EVO'LUTIONARY ASPECTS OF THE ECOLOGY

OF ARBOVIRUSES IN BRAZILIAN AMAZONIA, SOUTI-1

)I
AMERICA.
s
I Nicolas DI'XjAi,I,IIN'
8
Ainélia P. A.TI<AVASSOS DA IIOSA'
Pedro F. C.VASCONCIMX'
Gregorio C. SA Fii,iio?
Elisabeth S. TIWVASSOS DA ROSA?
Sueli G. ROI)KI(~UIIS'
Jorge E S. TI~AVASSOS DA ROSA^

1ORSTOM B.P. 5045, 34032 Moiitpcllicr Ccdcs 0 I Francc.

2 Instituto Evaiidro Chagas, Fundação Nacioiial de Saiidc - MS, C. P. 1128, 66090-000 Bcldm l " 5 Brazil.

42
Y

ìi
 INTRODUCTION

The Amazonian rcgion of Brazil is probably tlic world’s richest rescrvoir of arboviruscs. The 183
different types of arboviruses so far detcctcd in this rcgion (Tablc 1; Hervé d., 1986; Pinhciro aal., 1986;
Travassos da Rosa d., 1986, 1987, 1989 and unpublishcd data), account for ncar onc third of thc world’s
arboviruscs: a total of 533 (Karabatsos, 1985).Ofthcsc, I36 (83.4 %) arc cndcmic in this part of thc ncotropical
zoogcograpliical rcgion.
Of iiiaiii iiitcrest in relation with thc man-made modifications of thc natural environment is tlie study of
the ecological factors which allow the coexistclice of such a great nuiiibcr and variety of viruses and their
coniplcs transmission cycles (Pinheiro u., 1977; Dison dal., 1981). Tlie virological and serological data,
obtained betwccn 1954 and 1992 at the Evandro Chagas Institute / National Health Foundation (Belém), will
be analysed from two complemcntarypoints of view: (i) the definition ofthe ecological niche of each arbovirus
and (ii) the ecological factors which have possibly constrained their evolution.
The ccological iiichc conccpt has bccn uscd rccciitly by Calishcr (1994) in rclation with tlic dcfinitioii of
the virus spccies; “A viriis species is a polvfliefic class qf viruses îhat constitiiîes a replicaling lineage and
occupies apnrticzilnr ecological niche .‘(emphasis by LIS). Othcr definitions have been proposed by ecologists.
One which best suits tlie arboviniscs is as follows: “A niche is a multi-dimcnsiolial hypcrvolunic of resourcc
ases” (Colinvaux, 1986: 3 1). In tlie case of arboviruses, each host or altcrnatively, each conipoiieiit of the
hosts’ cnviromiient inay reprcsent one of thcse resource ases or variablcs, allowing for tlie quantification of
I
tlie niche. Multifactorial data analysis methods, which havc been uscd here for tlie first time with arboviruses
k (to our knowledge), sccni particularly well suited to (i) the nuincrical definition of the niche of cach virus
, species and (ii) the study of the ecological grouping of the viruses.
# The question undcrlying our prcsent work relatcs to tlie ecological factors which prevent arboviruses
from multiplying randomly in all available hosts. There are probable constraints of various origins and located
at various levels, from inside the ccll to the ccosystem: genetical (or physiological) (Dubois, 199I),eco-
ethological and historical (or biogcobraphical) (Barbault, 1991).
I
M.m” AND RIETIIODS
SEIWLOGICAL
AND VIROLOGICAL RIETIIODS
The crude data were reprcseiited by the isolated strains and the results of haemagglutination inhibition
(HI) tests (the laboratory techniques are described in detail in Shope & Sather, 1979). Tlie HI tests liave been
considered positive for a particular arbovirus if it showed a titer at least four-fold higher than any other tested
antigen in the same scrological (cross-reacting) group. This “four-fold titer criterion7’has been established
either froin unpublished results of experuiients conducted on mice, rats and fowls, or from follow-up serological
studies in naturally infected people and sylvatic animals. This criterion inay appear overrigorous but the main
objective was to prevent the introduction of falsc positives in the data, cvcn at cost of sonie false negatives
Wicn sera were availablc, HI rcsults which appearcd doubtful havc bccn chcckcd by scrolieutralizatiolitest
(except in the case of turtle sera which do not contain iieutralizing antibodies. APA Travassos da Rosa,
unpublished data). A contingency table has been constriictcd, of which three subsets have been submitted to
I
the treatmiits described below.

