Revista de Saúde Pública
I SSN 0034- 8910 versão im pressaRev Saúde Pública 2003; 37(5)
Ecology of Lutz om yia (Nyssom yia)
whitm ani
in an urban area in
Braz il
Ueslei Teodoroa, Dayane Alber t onb, João Balduíno Kühla, Elcio Silv est r e dos Sant osc, Dem ilson
Rodrigues dos Sant osc, Adem ar Rodrigues dos Sant osc, Ot ílio de Oliveirac, Thaís Gom es Verzignassi Silveiraa and Maria Valdrinez Cam pana Lonardonia
a
Depart am ent oo de Análises Clínicas da Universidade Est adual de Maringá, Maringá, PR, Brazil.
b
Faculdade de Farm ácia e Bioquím ica da Universidade Est adual de Maringá, Maringá, PR, Brazil.
c
Núcleo de Ent om ologia da Secret aria de Saúde do Paraná, Maringá, PR, Brazil
ABSTRACT
Objectives
To st udy t he fauna, hour s of act iv it y and seasonalit y of phlebot om ines in forest anim al habit at s in t he I ngá Park, on t he urban perim et er of t he m unicipalit y of Maringá, Paraná St at e, Brazil.
Methods
Re sults
The Shannon t raps yielded 13,656 phlebot om ines, wit h predom inance of Lut zom y ia w hit m ani
( 98.7% ) . The Falcão t r aps y ielded 4,040 phlebot om ines, w it h L. w hit m ani again predom inat ing ( 96.3% ) . L. w hit m ani was m ost frequent ly found bet ween 12: 00 m idnight and 2: 00 a.m . in t he Shannon t r aps. This species w as m ost fr equent ly collect ed in t he m ont hs of August ( 55.1% ) in t he Shannon t raps, and in March 1999 ( 19.2% ) , Novem ber 1999 ( 15.9% ) and August 2000 ( 20.6% ) in t he Falcão t r aps. Mor e phlebot om ines w er e colle ct ed in Falcão t r aps inst alled in shelt er s for capt iv e m am m als ( 84.0% ) .
Conclusion
Ther e w as a clear pr edom inance of L. w hit m ani in t he I ngá Par k . The gr eat est fr equency of L. w hit m ani was in August from Shannon t raps, and in March, August and Novem ber from Falcão t r aps. Th e peak act iv it y of L. w hit m ani t ook place bet ween 12: 00 m idnight and 2: 00 a.m .
Keywords
Psy chodidae. Leishm aniasis, cut aneous. Ecology , v ect or s. I nsect v ect or s. Seasonal v ar iat ions. Ur ban zones. Am erican t egum ent ary leishm aniasis. Phleb ot om inae sandflies. Lut zom yia w hit m ani.
I N TRODUCTION
Up t o t he m iddle of t he 20t h cent ur y, appr oxim at ely 40,000 cases of leishm aniasis had occur r ed at various localit ies wit hin Brazilian t errit or y .5 Subsequent ly , t her e w as a br ief per iod of r espit e, but ov er t he last t w o decades t he num ber of cases has not iceably incr eased and cases ar e being not ified fr om all Brazilian st at es.5,7
I n t he St at e of Paraná, Am erican t egum ent ary leishm aniasis had als o been r ecor ded since t he beginning of t he 20t h cent ur y , w it h r epor t s of cases up t o 1958.5 I t st ar t ed t o be officially not ified again fr om 1980, w it h t he occur r ence of cases in 276 of t he st at e’s 399 m unicipalit ies and concent r at ion in it s nor t her n and w est er n r egions, despit e t he defor est at ion of m or e t han 90% of t he st at e’s t er r it or y .5
The occurrence of t egum ent ary leishm aniasis in t he urban zones of large and m edium- sized cit ies has been not ed in Brazil since t he beginning of t he 20th cent ury. I n t he St at e of Par aná, t her e has been not ificat ion of cases of t his disease in t he urban areas of sm all cit ies ( Cianort e) and m edium - sized cit ies ( Mar ingá) .5 Thus, t her e is an int er est in st udying t he ecology of phlebot om ines in t he ur ban ar ea of t he m unicipalit y of Mar ingá, since t hese insect s t r ansm it t he pr ot ozoa of t he Leishm ania genus t hat act as et iological agent s for t egum ent ar y leishm aniasis.1 , 2 , 6 , 8 , 1 0 I n t he I ngá Park, t he rem aining nat ive
Leishm ania, in addit ion t o species kept in capt ivit y, t her eby m aking possible t he exist ence of a com plet e en zoot ic cy cle f or Leishm ania Ross, 1903.
