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3 3 6

Revista da Sociedade Br asileir a de Medicina Tr opical 3 8 ( 4 ) :3 3 6 -3 3 8 , jul-ago, 2 0 0 5

ARTIGO/ARTICLE

Pr eliminar y study into the landing behaviour on the human body

of morning-biting mosquitoes in Atlantic forest in the

State of Santa Catarina ( Diptera: Culicidae)

Estudo preliminar sobre o comportamento de pouso no corpo humano

de mosquitos de atividade matutina em Mata Atlântica

no Estado de Santa Catarina

Carlos Brisola Marcondes

1

and Ueslei Paterno

1

ABSTRACT

Mo sq u i to e s ( 2 2 sp e c i e s) ( 0 .5 %) a n d Runc ho myia r e ve r sa ( 5 %) b i ti n g h u m a n s i n th e m o rn i n g i n Flo ri a n ó p o li s, Sta te o f Sa n ta Ca ta ri n a , we re si gn i f i c a n tly m o re c o m m o n b e lo w th a n a b o ve wa i st a n d a ll Wye o myia inc audata we re c o lle c te d b e lo w th e wa i st. Sh o rt tro u se rs a re n o t re c o m m e n d e d , u n le ss u si n g re p e lle n ts.

Ke y-words:Cu li c i d a e. Runc ho myia r e ve r sa. Oc hle r o tatus sc apular is. Pro te c ti o n. La n d i n g Be h a vi o u r.

RESUMO

Mo sq u i to s ( 2 2 e sp é c i e s) ( 0 ,5 %) e Runc ho myia r e ve r sa ( 5 %) , p o u sa n d o e m h u m a n o s p e la m a n h ã e m Flo ri a n ó p o li s, Sa n ta Ca ta ri n a , f o ra m si gn i f i c a ti va m e n te m a i s n u m e ro so s a b a i x o d a c i n tu ra , e to d o s o s Wye o myia inc audata f o ra m c o le ta d o s a b a i x o d a c i n tu ra . Este s d a d o s re f o rç a m n ã o se r re c o m e n d á ve l u ti li za r c a lç a s c u rta s n a f lo re sta , a m e n o s q u e se u se m re p e le n te s.

Pal avr as-chave s: Cu li c i d a e . Runc ho myia r e ve r sa. Oc hle r o tatus sc apular is. Pro te ç ã o . Co m p o rta m e n to d e p o u so .

1 . Lab o r ató r io de Ento mo lo gia Mé dic a do De par tame nto de Mic r o b io lo gia e Par asito lo gia do Ce ntr o de Ciê nc ias B io ló gic as da Unive r sidade Fe de r al de Santa Catar ina, Flo r ianó po lis, SC, B r asil.

Par tially financ e d b y CNPq ( Pr o c . -6 9 0 1 4 3 /0 1 -0 ) .

Addr e ss to: Pr o f. Car lo s B r iso la Mar c o nde s. Lab o r ató r io de Ento mo lo gia Mé dic a/DMP/CCB /UFSC. Caixa Po stal 4 7 6 , 8 8 0 4 0 - 9 0 0 Flo r ianó po lis, SC. Te l: 5 5 4 8 3 3 1 - 5 2 0 8 , Fax: 5 5 4 8 3 3 1 - 9 2 5 8 .

e - mail: c b r iso la@ mb o x1 . ufsc . b r Re c e b ido e m: 1 7 /0 8 /0 4

Ac e ito par a pub lic aç ão e m 3 /5 /2 0 0 5

Mosquitoes can transmit several pathogenic agents by the bite

to human and to several animals, including Pla sm o dium spp,

helminths and arboviruses. Several methods have been proposed for the personal protec tion of humans, inc luding repellents and

spec ial c lothes1 6. Sinc e mosquitoes prefer to land and to bite

o ne o r ano the r par t o f the b o dy, a c o mpr e he nsio n o f this distribution c an be useful for protec tion.