NIJMERICAL AND srmsmxi.,MCr w D s

I

The structure of tlie data was first explored qualitatively, using presence (1) vs. absence ( O ) of each virus
Y
in each host as characters (annexes 1& 2). The hosts havc been grouped at the order or genushbgenus levels
for vertebrates and arthropods, rcspe&ely. The subsets wverc as follows: (a) arbovirusesknown from arthropods
only; (b) arboviruscs known from vertebrates only and (c)arboviruses known froin both types of hosts. These
analysis were bascd on tlic phylogenetic method (Wilcy, 1981; d’Udckem-Gevers, 1990; Hennig in Goujet
al., 1988; Janvier in Goujct d., 1988) and have bccii conducted with the PAUP software (Swofford, 1993).
For each subset, an unrootcd coiisensus tree was computed, adopting tlie “50 %-majority rule” (Margush &
McMorris in Swofford, 1993).
Quantitative treatments were done on the uacoded data matrix (contingencytable) or subsets of it (Annexes
4-6). Two methods of multifactorial analysis, the factorial analysis of correspondances and the hierarchical

43
ascendent classification (AnaMul and ADDAD packages, rcspectively) have provcd useful for this approach
(Fénelon, 1981; Febvay & Bonnot, 1990). In order to study thc ecological rclationships csistiiig betwecn the
arboviruses more specifically, the hosts have been grouped accordin2 to thcir terrestrial/ arboreal and diurnal/
nocturnal habits (variables nuniber 32 to 37 in Anncs 1). A more detailed study of the bird-associated
arboviruses, based on data about habitat and lcvel prefcrcnces of the hosts has bccn done in a separate papcr
by Dégallier et. ( 1992b) and will only bc summarized bclow.

RESULTS
The following sample sizes (nuniber of specinlens or pools) formed the basis of the present study:
haematophagous Diptera, more than 515 O00 pools; marsupials, 6,427; bats, 9,276; wild monkeys, 2,428;
rodents, 18,741; edentates, 861; carnivorous, 36 1: ungulates, 3,374; birds, 12,423; reptiles, 6.052; amphibians,
1,509.

TIIEQUALITATIVE APPROAClI
NUMBER OP IIOS~SBY VIRUS

Tlie number of different spccies of hosts for each virus group (tablc 2) givcs a crudc indication of thcir host
spectrum, and consequcntly, of the iiitciisity of their adaptivc radiation. It is obvious l’rom thcsc data (coniparcd
with thosc in tablc 1) that tlic virus faniilics with grcatcr niumbcr OFspccics arc not ncccssarily thosc wliich
were found in the greater varicty of hosts. For csamplc, thc Flaviviridac and Togaviridac with only 8 viral
species each in the Brazilian Amazon region, have bcen found associated with at lcast 57 and 56 diffcrcnt
hosts, respectively. This compares with 54 hosts known for the Bunyaviridae which includes 45 species. On
b
the other hand, the Reoviridae, ayounting for 63 different viruses, arc known from only 14 differcnt spccics
of hosts. Thus, the ecological diversification, in tcrnis of number of hosts involved in transmission cycles,
seems to be independant from the $$teniatic divcrsity of thc viruses (= nuniber of spccies). However we will
sec in later discussion thc importan& of sampling bias on this pattcrn.

Table 1:Numbcrs of genera, serological groups and species for each family of arboviruses present in the
amazonian region of Brazil; their order of enumeration follows dccrcasiiig nuiiibcr of spccics.

Family genera groups species

Bunyaviridae 2 70
Biinynvirus (a) 45
Phlebovirus 25
Reoviridae 63
Rliabdoviridae 15
Togaviridae 8
Flaviviridae 8
Coronaviridae 1
Poxviridae 1
Unclassified 12
Arenaviridae (0 3)
Herpesviridae(0 1)
,.
Paramyxoviridae(0 1)
i

(*) with 1 Bicnyavinis-like virus included

(b) with 4 ungrouped viruses included
with 3 ungrouped viruses included
(d) with 3 ungrouped viruses included
(e) with 1 ungrouped virus included

(0 probably not arboviruses

44
 NUMUEH OF VIRUSES I ~ YIIOS‘I’

Table 3 shows the nuniber of diffcrcnt spccics of viruses found in each ecological typc and/or systcinatic
group of hosts.
Some types of hosts seem to be more favorablc to the speciation of arboviruses than others. Aniong the
arthropods, sandflies arc almost the solc hosts €or the majority of Reoviridae hiown from our region. As these
viruses do not forni agglutinins in vertebrates, it is not yct possible to know if they are diversified in this
respect. Due to their minutencss and tlie lack of an idciitification key for fresh females, the phlebotoniine
sandflies wcrc not identified and thus, may contain niany species with various habits. On average, nocturnal
mosquitoes harbor more diffcrcnt viruscs than diurnal ones. This difference rcsults mainly from the nuniber of
Bunyaviridae transmitted by nocturnal mosquitoes. Among tlie vcrtcbratcs, tlic samc may be said, i. e., that
tlic nocturnal oncs harbor a larger variety of viruses, duc cspccially to tlic prcdominancc of the bunyaviruscs.
The Flaviviridac sccm to bc as “diurnal” than ‘Ìiocturnal” but the Togaviridae niay be more “diurnal” if wc
consider tlieir vertcbratc hosts.
Nevertheless, thc data discussed in tlie two previous paragraphs are very Cnide and will be examined in
more details in tlic following sections.