I n an earlier st udy in t he I ngá Park and anot her t wo preserved areas wit hin t he urban perim et er of Mar ingá t hat ar e cov er ed w it h nat iv e for est , phlebot om ines w er e found t o be pr esent w it hin t he forest , especially w it hin habit at s for w ild anim als.1 6 I n t he pr esent inv est igat ion, t he aim w as t o expand t he knowledge of phlebot om ine fauna com posit ion, t he inclinat ion of t hese insect s t o feed on blood fr om cer t ain host s, and t he hour s of t he night and t he m ont hs in w hich t hey ar e m ost fr equent , in t he I ngá Park.
M ETHODS
The I ngá Par k , w her e t he r esear ch w as car r ied out , is a pr eser v ed ar ea cov er ed w it h nat iv e for est , locat ed on t he urban perim et er of t he m unicipalit y of Maringá, in t he St at e of Paraná, w it h an area of 47.43 hect ar es. The for est is of dense t r opical t o subt r opical t r ansit ion t y pe, w it h par t ial leaf fall fr om som e t ree species in t he less fav or able w int er season, w hen a slight dr ought t ak es place. The m unicipalit y of Mar ingá is locat ed in t he nor t hw est of t he st at e at t he lat it ude of 23° 25’ sout h and longit ude of 51° 25’ w est of Gr eenw ich. I t has av er age annual pr ecipit at ion of bet w een 1500 and 1600 m m and an average annual t em perat ure of 20 t o 21° C, wit h average m axim um s of 27 t o 28° C and m inim um s of 16 t o 17° C. I n t he least rainy t hree m ont hs ( June, July and August ) , t he precipit at ion m easured is 200 to 250 m m and in the rainiest t hree m ont hs ( Decem ber, January and February) it is 500 to 550 mm.
The phlebot om ine collect ions were carried out using Shannon and Falcão t raps. During t he period w hen t he research w as carried out , infrast ruct ure w ork w as being perform ed inside t he I ngá Park, w hich m ade it difficult t o access t he Shannon t r ap inst allat ion localit ies. Thus, it w as decided t o m ov e t he Shannon t r ap locat ions, such t hat t he Shannon t r ap collect ions w er e div ided int o t w o st ages. I n t h e fir st st age, collect ion s w er e done from Oct ober 1998 t o Sept em ber 1999. On t wo night s per m ont h, from 6: 00 p.m . t o 6: 00 a.m ., collect ions were done using Shannon t raps inst alled on t he banks of t he Moscados st ream ( Figure 1) . On anot her t wo night s, from 8: 00 p.m . t o 12: 00 m idnight , collect ions were done using Falcão t raps inst alled in shelt ers for capt ive birds, m am m als and rept iles.
I n t he second st age, from Oct ober 1999 t o Sept em ber 2000, t he Shannon t raps w ere inst alled on a kiosk used for recreat ion, beside t he lake form ed by t he Mosc ados st r eam ( Figur e 1) . At t his new localit y , t her e w as no int er fer ence bet w een t he collect ions v ia t he t w o t r ap t y pes. Thus, on t w o night s of each m ont h, collect ion w as done sim ult aneously for t he t w o collect ion m et hods, at t he sam e t im es as for t he fir st st age.
Figure 1 - Localities for phlebotomine collection in the Ingá Park, on the urban perimeter of Maringá, State of Paraná, southern Brazil.
FT1 – in a cage div ided in t w o, housing a pair of lions (Pant hera leo) in one half and a howler m onkey (Alou at t a fu sca) in t he ot her;
FT2 – in a shelt er cont aining a large num ber of capuchin m onkeys (Cebus apella) ;
FT3 – in a pair of coupled shelt er s cont aining a r accoon (Pr ocy on can cr iv or u s) , t w o t iger cat s (Leopar dus t igr inus) and one bird (Penelope obscur a);
FT4 – in a shelt er cont aining a pair of peccar ies (Tay assu pecar i) , w h ich w er e su bst it u t ed by a r accoon (Pr ocy on can cr iv or u s) in Apr il 1999 t hat , in it s t ur n, w as subst it ut ed by a large num ber of coat is (Nasua nasua) ( close t o 100) , in April 2000;
FT5 – in a shelt er cont aining a large num ber of forest bird species;
FT6 – in an ar ea closed off by w ir e net t ing, cont aining sev er al t or t oises (Geochelone chilensis) , w hich w er e subst it ut ed by caim ans (Caim an spp.) in April 1999.