Studie s have indic ate d diffe r e nt b e havio r s fo r the var io us

mo squito spe c ie s ( e .g.3 1 7) ; Se r vic e1 7 r e vise d tho r o ughly the

s tu d i e s o n b a i t c a tc h e s o f m o s q u i to e s , i n c l u d i n g th e distr ib utio n o f b ite s o n the b o dy and fac to r s influe nc ing this,

suc h as the e liminatio n o f CO2, he ight o f flight and sme ll.

The growing number of people walking in Atlantic forest, for tourism, researc h and other ac tivities indic ates a need for more knowledge on the biting habits of mosquitoes and on means

of protec tion. Despite the c ontinental dimensions and regional differenc es of Brazil, the distribution of landing on the human

body has only been studied in the Amazon fo r e st3.

The landing behaviour of mosquitoes on the human body was

studied in the morning in a secondary Atlantic forest on the Island

of Santa Catarina, State of Santa Catarina, in southern Brazil.

Mosquitoes were c ollec ted along a trail in a c onservation

unit in the North of the Santa Catarina Island ( “Unidade de

Conservaç ão Ambiental Desterro”, henc eforward abbreviated

UCAD; 2 7o3 1 ’ 5 0 . 8 ” S, 4 8o3 0 ’ 4 4 . 3 ” W) , Mun ic ipa lity o f

Florianópolis, State of Santa Catarina. The unit has been described

elsewhere1 5. B riefly, it has 4 9 1 .5 ha and is c overed by dense

Atlantic rain forest, partly damaged many years ago, and now in

rec uperation; the trail is 9 7 1 m long, with altitudes varying from

2 5 to 1 5 0 m a.s.l. The c ollec tors, one of them ( CBM) wearing

short trousers ( mid thigh) , re ga tta shirt and boots with short

soc ks, and the other full c lothing, c ollec ted mosquitoes landing

on eac h of their bodies using suc tion and plastic tubes. They

walk e d r apidly alo ng the tr ail, sto pping at te n po ints, and

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3 3 7

Ma r c o nde s CB a nd Pa te r no U

desc ribed previously1 5. Collec tions were started 1 -1 .5 hours after

sunrise, and developed weekly from September to Dec ember 2 0 0 1 ( spring) . Two c ollec tions were done at a point ( 1 0 ) from

7 to 1 1 a.m., 1 5 minutes per hour; both were interrupted by

strong winds at this hour.

Mosquitoes collected above and below waist were preserved in

separate killing bottles, containing ethyl acetate, transferred on the same day to dry boxes, and afterwards fixed, if necessary, to triangles

on pins, ready to be identified by the use of keys4 8 9 1 0, besides

comparison with original descriptions and insects in the collection

of Fa culda de de Sa úde Pública of Universida de de Sã o Pa ulo, São Paulo. Data were analyzed by ANOVA with one variable.

A total of 3 5 3 female mosquitoes were collected ( Table 1 ) .

They belonged to 2 2 species, 1 7 were classified in Sabethini. The

statistical analysis was only performed for the most common species

(Runcho m yia reversa and Ochlero ta tus sca pula ris) . An additional analysis was performed taking the mosquitoes as a whole.

Ru. re ve rsa was significantly more common below than above the waist ( mean: 3 vs. 0 .4 3 mosquitoes/sample; F = 6 .5 6 vs.

F

c rit, 5 % = 4 .0 ) . The differenc e for Oc. sca pula ris ( mean: 1 .0 9 vs.

0 .7 7 m/sample; F = 2 .3 1 vs. Fc rit, 1 0 % = 2 .7 8 ) , similar to that of

Ru . re ve rsa, was no t signific ant even at 1 0 % . Th e s um o f

mosquitoes below the waist was signific antly higher than above

( me an: 3 .3 3 vs. 1 .2 5 m/sample ; F = 9 .8 9 vs. Fc r it, 0 .5 % = 8 .1 1 ) .