The phylogenetic assumptions

Any phylogenetic study niay ideally need assumptions about (i) tlie transformation sequence of the states
of tlie characters, and (¡i) tlie states wvliich niay be considered as apomorphic (= dcrived or specialized) or
plcsiomorphic (= anccstral or primitive).
However, in the casc of arboviruses, fcw authors hnvc ndrcsscd this qucstion. Mattingly ( 1960) and Calishcr
L

(19S8) supposed that thc CuIm - bird cycle of niany arboviruscs inay be primitive (plcsiomorphic). I n fact, if
a
the arboviruscs can be considered!to have originatcd in arthropods before they become adaptcd to vcrtcbratcs
(Goldbach & Wellink, 1988) havc<si!ggcsted the samc for inscct viruses which adapted to plant), it would be
reasonable to associate ancestry of the vcrtebratc group with diversity of arboviruscs. The phylogeny of
mosquitoes is even worse hiown and cannot give any indication to solve this qucstion although culicincs were
first recordcd from the Oligoccnc. Thus, the prcsciit study lias been donc, without doing m y apriori polarization
of tlie characters.

Results of the phylogenetic analysis

Figures 1, 2 and 3 show hypothctical pliylogcnics of tlic arboviruscs whosc arthropod and vcrtcbratc, only
arthropod, or only vcrtcbratc hosts arc known, rcspcctivcly.
Fifty, 34 and 29 viruses liave been included in these rcspcctivc subsets. Sisty diffcrcnt viruses are known
only from phlcbotomine sandflies (Travassos da Rosa aal., 1983, 1954; see also anncx 3) and, as such, liave
been grouped under tlic denomination: “sandfly bornc”.
The first consensus tree (Figurc I ) was computed from a total of 500 trccs, each of 14 I steps. Its rcsolutioii
is not perfect as it shows yct sonic polychotomies. Thus, the viruscs Acara to Ncpuyo, Bcnfica to Guajara,
Bcnevidcs to Itaqui, lrituia to Tapara and Jurona nced to be studied in more dctail with rcspect to their hosts
andior the possible sampling bias. Some ecological groups seem better established if we consider tlie value of
the majority-rulc indcs: Moju to Una, Marituba to SLE. Turlock to Triniti, and Guaroa to Oropouchc.
Thz second consciisus trce (Figure 2), obtained from 500 most parsimonious trees, each 27 steps-long, and
\\hich shows tlic hypothcticai rc1;ationships of the viruscs isolatcd only fron! liaematophagous arthropods,
L appcars evcn lcss resolvcd than tlil previous one. With tlic csccption of little groups likc Buritirana/Itacaiuiias
and TaiassuiNyeoniyk, th:: g-oups:,arc cither polychotomous or with poor conscnsus rates. However, despite
its pol~~chotomy, the Anlniateua to %ucunli group was prcsent in more than half of the trees.
Kcmarks of the sanie order than tlie preceding can be made about tlie tree presented in Figure 3 , where
viruses only kn0n.n from vertebrate hosts have been considered (consensus tree obtained from 1O2 distinct
trees, each 2.6-steps-long). The relationships between the viruses from Agua Preta to Parisa and Beleni to
Jatobal are poorly resolved. 011tlic other hand, some associations appeared at greater rates: AnliangalJari;
Araguari/Itaituba/Piry and Bocas to Timbó. One group seems to be fairly resolved: Urucuri to Utinga.

45
Table 2: Minimum numbers of different specics of vertebrate and arthropod hosts for each family and/or
genus of arboviruses prcsent in the amazonian rcgion of Brazil; thcir order of ciiumcration follows decreasing
total number of species.

Virus/Min. Nr. of different species

Family/Genus Vertebrates Arthropods Total

Flaviviridae 37 20 57
Togaviridae 39 . 17 56
Bunyaviridae
Bunynviriis 15 39 54
Phlebovirits 9 3 12
Reovir idae 2 12 14
Rhabdoviridae 3 6 9
Coronavir idae 1 1
Poxviridac 1 1
Unclassified - 2 2

TIIEQUANTITATIVE APPROACH

The quantitative analysis have becn donc with tlic viruses whose cycles arc bcttcr known, i .e. which havc
bcen found in both vertebrate and arthropod hosts. A spccial analysis has bceii donc prcviously with thc
viruscs known from birds (Degallicr d., 1992b). Y