The light sour ce for t he Shannon t r aps w as a 100W incandescent light bulb. The phlebot om ines w er e collect ed fr om t he int er nal and ext er nal w alls of t he t r ap by t w o per sons using glass t ubes cont aining cot t on st eep ed in chlor ofor m . Hour by hour , t he insect s collect ed in t hese t r aps w er e packed in sm all cardboard boxes and subsequent ly prepared and ident ified in t he laborat ory.
The Falcão t r aps w er e pr ov ided w it h 3W light bulbs 3W. Aft er collect ion, t he insect s w er e killed using chloroform and also packed int o sm all cardboard boxes, for subsequent preparat ion and ident ificat ion in t he labor at or y.
The changes in anim al dist ribut ion m ade during t he period t hat t he work was perform ed were m ade by t he adm inist r at ion of t he I ngá Park, wit h t he aim of t he anim als’ wellbeing.
To draw up t he graph of m ont hly phlebot om ine dist ribut ion, t he William s geom et rical average ( MGW)4
for t he collect ions done w as ut ilized. The num ber s of phlebot om ines capt ur ed in t he differ ent t r aps w er e com par ed v ia v ar iance analy sis. The chi- squared t est was ut ilized for com paring t he num bers of phlebot om ines of each sex . The significance lev el consider ed w as p= 0.05, w it h t he ut ilizat ion of t he St at ist ica soft w ar e, v er sion 5. 5.
RESULT S
The species colle ct ed ar e r epor t ed in t he Table.
Table – Phlebot om ines collect ed in t he I ngá Park, on t he urban perim et er of Maringá, from Oct ober 1998 t o Sept em ber 2000.
Shannon Trap Falcão Tr ap
Species / Sex Fem ale Male Subt ot al Fem ale Male Su bt ot al Tot al
Lut zom y ia w hit m ani 10,063 3,410 13,473 2,161 1,727 3,888 17,361
Lut zom y ia neiv ai 8 16 24 27 21 48 72
Lut zom y ia fischer i 5 0 5 1 0 1 6
Lut zom y ia m ont icola 17 0 17 8 2 10 27
Lut zom y ia fir m at oi 1 1 2 4 1 5 7
Lut zom y ia cor t elezzi 7 1 8 2 0 2 10
Lut zom y ia sp. 9 2 11 3 0 3 14
Lut zom y ia pessoai 0 0 0 1 1 2 2
Lut zom yia shannoni 0 0 0 0 1 1 1
Br um pt om y ia
br u m pt i 13 1 14 1 3 4 18
Tot al 10,177 3,477 13,654 2,237 1,802 4,039 17,693 No. of collect ion
hours 576 576 576 192 192 192 - Hourly average 17.7 6.0 23.7 11.7 9. 4 21.0 -
I t w as not ed t hat t he quant it ies of phlebot om ines collect ed in t he Shannon and Falcão t r aps w er e 13,654 ( hourly average of 23.7) and 4,039 ( hourly average of = 21.0) , respect ively ( Table) . I t was also obser v ed t hat L. w hit m ani account ed for 98.7% of t he phlebot om ines ( 13,473 specim ens) collect ed fr om t he Shannon t r aps and 96.3% ( 3,888 specim ens) fr om t he Falcão t r aps. The num ber s of species collect ed in t he Falcão and Shannon t r aps w er e 10 and 8, r espect ively. More fem ale phlebot om ines w ere collect ed in t he Shannon t raps t han m ales ( p< 0.01) , but t his w as not seen in t he Falcão t r aps.
Figure 2 show s t hat t he annual dist ribut ion of L. whit m ani (MGW) w as sim ilar for t he t w o t r ap t ypes. I n
Figure 2 - Seasonal distribution of the collections of Lutzomyia whitmani in Shannon traps and the set of six Falcão traps, in the Ingá Park, on the urban perimeter of Maringá, from October 1998 to September 2000.
Figur e 3 show s t he dist r ibut ion of L. whit m ani ( MGW) in each of t he Falcão t r aps. The quant it y of
phlebot om ines collect ed in FT4 w as significant ly differ ent fr om t he quant it ies collect ed in FT1, FT2, FT5 and FT6 ( p≤0.05) . Alt hough t he quant it ies of t his phlebot om ine in t he t r aps FT3 and FT4 w er e not st at ist ically differ ent fr om each ot her ( p= 0.95) , t he quant it y of phlebot om ines collect ed in FT3 w as not st at ist ically differ ent fr om w hat w as collect ed in t he ot her t r aps ( p≤0.18) .
Figure 3 - Seasonal distribution of Lutzomyia whitmani specimens collected in Falcão traps (FT) in shelters for captive forest animals in the Ingá Park, on the urban perimeter of Maringá, from October 1998 to September 2000.