Se ve r al spe c ie s ( e .g., An o p h e le s c ru zi i) se e m to b e mo r e

c o mmo n b e lo w the waist, and have e ve n b e e n c o lle c te d o nly

b e lo w it (Wye o m yi a i n c a u d a ta and so me o the r Wye o m yi a) .

Results of the spec ies for whic h it was developed a statistic al

analysis and fo r the sum o f mo sq uito e s indic ate that it is rec ommendable to protec t mostly below the waist for walking in

the morning in this area. Young walkers, mostly students, besides

people c ollec ting wood and other materials, frequently use short

trousers ( b e rm uda s) and low boots to walk in the forest. If

people insist on leaving their legs exposed, they should apply

repellents, preferably those c ontaining deet (

N,N-diethyl-meta-toluamide)5. Thic k soc ks c ombined with long trousers offer good

protec tion when the bottoms of the trousers are tuc ked into the

soc ks1 6; in fac t, one of the trainees of our laboratory, who did

not do this, was appalled by the entry of a large beetle into his

paints. The fac t that hard tic k larvae m icuins) , snakes, ants and

other harmful animals are c ommon in this area, and probably in similar Atlantic forest areas reinforc es the need to properly

protect the legs, by applying deet both on the skin and on clothing.

Oc. sca pula ris is probably an important vec tor of Diro fila ria im m itis in the State of Rio de Janeiro7, and this worm is very

c ommon ( 1 5 %) among dogs in the region of Conc eiç ão Lagoon1,

some kilometers from the area where this study was developed.

Two o the r spe c ie s pr e vio usly r e po r te d to b e infe c te d with

mic rofilariae of D. im m itis, Ae . a lb o pictus2 and Wy. b o urro uli7,

were c o llec ted in UCAD, respec tively o n humans1 5 and in a

bromeliad1 2. However, sinc e this worm seems to oc c ur mostly in

assoc iation with dogs, houses and modified environments, the

r isk in uninhab ite d fo r e sts sim ilar to UCAD is ne gligib le .

Oc. sca pula ris was also inc riminated as a vec tor of Roc io virus

in the State o f São Paulo4; this dange r o us vir us sho uld b e

investigated in UCAD and other loc alities in Santa Catarina, before

human c ases oc c ur.

A study of preferences for body parts in diurnal mosquitoes in

the canopy of Amazonian rain forest3 indicated that Ha e m a go gus

ja nthino m ys preferred to land on the legs and mostly on the feet,

while species of Sa be the s preferred the head; the bait collector

wore only bathing trunks. The study at UCAD inc luded nine c o lle c tio ns, to taling 8 .6 ho ur s, c o mpar e d to 2 5 5 ho ur s o f c ollec tions ( 8 5 days, three hours per day) in the other study;

moreover, the present study was developed on the ground, while in the Amazonian study mosquitoes were collected at 1 5 or 2 0 m above ground level. The mean number of mosquitoes collected

per hour ( sum of collected mosquitoes/hour) were, respectively for the study in Amazon and that in UCAD, 2 .9 and 4 1 .6 . Thus, the intensity of attack by mosquitoes seems to be much higher in the UCAD study when compared with the Amazonian study.

Sa be the s mosquitoes were rare in the present study ( 0 .3 5 / hour) , in comparison with the Amazonian study ( 2 .2 2 / hour) .

