Leishmania.

L. ayrozai is recognized as a highly anthrophilic species in the mountainous region of the southeast of Brazil (Mayrinks et al. 1979), where it is more frequent in warm and humid months, reducing its density in cold and dry months. Rangel & Lainson (2003) report that L. ayrozai can be a probable transmitter of Leishmania (Viannia) naiffi among armadillos, known as reservoirs of this species of Leishmania in Amazonian region.

In 2006, this sand fly, together with L. davisi, were present only in the woods.

In relation to the L. davisi, the literature reports that this sand fly is known as the potential vector of Le. (V.) braziliensis and Le. naiffi in Brazil, being found infected in the nature with both protozoans (Grimaldi et al. 1991).

Alves (2007) did not mark the occurrence of L. aragaoi and L. davisi, or the burrows of wild animals when he studied this same area (J.R. Carreira-Alves, personal communication). It became clear that the armadillo burrow had an important role in the dispersion and distribution of the local sandfly fauna (Aguiar & Vieira 2018).

Although in Carmo L. whitmani had been collected in small quantity it is important to observe that this sandfly is seen as the vector of Le. (V.) braziliensis in different regions of the Brazil (Grimaldi et al. 1989, Queiroz et al. 1991). It should be also mentioned its association to the transmission of Le. (V.) shawi.

L. carrerai carrerai one of the vectors of Le. (V.) braziliensis in Brazil and Bolivia (Le Pont et al. 1988), has also the capacity to transmit Le. (Leishmania) amazonensis (Lainson and Shaw 1972), to hamster (Ryan et al. 1987). Alves (2007) did not found L. carrerai carrerai in the previous study. So, the finding in the present study may be seen as the consequence of a process of sandfly fauna recomposition.

Saraiva et al. (2010) reported the first record of Leishmania braziliensis infecting a female of L. cortelezzii in the State of Minas Gerais.

In our study, this species was the second most collected in light traps placed near the houses and was also found in the forest.

Considering that, currently, the first animal pens were removed from this site of collection and this species of sandfly have not been registered by Alves, L. cortelezzii may have migrated from the existing forest about 40 meters from the house, which would have showed the spread of this species.

Carvalho et al. (2014) reported that L. fischeri was found naturally infected with Le. (V.) braziliensis in the southeast and south of Brazil. In 2006/07, L. fischeri was only collected in the forest in a very low frequency, results that agreed with those reported by Forattini (1973). This species was most frequent in the summer and was not collected by Alves (2007).

Lainson (1983) suggested that L. fischeri can have adapted to the anthropic environments; however, it also transmits Le. (V.) braziliensis to the wild animals in the secondary forests.

According to the literature the species L. intemerdia, L. whitmani, L. migonei, L. ayrozai, L. davisi and L. carreirai carreirai, collected in both studies, are Leishmania vectors.

It is Worth noting that five species are considered vectors of cutaneous leishmaniasis in Brazil: L. intemerdia, L. whitmani, L. davisi, L. ayrozai and L. carreirai carreirai, which correspond to 94.4 % of the specimens captured in the 2006, with 93.3 % being from L. intermedia.

L. lenti was captured inside the residence by Alves (2007). Although it has been captured on a large scale in this place, there is no evidence that this species is a vector of leishmaniasis in Brazil (Andrade Filho et al. 2001).

However, this was the first record of L. lenti in the mountainous region of the State of Rio de Janeiro (Alves 2007).

Alves (2007) reported that L. quinquefer was collected in the external wall. In our study, this species was also collected in the peridomicile, but in a banana tree using a light trap. In both the studies, this species was collected in low frequency in the summer, suggesting its preference for hot and humid climates.

Rangel et al. (1990) reported that L. quinquefer was collected only in dogs and horses in Mesquita, State of Rio de Janeiro, an area with cases of ATL in humans and dogs caused by Le. (Viannia) braziliensis. Menezes et al. (2002) observed that, in this area, some specimens of L. quinquefer were attracted to human beings in forest habitats.