I n Figur e 4, it can be seen t hat L. w hit m ani was present in t he Shannon t raps from 6: 00 p.m . t o 6: 00 a.m .
Figure 4 - Hourly frequency of Lutzomyia whitmani in Shannon traps in the Ingá Park, on the urban perimeter of Maringá, from October 1998 to September 2000.
D ISCUSSION
Th e sp ecies L. shannoni can now be added t o t he nine species of phlebot om ine pr ev iously not ed in t he I ngá Park.1 6 The alm ost absolut e dom inat ion of L. w hit m ani ov er t he ot her species cor r obor at es w hat was previously observed in t his park.1 6 The high pr ev alence of t his species has been obser v ed in endem ic areas of t egum ent ary leishm aniasis in nort hern Paraná.6 , 1 1 - 1 6 The infect ion of L. w hit m ani by
Leishm ania ( Viannia) braziliensis t hat has been pr ov en in t he St at es of Par aná6 and Ceará1 , 8 highlight s t he im por t ance of t his species in t he epidem iology of t hat disease.
The hourly average num ber of phlebot om ines collect ed in t he Shannon t raps ( 23.7 specim ens) w as sim ilar t o w hat w as collect ed am ong t he Falcão t r aps ( hour ly aver age of 21.1) . How ever , t he dist r ibut ion of t he Falcão t r aps am ong a gr eat er num ber of ecot y pes fav or ed t he collect ion of a great er num ber of species.
The concent r at ion of phlebot om ines in t he shelt ers for capt ive forest anim als, especially m am m als ( FT3 and FT4 ) suggest s t hat t hese insect s ar e st r ongly at t r act ed t o such anim als, ex cept in t he cases of prim at es and felines ( lion) . This fact has already been not ed in t he I ngá Park.1 6 The r esult s suggest t hat t he lar ger quant it ies of phlebot om ines collect ed in FT3 and FT4 m ay hav e been due t o t he pr esence of m am m als in t he shelt er s w her e t hese t r aps w er e placed. How ev er , accor ding t o Cam pbell- Lendr um et al3 ( 1999) and Quinnel et al9 ( 1991) , t he or der of pr efer en ce t h at t h ese in sect s show in r elat ion t o host s is a funct ion of t he size or densit y of such host s.
previously,1 6 in t he sam e shelt er , t her eby giv ing ev idence t hat t hese insect s ar e lit t le at t r act ed t ow ar ds pr im at es.
The t im e of gr eat est fr equency of L. w hit m ani was from 12: 00 m idnight t o 2: 00 a.m . However, in t he I ngá Park t here is a risk of infect ion by Leishm ania t hr oughout t he night , especially bet w een 8: 00 p.m . and 5: 00 a.m . I n t he endem ic areas in nort hern Paraná, t im es of great est frequency of phlebot om ines sim ilar t o t hose observed in t he present invest igat io n have been observed.1 1 , 1 3
I n t he collect ions done using Falcão t r aps, t he m aj or it y of L. w hit m ani specim ens ( 52.2% ) were collect ed during m ont hs t hat are norm ally hot t er and rainier ( March, April and Novem ber) , alt hough a considerable proport ion ( 31.1% ) w ere collect ed in colder and drier m ont hs ( June, August and Sept em ber) . Thus, seasonalit y sim ilar t o what has previously been observed in rural areas of nort hern Paraná for L. w hit m ani using t he sam e t r ap t ype can be confir m ed.1 1 , 1 4 , 1 5 The result s from t he pr esent w or k also show t hat , in t he collect ions per for m ed in t he Shannon t r aps, t he gr eat est num ber of specim ens of L. w hit m ani ( 55.1% ) w as collect ed in one of t he dr iest and coldest m ont hs of t he y ear ( August ) . This t her efor e differ s fr om t he seasonalit y observed previously,1 2 which was also in t he rural ar ea of t his r egion, and using t he sam e t r ap t y pe.