The multidimensional ecological niche

Tlie first four factors which resulted froni the corrcspondance analysis, account for 91.9 96 of tlic total
inertia of the dot cloud. Tlie representation of the variables is best along the factors 1,2, 3 and 4 (Figure 4).
The fomier seems to be oriented from diumal to nocturnal canopy vcrtebrates, from diurnal to nocturiial
ground vertebrates and from diunial to noctunial mosquitoes. The third factor is less discriminant for these
saine ecological variables. The fourth factor separates wcll thc mosquito-relatcd variablcs (diuriiaynocturIla1).
However, in order to interpret graphically the relationships between these variablcs and the viruses, we havc
to consider the relative contribution of each of the latter to the same factors. Figurcs 5 and 6 show simultaneously
tlic projcctions of thc variablcs and viniscs on thc plaics fornicd by thc factors 2 and 3, and 2 and 4, rcspcctivcly.
Only the elements which contributed for at least 20 % of thc total inertia of at least one of the two factors have

Table 3: The hosts of sylvatic arboviruses in Brazilian Aniazonia, grouped according to their ecological
characteristics. For each type of host is indicated the number of virus species associated with.

Mosquitoes Sandflies Midgcs Ticks Vertebrates

Arbovirus Nocturnal Diuqpai Diurnal Nocturnal
Families i, b terr. canopy terr. canopy
I .
Flaviviridae 4 4 O 6 6 6 6
Togaviridae 6 6 O 6 7 5 5
Bunyaviridae 37 19 2 13 17 21 17
Reoviridae 8 5 51 O 1 2 O
Rhabdoviridae 3 3 3 4 2 1 1
Coronaviridae O O O 1 O O O
Poxviridae O O O O O 1 O
Unclassified 4 2 2 O O O 3
~~ ~~

Total 63 40 69 4 3 36 40 45 38

46
 been retained. For clarity, the labcls of tiic elcnicnts which coiitributcd significantlyto the two factors are in
boldface and those \dich contributed only to tlie ordinate factor are in italics,
The following associations may be deduced from tlie Figurcs 5 and 6:
- BEN, ICO, BSB, MOJU, ACA, BSQ, CAR, CAR-likc, CATU, MUC, NEP, CAP, GMA, BVS, ITQ,
MUR, ORI, BIM, GJA, GAM, AURA, Trombetas: nocturnal tcrrestrial vertcbrates/noctunial mosquitoes;
- UNA, MCA, ILH, TNT, KRI, MAG (+ KWA-like, ANU diumal terrestrial vertebrates/diurnal
I?):

mosquitoes;
- YF, GRO, MAY, SLE, TCM, TUR, WEE, ORO, TCM, JUR: diurnal canopy vertebrates/diurnal
I
mosquitoes;
Thc viruscs EEE and PAC-likc scciii to localizc at intcrnicdiatc positions, bctwccn diurnal and nocturnal
and bctwecn canopy and ground-dwcliing hosts. I n tlic following scction, w c will ‘-80back” to thc wcodcd
data to csaminc thc csact ecological coniponcnts of cach of thcsc groups.

T l I E ECOLOCICAI~(NURIEIIICAL,) CI,/\SSIIWAIION
Thc ecological groups obtained,,bythe ascendclit hicrarchical classification algorithm arc sliowi in Figures
7 and 8 for the viruses and thcir serological groups, respectively. The proportions representing the different
types of hosts have been put on thc ordinate scalc. Scrological group A and buiiyaviruscs may contain sonic
viruses which do not cross react inside thesc groups, thus they have becn indicated by an asterisk.

Aciiru
Ncpupo
Ikrifica
I
L
I%l,SIlI%IISIl
Caranaru like
Guajhra
i fkr1cvitlcs
Capim
ilaqui
1 O0 Mwju
83 Orihoca
Guallla
Magu;tri
u na
7 “C
95
hhriLubil
Apcu
Murulucu
Ananindcua
LISI. Et]. 13nc.
c;ltu
1O0 Ciiriiparu
It;lporarlga
1 O0 Bussuquara
St. Louis Enc.
Bi miti
Monle Dourado
lriluia
Pacui
Santiircm
Tapam
1 O0 Aura
Kairi
Tronibclas
J II rollii
Kwalta like
l’ncoril like
‘rur Ioc k
W C S I . Eq. EIIC.
MaCJUJ

!.W
Pixuna
Triniti
Gaciihoa
Guama
Tacaiu1rra
Iltaus
1 O0 M;iy:iro
1O0 Muciunho
1 O0 Ycllow Fcvcr
1O0 Icoaraci
LOropouchc

Figure 1.Unrooted, 50 % - majority rule consensus tree of the arboviruses known from both vertebrate and
arthropod hosts in Brazilian Aniazonia, 1954-1992. The value at base of each group is the proportion (%) of
the 500 most parsimonious trees which show thc group.