De Souza et al. (1995) studied the sandfly fauna of São José do Vale do Rio Preto, State of Rio de Janeiro, observed various L. quinquefer specimens which fed from a gecko on the external wall.

L. quinquefer can belong to a group of sandflies that feeds off cold blooded animals (E.A.B. Galati, unpublished data). However, when Galati et al. (1996) studied the sandfly fauna from Gorguinho, Mato Grosso do Sul, they collected a sample of L. quinquefer using human bait, probably by accident.

Also, Brazil & Brazil (2003) and Brazil et al. (2006) collected various species of sandfly, including L. quinquefer, which was believed to have a preference to feeding off cold blooded animals.

Alves (2007) did not report the occurrence of L. monticola, but collected male specimens in the peridomicile and in the forest using light traps. In the forest, specimen was collected in February, while the others were collected in March.

We also collected a male specimens of L. monticola of peridomicile in August 2006, since this environment is not the preferred habitat for these species, unless there are domestic animal shelters (Aguiar & Medeiros 2003).

Considering the revision made by Carvalho et al. (2014), we registered for the first time the collection of the above mentioned species in the municipality of Carmo.

Additionally, we call attention to the record of the species B. avellari and B. nitzulescui as new in the mountain region of State of Rio de Janeiro.

Likewise, we point out as new records for Carmo nine species of the genre Lutzomyia: L. fischeri, L. lanei, L. lutziana, L. monticola, L. aragoai, L. cortelezzii, L. sordellii, L. carrerai carrerai and L. davisi. In addition, the latter two species are cited for the first time in the mountain region of the State of Rio de Janeiro. As pointed out by Alves 2008, Carreira-Alves 2008.

In their research, Aguiar & Vieira (2018) pointed out the main habitats of sand flies in Brazil. We highlight the following, the location and the species that were collected in our study in environments different from those recorded by the authors.

In tree trunk were collected L. intermedia and L. lenti; while in the stye L. ayrozai and B. guimaraesi and finally in forest we recorded the presence of B. avellari, B. brumpti, B. cardosoi, B. guimaraesi, B. nitzulescui, L. aragaoi, L. ayrozai, L. cortelezzii, L. davisi, L. fischeri, L. lanei, L. lenti, L. migonei, L. monticola, L. quinquefer, L. sordellii and L. whitmani (Alves 2007, 2008, Carreira-Alves 2008).

CONCLUSION

The abundance was relatively greater in 1994/95 and showed that the presence of styes influenced the collection of specimens, besides revealing L. intermedia high preference for pigs and their shelters. In 2006/07 and showed that the removal of domestic animal shelters modified the sandfly fauna and confirmed the high adaptability of L. intermedia, to the changes made by man in the studied location.

It has been proved yet that these modifications influenced the dispersion and distribution of sandflies fauna existing in the woods. At the same time, it was formed a marginal area with the necessary ecological conditions for the species of peridomicile. In relation to that, it can be supposed that in 2006/07 there was a major diversity of the suspicious species as vector of Leishmania.

In general, our data can help to improve the public health services and develop effective measures for the control of leishmaniasis vectors in Carmo county and in the mountainous region of Rio de Janeiro State.

ACKNOWLEDGMENTS

We would like to thank Mr. Paulo Lemgruber and his wife, owners of São José farm, for their support and also to Mr. João Sebastião Marques and family. The Heloisa Maria Nogueira Diniz the production and processing of images. To the reviewers for their valuable collaboration.