The r esult s fr om t he pr esent inv est igat ion show t hat t her e is clear pr edom inance of L. whit m ani in t he I ngá Park, since t his species had alm ost absolut e pr ev alence using bot h collect ion m et hods. The r esult s suggest t hat r accoons, coat is, peccar ies and t iger cat s at t r act m or e phlebot om ines t hat t he ot her m am m als, forest birds and rept iles present in t he I ngá Park. The frequency of L. w hit m ani
incr eases up t o 12: 00 m idnight , rem ains const ant unt il 2: 00 a.m . and t hereaft er gradually decreases. I n t he collect ions using Falcão t r aps, L. w hit m ani is m ost frequent in March, April and Novem ber, when t he t em perat ures and rainfall in nort hern Paraná are higher. I n t he collect ions using Shannon t r aps, L. w hit m ani is m ore frequent in August , when t he t em perat ures and rainfall are lower. I t is recom m ended t hat people be prohibit ed from ent ering and rem aining in t he I ngá Park during t he night , so as t o av oid infect ion by Leishm ania. Fur t her ev aluat ion t hr ough st udies on t he at t r act ion of phlebot om ines t ow ards forest anim als needs t o be undert aken.
REFEREN CES
1. Azev edo ACR, Rangel EF, Cost a EM, Dav id JR, Vasconcelos AW, Lopes UG. Nat ur al infect ion of L. ( Ny ssom y ia) w hit m ani ( Ant unes & Cout inho,1939) by Leishm ania of t he braziliensis com plex in Bat ur it é, Cear á St at e, Nor t heast ern Brazil. Mem I nst Osw aldo Cr uz 1990; 85: 251.
2 . Azevedo ACR, Rangel EF, Queiroz RG. L. m igonei ( França, 1920) nat urally infect ed w it h peripylarian flagellat es in Bat ur it é, a focus of cut aneous leishm aniasis in Ceará St at e, Brazil. Mem I nst Osw aldo Cr u z 1990; 85: 479.
3. Cam pbell- Lendrum DH, Pint o MC, Brandão- Filho SP, Souza AA, Ready PD, Davies CR. Experim ent al com parison of ant hropophily bet ween geographically dispersed populat ions of Lut zom y ia w hit m ani
4. Forat t ini OP, Gom es AC, Sant os JLF, Galat i EAB, Rabello EX, Nat al D. Observações sobre at ividades de m osquit os Culicidae, em m at a residual no Vale do Ribeira, São Paulo, Brasil. Rev Saúde Pública
1981; 15: 557- 86.
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7. Minist ér io da Saúde. Fundação Nacional de Saúde. Manual de cont r ole da leishm aniose t egum ent ar am er icana. Brasília ( DF) ; 2000.
8 . Queiroz RG, Vasconcelos I AB, Vasconcelos AW, pessoa FAC, Sousa RN, David JR. Cut aneous leishm aniasis in Ceara in Nort heast ern Brazil: incrim inat ion of Lut zom yia w hit m ani ( Dipt era: Psy ch odidae) as a v ect or of Leishm ania braziliensis in Bat urit é m unicipalit y. Am J Tr op Med Hy g
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12. Teodoro U, La Salvia Filho V, Lim a EM, Misut a NM, Verzignassi TG, Ferreira MEMC. Leishm aniose t egum ent ar: flebot om íneos de área de t ransm issão na região nort e do Paraná, Brasil. Rev Saúde Pública
1991; 25: 129- 33.
13. Teodor o U, La Salvia Filho V, Lim a EM, Spinosa RP, Barbosa OC, Ferreira MEMC, Silveira TGV. Flebot om íneos em áreas de t rasnm issão de leishm aniose t egum ent ar na região nort e do Est ado do Par aná, Br asil: var iação sazonal e at ividade not ur na. Rev Saúde Pública 1993; 2 7: 190- 4.
14. Teodoro U, La Salvia Filho V, Lim a EM, Spinosa RP, Barbosa OC, Ferreira MEMC, Lonardoni MVC. Obser vações sobr e o com por t am ent o de flebot om íneos em ecót opos flor est ais e ext r aflor est ais, em ár ea endêm ica de leishm aniose t egum ent ar am ericana no nort e do Est ado do Paraná, sul do Brasil. Rev Saúde Pública 1993; 27: 242 - 9 .
15. Teodoro U, Kühl JB, Thom az- Soccol V, Fer r eir a MEMC, Lozov ei AL, Silv eir a TGV. I nfluence of per i-dom iciliar environm ent al condit ions in t he dispersion and proliferat ion of phlebo t om ine sandflies in Paraná St at e, Sout her n Br azil. Arq Biol Tecn ol 1997; 40: 747- 51.
Address to correspondence
Ueslei Teodoro
Depart am ent o de Análises Clínicas da Universidade Est adual de Maringá Av. Colom bo, 5790
87020 - 900 Maringá, PR, Brazil E- m ail: ueslei@wnet .com .br
Fundação Nacional de Saúde e Universidade Est adual de Maringá
Received on 20/ 7/ 2002.Reviewed on 15/ 4/ 2003. Approved on 13/ 5/ 2003.
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