47
I
 Some reinarks which reniain of preliminary naturc can be drawn from this analysis: (i) thcrc is a continuum
(or gradient) from “diurnal” to “noctur~ial”viruses and from cbarboreal*’ to “terrestrial”; (ii) some groups like
the GAM to WEE, TUR to ACA and Trombetas to GRO were mostly found in “diunial canopy vcrtebratcs”
aiid “nocturnal mosquitoes”; (iii) the PIX/ TNTI MAG group is predoniinantly “diurnal” and “tcrrestrial”,
opposing to the almost strictly “canopy-liking” viniscs MAY, ILH, YF and UNA; (iv) thc ccology of somc
groups of viruscs like ORO/ ANU, Tapara to KRI and IC0 weds more inforination to bc gathered, cspecially
about their vectors; (v) in fig. 8, we see that with some csccptions, each serological group lias but one virus in
one ecological group; we need finer definitions of the nichcs of 2 Iviruses pertaining to A, B, BUN, C, CAP,
CGL and GMA serological groups.

74 Melao
Scrra do Navio
Trocara

60 - Galibi
lcri
Purus
72 Ilupi ranga

48
 The bird-associated viruses
We will summarize below the main results of this spccific study, alrcady published by Dégallier a.
(1 9924. The subset including thc bird-associated arboviruscs accountcd for 30 different arboviruscs. An
ascciideiit hierarchical classification has bceii obtained, using as ecological variables five types of vegetation,
two of which (igapo or inuiidatcd forest and “terra fimic” forest) lias becn subdividcd in two and five strata,
Agua Preta
Caj,v,ci ras
Juruaca
Mapueri
Mojui dos C‘anipos
Parixa
Bclem

1O0
ltaituha

- 85

Candiru
7Cacipacorc
L Utinga
Figure 3. Unrooted, 50 % - majority rule consensus trec of the arboviruses luiowvn only from vertebrate hosts
A in Brazilian Amazoiiia, 1954- 1992. The value at base of each group is the proportion (YO) of the 102 most
parsimonious trees wliicli show the group.
respectively. A gradient (contiiuum) has becn observed between bird species which prefer secondary vegetation
or forest (= “capoeira”) and, those which are found mainly in priiiiary forest.
CDU virus lias been found iiiaiiily in canopy birds which are dwelling mainly (50 %) above 15 and 30 m.
This virus, as for sonic others (CPC, MAY, ILH, TCM), lias an important sccoiidary forest component (25
%). The birds which are hosts of UTI, KWA, GAM and IC0 viruscs arc spccics living exclusively in the
“terra-firme” forest.
49
 EEE virus has been “found” in all but one rare type of vegetation or strata (forest on sandy ground) and is
considered as ecologically versatile. This may be linked to a great potential of this virus to colonize new
niches, including in urban environnient (strains isolated from mosquitoes in Fortaleza, Ceará, Brazil).
I 1
100% Canopy diurnal Vert.

Ground diurnal Vert.

80%
Canopy noct. vert.

60% Ground noct. Vert.

Diurnal mosquitoes
40%
Noct. mosquitoes

20% Ticks

Culicoid midges
0%
Factor 1 Factor 2 Factor 3 Factor 4
@¡ Phlebotomine sandflies
_______-_ -

Figure 4. Contribution (% of explained incrtia) of tlic ninc ccological variables to tlic factors 1-4 of tlic
correspondance aiialysis of the arboviruses known from both arthropod and vertebrate hosts in Brazilian
Anazonia, 1954-1992.

r
The viruses which niay be considered tlie more prone to infect huntan people in rural places are BSQ,
GMA, MUC, MUR and APEU because they have been found in birds which arc living in the secondary (or
degradated) enviromnents nixed with cultivated areas as is often the case in Aniazonia. They are actually
fairly prevalent in human sera.

DISC~JSSION
The ecological niche concept for arboviruses
Previous works have already dcscribcd the probablc sylvatic cycles of many amazonian arboviruses
(Woodall, 1967; Dégallier, 1982; Hervé d . , 1986). Howcvcr, tlic grouping of ccologically siniilar viruscs
was made mainly after the number and naturc of the hosts, i. e. tlic rclativc “complcsity” of the cyclcs. Wc
have reexamined the sanie data in a phylogcnctic pcrspcctivc. In a quantitativc ccological study of tlic viruses

GAAßTrombetas
AURA. ” ’’

8
li
u.