This rarity of mosquitoes of Sa be the s in the UCAD study could be

due to biologic al c harac teristic s of the loc al spec ies and to

differences in methods, but it is more probably due to the scarcity

of breeding sites. Sa. aurescens is currently very common in bamboo

holes in 2 0 0 313, at one of the points of collection ( n. 9 ) of1 5, while

Table 1 - Distribution of mosquitoes landing on the human body in Atlantic forest during the morning at Florianópolis, State of Santa Catarina, Brazil

Species/ body r egions Above waist Below waist Total

Aedes a lbo pictus 1 - 1

Ano pheles cruzii 4 15 19

Culex ( Mela no co nium ) sp - 2 2

Culex ( Micro culex) sp - 1 1

Lim a tus durha m i 5 - 5

Ochlero ta tus sca pula ris 32 33 65

Ochlero ta tus serra tus 4 2 6

Pso ro pho ra fero x 3 - 3

Runcho m yia reversa 1 0 9 4 1 0 4

Sa bethes ( Sa bethinus) sp 1 - 1

Sa bethes a lbiprivus 1 - 1

Sa bethes a urescens 1 - 1

Sha nno nia na fluvia tilis 3 8 11

Tricho pro so po n digita tum 6 6 12

Wyeo m yia bo urro uli 1 - 1

Wyeo m yia ( Pho ) da visi 1 3 4

Wyeo m yia ( Den) sp 1 - 1

Wyeo m yia ( Pho ) fuscipes - 1 1

Wyeo m yia ( Pho ) ga lva o i - 12 12

Wyeo m yia ( Pho ) inca uda ta - 37 37

Wyeo m yia ( Wye) sp 1 - 1

Wyeo m yia bo urro uli 2 - 2

Wyeo m yia ( Pho ) pa llido venter - 4 4

Wyeo m yia ( Pho ) pa lm a ta - 2 2

Wyeo m yia ( Pho ) pilica uda - 1 1

Wyeo m yia ( Pho ) splendida - 1 1

Wyeo m yia ( Pho ) theo ba ldi 3 11 14

Wyeo m yia ( Pho ) damaged 5 16 21

Wyeo m yia damaged 6 4 10

Culicidae damaged 1 8 9

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Revista da Sociedade Br asileir a de Medicina Tr opical 3 8 ( 4 ) :3 3 6 -3 3 8 , jul-ago, 2 0 0 5

bamboo internodes perforated by animals and tree-holes are very

rare in the area ( CB Marcondes- unpublished results) . Two small

holes ( 1 0 -1 5 ml of water) in a palm tree cited before1 2, near point

8 of1 5 have always had immature forms of mosquitoes, including

Sa . a lb i p ri vu s, Sa . p u rp u re u s a n d To x o rh yn c h i te s s p. ( CB Marc ondes: unpublished results) . This indic ates that the available breeding places in phytotelmata are well exploited by

local mosquitoes. The three Sa be the s mosquitoes were collected

around 1 0 :3 0 a.m., on November 1st, landing above the waist.

Studie s o n landing b e havio ur in whic h mo squito e s ar e

c ollec ted for a long period ( e. g.3) may show a depletion of the

quantities c ollec ted after a peak of ac tivity in the first few minutes.

The rapid movement of the c ollec tors/baits in the study of UCAD,

b e twe e n th e po in ts , m a y h a ve s tim ula te d s o m e diur n a l

mo squito es, resting in the vegetatio n, to bite, as previo usly

observed ( see1 7, p. 3 5 2 ) . This behaviour is similar to that of

walkers in the forest, and differenc es in the methods c an impede

a prec ise c omparison between these studies.

The applic ation of repellent on feet and ankles prevented

bites of An. a ra b ie nsis on these parts of the body, and reduc ed

by more than three-fold the total number of bites, modifying the

pr o po r tio n o f b ite s o n o the r pa r ts fr o m 1 8 . 9 to 1 0 0 %6.

Consequently, even with good protec tion of those parts of the

body preferred by the mosquitoes, it is nec essary to evaluate the transferenc e of the mosquitoes to other parts; whenever this

oc c urs, a more c omprehensive protec tion is nec essary.

Mo r e de ta i l e d s tu di e s o n th e l a n di n g b e h a vi o u r o f

mo squito e s and o the r b iting inse c ts must b e unde r tak e n in

th e Atla n tic fo r e s t, o ve r a lo n ge r pe r io d a n d n o tin g th e e nvir o nme ntal c o nditio ns dur ing c o lle c tio n.