REFERENCES

• AGUIAR GM & MEDEIROS WM. 2003. Distribuição Regional e Hábitats das Espécies de Flebotomíneos do Brasil. In: Rangel EF & Lainson R (Eds), Flebotomíneos do Brasil. Rio de Janeiro, Fundação Oswaldo Cruz, p. 207-255.
• AGUIAR GM, MEDEIROS WM, SANTOS TG, KLEIN AF & FERREIRA VA. 1993. Ecology of sandflies in a recente locus of cutaneous leishmaniasis in Paraty, litoral do Rio de Janeiro State (Diptera: Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 88: 339-340.
• AGUIAR GM & SOUCASAUX T. 1984. Aspectos da ecologia dos flebótomos do Parque Nacional da Serra dos Órgãos, Rio de Janeiro. I Frequência mensal em isca humana (Diptera, Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 79: 197-209.
• AGUIAR GM & VIEIRA VR. 2018. Regional distribution and habitats of Brazilian Phlebotomine Species. In: Rangel EF and Shaw JJ (Eds), Brazilian Sandflies. Rio de Janeiro, Springer, p. 251-298.
• ALVES JRC. 2007. Espécies de Lutzomyia França (Diptera: Psychodidae, Phlebotominae) em Área de Leishmaniose Tegumentar no Município de Carmo, RJ, Brasil. Neotrop Entomol 36: 593-596.
• ANDRADE-FILHO JD, VALENTE MB, ANDRADE WA, BRAZIL RP & FALCÃO AL. 2001. Flebotomíneos do Estado de Tocantins, Brasil (Diptera: Psychodidae). Rev Bras Med Trop 34: 323-329.
• BRAZIL RP & BRAZIL BG. 2003. Biologia de Flebotomíneos Neotropicais. In: Rangel EF and Lainson R (Eds), Flebotomíneos do Brasil. Rio de Janeiro, Fundação Oswaldo Cruz, p. 257-274.
• BRAZIL RP, PASSOS WL, FUZARI AA, FALCÃO AL & ANDRADE-FILHO JD. 2006. The peridomiciliar sand fly fauna (Diptera: Psychodidae) in areas of cutaneous leishmaniasis in Além Paraíba, Minas Gerais, Brazil. J Vector Ecology 31: 418-420.
• CARREIRA-ALVES JR. 2008. Espécies de Phlebotominae (Diptera: Psychodidae) da fazenda São José, Município de Carmo, Estado do Rio de Janeiro, Brasil. Ph. D Resume of dissertation. Rev Patol Trop 37: 371-372.
• CARREIRA-ALVES JR, CUNHA SP, SOUZA MB, MEIRA AM, PONTE CS & ANDRADE MV. 1998. Research phlebotominae (Diptera: Psychodidae) in a district called “baixada de Jacarepaguá”, in County of Rio de Janeiro, RJ, Brasil. Mem Inst Oswaldo Cruz 93: 342.
• CARVALHO BM, DIAS CM & RANGEL EF. 2014. Phlebotomine sand flies (Diptera, Psychodidae) from Rio de Janeiro State, Brazil: species distribution and potential vectors of leishmaniasis. Rev Bras Entomol 58: 58-87.
• DE SOUZA MB, MARZOCHI MCA, CARVALHO RW, CONCEIÇÃO NF & PONTES CS. 1995. Flebótomos em áreas de ocorrência de leishmaniose tegumentar no município de São José do Vale do Rio Preto, Rio de Janeiro, Brasil. Parasitol al Dia (Flap): 97-103.
• FORATTINI OP. 1960. Novas observações sobre a biologia de flebótomos em condições naturais (Diptera: Psychodidae). Arch Hyg Saúde Pública 25: 209-215.
• FORATTINI OP. 1973 Entomologia Medica. 1ª ed. Edgar Blucher EDUSP, São Paulo, 641 p.
• FORATTINI OP, RABELLO EX, SERRA OP, COTRIM MD, GALATI EAB & BARATA JMS. 1976. Observações sobre a transmissão da leishmaniose tegumentar no Estado de São Paulo, Brasil. Rev Saúde Pública 10: 31-43.