CATU
Muc

50
 pertaining to the group C of Bzinymirzis, Woodall (1979) lias sliow~ia marked niclic separation between
canopy- and ground level-transmitted viruses and, when two viruses appeared to share tlie same niche, that
the vectors were distinct species. Thus, for establishing themsclves in a locally stable equilibrium, related
viruses cannot share tlie same arthropod and/or vcrtebrate hosts. It niay even be said that the less they are
serologically related, tlie iiiore they can share tlie same ecological niche.
Tlie complexity of the amazonian environment, cscmplified by an cstremc divcrsity of vcrtcbratc and
arthropod spccics, and conscqucntly of nichcs, liavc favourcd thc diversification and sympatry OF many

UNA

MAY
MuGm m(“
... GMÄ..cATÜ.
MR ~ I T Q . B V ...
=..q$@o
= S CAP
B......

PAC-like ...!?!M.CAR-like

arboviruses of the same group. As tlie prcsent study has show, the presence of two or more different viruses
of the saine serological group in what has bccii charactcrizcd as one nichc may bc duc to the coarseness of tlic
ecological variables which have bcen considcrcd. As many ccologists havc shown, temporal and spatial variablcs
may also be includcd in the multidimensionaldefinition of the nichcs. Tlie isolatioiis of strains andor serological
coilversions in sentinel animals should be iiiterpreted in the futurc for tlic “temporal” characterization of the
niches.
Excepted for some viruses which are ecologically very distinct (PAC-likc, CDU), tlicre is no clear-cut
separation between one group and the nest along thc “ecological transccts” defincd either by the preferred
vegetatioli types and strata, or by the habits of thc hosts. This may mean that, with similar historical (=
biogeographical + genetical) constraints, tlie arbovirus population in a dcfincd coniinunity forms a dynamic
equilibrium. Subsets of this population may sliarc tlic same niche, at lcast at thc two lcvcls studicd hcrc, and
each nichc is separated from the others by ecological constraints acting on thc host populatioiis. I-lowcvcr. two
very differclit typcs of pcrturbations can modify this cquilibrium. Whcn soinc fluctuations arc going on in host
populations, as occurs seasonally for non-iiiuiiunc hosts, only tlic arbovirus transmission icvcls arc affcctcd.
On the contrary, whcn the host populations are permanently modified, the cquilibrium of arbovirus populations
need to shift to a new statc. Eventually, new niches may appcar nhich would be filled aftcr a short time. These
inay be colonized by new genotypes, obtained by recombination, reassortmcnt or introduction from adjacent
communities (Calisher, 1988). These relatively rapid adjustments of cquilibrium liavc been noted in the case
L
of the important perturbations iiiduccd by the filling of a dam rcscrvoir, where “ncw” arboviruscs appeared in
t
tlie area, either as exogenous material or as autoclitonous speciation.
The phylogenetic study of arboviruses, based on the viruses-hosts associations is yet vciy tentative because
of the lack of phylogenetic classifications of either group (Eldridgc, 1990). This author lias looked for sonic
evidcncc of a host-parasitc coevolution in tlie cast of tlic California scrogroup viruscs What \ve havc dcfincd
as historical constraints arc doubtlessly related with sonic effects of coevolution but it remains difficult to
distinguish these from tlie constraints arising from virus competition aftcr horizontal traiisfcrs (Tabachnick,
1991). These hypothesis need to be evaluatcd by molecular biologists.

51
 ANU ORO

ILH MAY UNA YI:

CAP EEE GAMSLE WEE

ACA APEU ITQ MTB UKI

TCMTUR

AURA GIA GRO KWA.likt!

Trombetas

MAG PIX TNT

BEN BIM BSB BVS CAR-

like RI NR KRI MCA
MD0 NEP KA-like STM
'lapan

CAR BSQ OMA ITP MOJLl

MUC

CAIU MUR

IC0

PAC

Figure 7. Ecological composition of the groups of viruses, obtained by the hierarchical ascendent classification U
analysis of the ecological data, available,for the agents known froin both arthropod and vertebrate hosts in Brazilian
hnazonia, 1954-1992. 'p
THEEVOLUTIONARY ASPECTS OF THE ECOLOGY OF ARBOVIRUSES
What happened with the viruses for which some evolutionary hypothesis.are available, based on protein
sequencing ? Levinson d. (1990) fimished some interesting hypothesis which will be discussed from an