ACKNOWLEDGEMENTS

To Drs. Oswaldo Paulo Forattini and Iná Kakitani, and to Mr. Ar is tide s Fe r n a n de s , o f Fa c ulda de de Sa úde Púb lic a o f

Universidade de São Paulo, for the useful c omments, for the

c hec king the identific ation of some mosquitoes and for training o ne o f the autho r s ( UP) . To Dr. Maike Her ing Queir o z, o f

Departamento de B otânic a of Universidade Federal de Santa

Catarina, for authorization to study the c ollec tions in UCAD, and

to Mr. Silvânio G. Costa, for the help in the field work.

REFERENCES

1 . Ar auj o RT, Mar c o nde s CB , Sar to r DC, B asto s LC. Canine dir o filar iasis in the r e gio n o f Co nc e iç ão Lago o n, Flo r ianó po lis, and in the Militar y Po lic e

Ke nne l, São J o sé , State o f Santa Catar ina, B r azil. Ve te r inar y Par asito lo gy 1 1 3 : 2 3 9 - 2 4 2 , 2 0 0 3 .

2 . Canc r ini G, Fr angipane di Re galb o no A, Ric c i I, Te ssar in C, Gab r ie lli S, Pie tr o b e lli M. Ae d e s a lb o p i c tu s is a natur al ve c to r o f Di ro f i la ri a i m m i ti s

in Italy. Ve te r inar y Par asito lo gy1 1 8 , 1 9 5 - 2 0 2 , 2 0 0 3 .

3 . Dé gallie r N, Sá Filho GCN, Silva OV, Tr avasso s- da- Ro sa APA, Silva OV. Co mpo r tame nto de po uso e m par te s do c o r po humano de mo sq uito s da Flo r e s ta Am a zô n ic a ( B r a s il) ( Dipte r a : Culic ida e ) . B o le tim do Mus e u Par ae nse Emilio Go e ldi6 : 9 7 - 1 0 8 , 1 9 9 0 .

3 . Fo r attini OP. Culic ido lo gia mé dic a.Edito r a da Unive r sidade de São Paulo , Vo l. 2 . São Paulo , 2 0 0 2 .

4 . Fo r attini OP, Kak itani I , Massad E, Mar uc c i D. Studie s o n m o sq uito e s ( Dipte r a : Culic ida e ) a n d a n th r o pic e n vir o n m e n t. 9 - Syn a n th r o py a n d e pide mio lo gic al ve c to r r o le o f Ae d e s sc a p u la ri s in So uth-Easte r n B r azil. Re vista de Saúde Púb lic a 2 9 : 1 9 9 - 2 0 7 , 1 9 9 5 .

5 . Fr adin MS. Mo sq uito e s and mo sq uito r e pe lle nts: a c linic ian’s guide . Annals o f Inte r nal Me dic ine 1 2 8 : 9 3 1 - 9 4 0 , 1 9 9 8 .

6 . Go ve r e J , B r aac k LE, Dur r he im DN, Hunt RH, Co e tze e M. Re pe lle nt e ffe c ts o n An o p h e le s a ra b i e n si s b iting hum ans in Kr uge r Par k , So uth Afr ic a. Me dic al and Ve te r inar y Ento mo lo gy 1 5 : 2 8 7 - 2 9 2 , 2 0 0 1 .

7 . La b a r the N, Se r r ã o ML, Me lo YF, Olive ir a SJ , Lo ur e nç o - de - Olive ir a R. Po tential vec to r s o f Di ro f i la ri a i m m i ti s ( Leidy 1 8 5 6 ) in Itac o atiara o c eanic r e gio n o f Nite r ó i Munic ipality State o f Rio de J ane ir o B r azil. Me mó r ias do Instituto Oswaldo Cr uz 9 3 : 4 2 5 - 4 3 2 , 1 9 9 8 .