• GALATI EAB. 2018. Phlebotominae (Diptera, Psychodidae): Classification, Morphology and Terminology of adults and Identification Taxa. In: RANGEL EF & SHAW JJ (Eds), Brazilian Sandflies. Rio de Janeiro, Springer, p. 209-212.
• GALATI EAB, NUNES VLB, DORVAL MEC, OSHIRO ET, CRISTALDO G & ESPINDOLA MA. 1996. Estudos dos flebotomíneos (Diptera, Psychodidae) em área de leishmaniose tegumentar, no Estado de Mato Grosso do Sul, Brasil. Rev Saúde Pública 30: 115-128.
• GRIMALDI JR G, MOMEN H, NAIFF RD, MCMHOL-PRATT D & BARRETT TV. 1991. Caracterization and classification of leishmanial parasites from humans, wild mammals, and sand flies in the Amazon Region of Brazil. Am J Trop Med Hyg 44: 645-661.
• GRIMALDI JR G, TESH RB & MCMAHON-PRATT D. 1989. A review of the geographic distribution and epidemiology of the leishmaniasis in the New Word. Am J Trop Med Hyg 41: 687-725.
• IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2016. Cidades. Disponível em: (http://www.cidades.ibge.gov.br/v3/cidades/municipio/3301207). acesso em 15/Out/2016.
  » http://www.cidades.ibge.gov.br/v3/cidades/municipio/3301207
• KÖPPEN W & GEIGER R. 2016. Wikipedia- Classificação climática de Köppen-Geiger. 2016. Disponível em: (https://pt.wikipedia.org/wiki/Classificação_climática_de_Koppen-Geiger). acesso 27/Out/ 2016.
  » https://pt.wikipedia.org/wiki/Classificação_climática_de_Koppen-Geiger
• LAINSON R. 1983. The American Leishmaniasis: some observation on their ecology and epidemiology. Trans R Soc Trop Med Hyg 77: 569-596.
• LE PONT F, BRENIERE FS, MOUCHET J & DESJEUX P. 1988. Leishmaniasis in Bolivia. 3. Psychodopygus carrerai carrerai (Barretto, 1946), new sylvatic vector of Leishmania braziliensis braziliensis in lowland Subandean region. Comptes Rendus de L’Academie des Sciences Serie III-Sciences de la Vie-Life Sciences 307: 279-282.
• LIMA LC, MARZOCHI MCA, SABROZA PC & SOUZA MA. 1988. Observação sobre a leishmaniose tegumentar, cinco anos após profilaxia. Rev Saúde Pública 22: 73-77.
• MAYRINKS W, WILLIANS P, COELHOS MV, MARTINS AV, MAGALHÃES PA & COSTA CADA. 1979. Epidemiology of dermal leishmaniasis in the Rio Doce Valley, State of Minas Gerais, Brazil. Ann Trop Med Parasitol 73: 123-137.
• MENEZES CRV, AZEVEDO ACR, COSTA SM, COSTA WA & RANGEL EF. 2002. Ecology of American leishmaniasis in the State of Rio de Janeiro, Brazil. J Vect Ecol 27: 207-214.
• MINISTÉRIO DA SAÚDE. 2019. Tabela de casos 1990-2018. Brasília: MS. Disponível em: (https://www.saude.gov.br/images/pdf/2019/outubro/14/LT-Casos.pdf) acesso em 01/Jun / 2020.
  » https://www.saude.gov.br/images/pdf/2019/outubro/14/LT-Casos.pdf
• PITA-PEREIRA D, ALVES CR, SOUZA MB, BRAZIL RP, BERTHO AL & FIGUEIREDO-BARBOSA A. 2005. Identification of naturally infected Lutzomyia intermedia and Lutzomyia migonei with Leishmania (Viannia) braziliensis in Rio de Janeiro (Brazil) revealed by a PCR multiplex non-isotopic hybridisation assay. Trans R Soc Trop Med Hyg 99: 905-913.
• QUEIROZ RG, VASCONCELOS A, SOUZA IAB, PESSOA FAC, ALENCAR JE & DAVID JR. 1991. Phlebotomine sandfly (Diptera: Psychodidae) fauna survey in American Cutaneous Leishmaniasis (ACL) focus in Baturité, Ceará State Northeast Brazil. Parassit 33: 159-167.