52

ri,
 ecological point of vicw. MAY (with UNA, not studied by thcsc authors), EEEWEE, AURA and MUC
(member of VEE coniplex) seem to have diverged in four different directions (fig. 7). As Halm d. (1988)
havc slio\vn, WEE virus arosc probably as a rccombinant bctwccn EEE and anothcr A Iphovi~uswhich may bc
AURA. EEE sccnis to be a vcry vcrsatilc virus, cspccially in birds (fig. 9) whcrcas AURA lias been found
only in monkeys. The ccological link betwccn the two may be the Melonoconion and Och/eroro/zwsubgenera
of Culex and Aedes mosquitoes, respectively.
O
as
2
!
6
a
O
6
h
O
8
O0

as
O
as
E

i
E
il
3
e
P

L I

Figure 8. Graphic representationof the saine data as in fig. 7, but \villi the serologicalgroups of viruses in place of their
actual names; when more than one virus is included in a group, the nuinber of virus species is shown in parenthesis;
asterisks refer to ungrouped viruses, i. e. virubs which do not cross react serologically inside tlieir group.
b
53
 CONCLUSIONS
Tlie present study was not dctailed enough to csplain why sonie viruses of the same serological group
coexist and othcr do not, but it allowed us to define tlic main ecological groups. Each of these groups further
needs to be studied separately as it has been done with the bird-borne arboviruses.
Despite the great number of tested pools between 1954 and 1992, serological and virological data are
lacking either for viruses which do not forni agglutinins, or about potential hosts which are difficult to collect.
It has been seen that less than one third (28.9 %or 50/173) of the viruses known from sylvatic hosts have been
found in both vertcbrate and arthropod hosts, 17.7 % (29/173) are knowii only from vcrtcbratc hosts and 54.3
% (94/173) only from arthropods. Among the lattcr, 63.8 O/o (60/94) are known only from phlebotominc
sandflies and represent probably a very complex ecological system, even if their vertebrate hosts are vcry
diverse.
Sampling bias may account for some distortions in the quantitative delineations of the niches. For example,
ground dwelling rodents, marsupials and birds are much casier to trap than canopy frequenting hosts and
among them those which cannot be attractcd by any type of baited trap. Thus, many species are poorly
known, not only for the viruses they may harbour but also for their bioecology. An important ecological
“axis” which has been yet neglected is the time or seasonal one. It is quite conceivable that sonie hosts may
harbour different viruses of the sanie serological group at different times of tlic year. This niay be especially
tlie case with bunyaviruses whose antibodies are not life-long lasting (Shope &., 1967). In future studies,
more precise serological tests may allow us to define each virus-host association better.
Nevertheless, the methodology followed in the above quantitative analysis revealed itself adequate to tlie
study ofthe multidiniensional niche concept of arboviruses, and it will also be a usefùl tool to make prcdictions
about the evolution of the arboviruses in response to modifications of the environment.

Acknowledgments 1

We wish to thank all staff members, both from the Evandro Chagas Institute and other Institutions, for
their past and present participation in the field and laboratory work which has made this paper possible. The
present work has beneficiated of the unvaluable financial and/or logistic help of Eletronorte (Eletrobras),
SUDAM (Polos Agropecuários da Aniazoiia), CNPq, ORSTOM and Foundation SESP (now National Health
Foundation, Ministry of Health). Thanks are also due to Dr. Brian H. Kay (CSIRO, Brisbane) who has kindly
reviewed tlie manuscript.

54
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56
 Annex 1. Types of hosts used as variables in qualitative and quantitative ecological analysis of the
sylvatic arboviruses found in Brazilian Aniazonia, 1954-1992.

Anopheles (Nyssorhynchzis) spp.

Anopheles (Anoplieles) spp.
Anopheles (Stethoniyia) spp.
Ciilex spp. (not CzilexhorMelanoconion)

Annex 2.Data matrix used in the qualitative aiialysis of the sylvatic arboviruses found in Brazilian Amazonia,
1954 - 1992; The three successive subsets correspond to viruses known from: arthropod and vertebrate
hosts; only arthropods and o d y vertebrates; the colunuis represent the variables 1-3 1 listed in annex 1; the
“Phlc” (= sandfly-bornc) viruscs arc listcd in thc anncs 3.
II.

ACA 0001000000000000001100011000000
ANU O00 1010001000100001000000010010
APEU 0001010100000000001010000010010
AURA 0000010100000000000000000000010
i(
BEN 0001000000000000000000010000000
BIM 0000010000000000000000010000000
BSB 0001000000000000010000010000000
BSQ O001 110001010000111101o 110 1011o
r
BVS 000l0l00000000000010000l0000000
CAP O00 1110000000000001000010000000
CAR O00 1 I1O000 1O0001 1o 1011o1 O0 1111o
CAN :, O00 1010000000000000000010000000
CATU 0011110001000010001010010000110
EEE O00 I l 10 10100000001 100001O0 1O0 11
GAM 1000001000000000000000000010000
GJA 0001000000010000000000010000000
GMA 000101o 10111100000100001O0 101o 1
GRO 1.
100000000000000001000000001111o
IC0 000000000000 1000101I1 11I1010 1I1
ILH 0000000 11o 1O000 I1000000I 10 I11 1I
IR1 0000000000001000000000010000000
ITP 0001010001000000101010011011111
ITQ O00 1o1000000000000 1000 110000000
JUR 00000000100000000000000000l0000
KRI 0000000100110000000000000000010
KWAl 0000100000000000000000000010000
MAG 1010010110110000001000010000001
MAY 00000000 I O0 100Io 1I I 1 10011o 11II O
,”
MCA 00000000000100000000000110I0000
I MDO 000000000000 1000000000I00000000
MOJU 00010100010110000010l00l0000000
MTB 0001010000000000001000000010000
MUC O00 1o 101 1 1o 100000010 1 1o I 101 111o
MUR 00010100000100100010100100100l0
NEP 0001000000000000001000010000010
ORI 00010101011100000010000l0000000