8 . Lane J . Ne o tr o pic al Culic idae . Dixinae , Chao b o r inae , tr ib e s Ano phe lini, To xo r hync hitini and Culic ini ( ge nus Cu le x o nly) . Unive r sidade de São Paulo , São Paulo , Vo l. 1 , p. 1 - 5 4 8 , 1 9 5 3 .

9 . Lane J . Ne o tr o pic al Culic idae . Tr ib e Culic ini, De i n o c e ri te s, Ura n o ta e n i a,

Ma n so n i a, Ortho po do m yi a, Ae do m yi a, Ae de s, Pso ro pho ra, Ha e m a go gu s, tr ib e Sab e thini, Tri c h o p ro so p o n, Wye o m yi a, Ph o n i o m yi a, Li m a tu s and

Sa b e the s. Unive r sidade de São Paulo , São Paulo , Vo l. 2 , p. 5 4 9 -1 1 1 2 , 1 9 5 3 . 1 0 . Lane J L, Ce r q ue ir a NL. Os sab e tíne o s da Amé r ic a ( Dipte r a, Culic idae ) .

Ar q uivo s de Zo o lo gia do Estado de São Paulo 3 : 4 7 3 - 8 4 9 , 1 9 4 2 . 1 1 . Lo pe s OS, Sac c he tta LA, Fo nse c a IE, Lac e r da JP. B e r tio ga ( Guama gr o up)

and Anhe mb i ( B unyamwe r a gr o up) , two ne w ar b o vir use s iso late d in São Paulo , B r azil. Ame r ic an J o ur nal o f Tr o pic al Me dic ine and Hygie ne 4 : 1 3 1 -1 3 4 , -1 9 7 5 .

1 2 . Mar c o nde s CB , Fe r nande s A, Pate r no U, Mülle r GA, Pinho LC, Str uffaldi DV. Ne w r e c o r ds o f mo sq uito e s fr o m the so uthe r n B r azilian state s o f Santa Catar ina and Rio Gr ande do Sul, with 1 8 spec ies new fo r the States ( Dipter a: Culic idae ) . Zo o taxa 3 4 7 : 1 - 6 , 2 0 0 3 .

1 3 . Mar c o nde s CB , Mafr a H. No va té c nic a par a o e studo da fauna de mo sq uito s ( D i p te r a : Cu l i c i d a e ) e m i n te r n ó d i o s d e b a m b u s , c o m r e s u l ta d o s pr e lim in a r e s . R e vis ta da So c ie da de B r a s ile ir a de Me dic in a Tr o pic a l 3 6 : 7 6 3 - 7 6 4 , 2 0 0 3 .

1 4 . Mitc he ll CJ , Fo r attini OP, Mille r B R. Ve c to r c o mpe te nc e e xpe r ime nts with Ro c io vir us and thr e e mo sq uito spe c ie s fr o m the e pide mic zo ne in B r azil. Re vista de Saúde Púb lic a 2 0 : 1 7 1 - 1 7 7 , 1 9 8 6 .

1 5 . Pate r no U, Mar c o nde s CB . Mo sq uito s antr o po fílic o s de atividade matutina e m tr ilh a e m Ma ta Atlâ n tic a e m Flo r ia n ó po lis , Sa n ta Ca ta r in a , B r a s il ( Dipte r a, Culic idae ) . Re vista de Saúde Púb lic a 3 8 : 1 3 3 - 1 3 5 , 2 0 0 4 . 1 6 . R o ze n d a a l J A. Ve c to r c o n tr o l m e th o d s fo r u s e b y i n d i vi d u a l s a n d

c o mmunitie s. Ge ne va, Wo r ld He alth Or ganizatio n, xii+ 4 1 2 p, 1 9 9 7 . 1 7 . Se r vic e MW. Mo sq uito e c o lo gy: fie ld- sampling me tho ds.Chapman & Hall,

Referências

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