• RANGEL EF, AZEVEDO ACR, ANDRADE CA, SOUZA NA & WERMELINGER ED. 1990. Studies on sandfly fauna (Diptera: Psychodidae) in focus of cutaneous leishmaniasis in Mesquita, Rio de Janeiro State, Brazil. Mem Inst Oswaldo Cruz 85: 39-45.
• RANGEL EF & LAINSON R. 2003. Transmissores de Leishmaniose Tegumentar Americana. In: RANGEL EF & LAINSON R (Eds), Flebotomíneos do Brasil. Rio de Janeiro, Fundação Oswaldo Cruz, p. 291-309.
• ROBERTS DR & HSI BP. 1979. An index of species abundance for use with mosquito surveillance data. Environ Entomol 8: 1007-1013.
• RODRIGUES WC. 2014. Dives - Diversidade de Espécies V3.0 - Guia do Usuário. Entomologistas do Brasil. Available from: http://www.ebras.bio.br/dives/ Acesso em: 15 de dezembro de 2016.
  » http://www.ebras.bio.br/dives/
• RYAN LA, LAINSON R & SHAW JJ. 1987. Leishmaniasis in Brazil. XXIV Natural flagellate infections of sandflies (Diptera: Psychodidae) in Pará state, with particular reference to the role of Psychodopygus welcomei as the vector of Leishmania braziliensis in the Serra dos Carajás. Trans Roy Soc Trop Med Hyg 81: 353-359.
• SANTOS-DE-MARCO T, GAIA MCM & BRAZIL RP. 2002. Influence of the lunar cycle on the activity of phlebotomine sand flies (Diptera, Psychodidae). J Am Mosq Control Ass 18: 114-118.
• SARAIVA L, ANDRADE-FILHO JD, SILVA SO, ANDRADE AS & MELO MN. 2010. The molecular detection of diferente Leishmania species within sand flies from a cutaneous and visceral leishmaniasis sympatric area in Southeastern Brazil. Men Inst Oswaldo Cruz 105: 1033-1039.
• TEODORO U, KUHL JB, ABBAS M & DIAS AC. 2001b. Luz e aves como atrativos de flebotomíneos (Diptera: Psychodidae), no sul do Brasil. Rev Bras Entomol 45: 167-172.
• TEODORO U, LA SALVIA Fº V, SPINOSA EM, BARBOSA RP, FERREIRA OC & SILVEIRA TGV. 1993. Flebotomíneos em área de transmissão de leishmaniose tegumentar na região norte do Estado do Paraná – Brasil: Variação sazonal e atividade noturna. Rev Saúde Pública 27: 190-194.
• TEODORO U, SILVEIRA TGV, SANTOS DR, SANTOS ES, SANTOS AR & OLIVEIRA O. 2001a. Frequência da fauna de flebotomíneos no domicílio e em abrigos de animais domésticos no peridomicílio, nos municípios de Cianorte e Doutor Camargo – Estado do Paraná – Brasil. Rev Patol Trop 30: 209-223.
• XIMENES MFFM, SILVA VPM, QUEIROZ PVS, REGO MM, CORTEZ AM & BATISTA LMM. 2007. Flebotomíneos (Diptera: Psychodidae) e Leishmanioses no Rio Grande do Norte, Nordeste do Brasil: reflexos do ambiente antrópico. Neotrop Entomol 36: 128-137.
• YOUNG DG & DUNCAN MA. 1994. Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the west Indies, Central and South American (Diptera: Psychodidae). 1ª ed. Memories of the American Entomological Institute, California, 867 p.
• YOUNG DC & PERKINS PV. 1984. Phlebotominae Sand Flies of North America (Diptera: Psychodidae). Mosquito News 44: 263-304.

Publication Dates

• Publication in this collection
  21 Mar 2022
• Date of issue
  2022

History

• Received
  18 Mar 2020
• Accepted
  15 July 2020