57
ORO O000 100100000100011111o 1101o 11o
PAC 0000000000001000000000010000000
PCAl 0000100000000000000000000010000
PIX 001000000001000000101001l010100
SLE O0011101010100001010 10111010110
STM 0000000000001000000000010000000
Tapa 0000000000001000001000010000000
TCM 100000001000000000000001 I o 111 1o
TNT 1010000000010000000000011010000
Troni 1000000000000000000000000000001
TUR O000 11000000000000000000101001o
UNA 00110001111100000000l0000010000
WEE 0000010100000000100000001010101
YF 0000000110010000101011010000110
ANH 0000000000000000000010000000000
AP 0000000000000000000000000000100
ARA 0000000000000000001000000000000
Belt 0000000000000000000000010000000
BLM 0000000000000000000000000010000
BOC 0000000000000000010000000000000
BUJ 0000000000000000001010011000011
Caja 0000000000000000000000000000100
CDU 0000000000000000000000111010110
CHO 000000000000000 10 10000000000000
COT1 0000000000000000000000010000000
CPC 0000000000000001101010011010110
CUI 0000000000000000000000000100000
ITA 0000000000000000001000000000000
Jacu 0000000000000000000000001000000
JAN 00000000000000000000 10000000000
Jato 0000000000000000000000000001000
Juru ’ 0000000000000000000000000000l00
MCO 0000000000000000010000000000000
MDC 0000000000000000000000000000100
MOR 00000000000000000000000l0000001
MPR 0000000000000000000000000000100
Pari 00000000000000000000000000001O0
PIRY 0000000000000000001000000000000
SM 0000000000000000010000000000000
TBT 0000000000000000000000010000000
TIM. 0000000000000000010000000000000
URU 0000000000000000000000011000100
UTI 00000000000000001000l00100100l0
ACD O000 10000000000000000000000000~
ARU O000 1I 0000000000000000000000000
Arum 1000000000000000000000000000000
Breu 1000000000000000000000000000000
Buri 0000000000000100000000000000000
CAN 0000000000101000000000000000000

58
Cara 1000000000000000000000000000000
Coda 0000000010000000000000000000000
Gali 0000000000100000000000000000000
IACO 0000000000010000000000000000000
IERI 0000000000 100000000000000000000
Iopa O000 100000000000000000000000000
Itac 0000000000000 100000000000000000
ITU 0000000100100000000000000000000
JAC 0000010000000000000000000000000
LUK 1010000100000000000000000000000
Majo 0000000100000000000000000000000
MEL 0000000100000000000000000000000
MIR 0000010100100000000000000000000
MQO 0000010001010000000000000000000
MUCU 1000000000000000000000000000000
Prka O000 100000000000000000000000000
Prni 0000100000000000000000000000000
PUR 0000000000100000000000000000000
SDN 0000000100000000000000000000000
SOR 0000000000010000000000000000000
Taia 0111000000010000000000000000000
TME 0010000000000000000000000000000
Trac 1000000000000000000000000000000
Troc 0000000100000000000000000000000
Tuci 1000000000000000000000000000000
TUCU 101o 11o 111110000000000000000000
W O 0100000000010000000000000000000
XIB 0000000000010000000000000000000
Phle 0000000000001000000000000000000

59
Annex 3. Probable new arbovirus types, isolated only froni phlebotomine sandflies in the Brazilian hiazonia,
1954 - 1992; NC = not classified; NG = not grouped.
Virus name Prototype Genus Antigenic group
Acatinga AR 482250 Orbiviriis Changuinola
Acurene AR 446985 Orbiviriis Changuinola
Almeirini AR 389709 Orbiviriis Cliangu iliola
Altamira AR 264217 Orbiviriis Changuinola
Ambe AR 40798 1 Phleboviriis Phebotomus
Changuinola
Anapu AU 4960 I4 Orbivirils
Aracai AR 425269 Orhiviriis Changuinola
Aratau AR 4288 12 Orbivirirs Clianguinola
Arawete AR 505 172 Orbiviriis Clianguiliola
Ariquenies AR 485678 Phleboviriis Phlebotomus
Aruaiia AR 4288 15 Orbivirtts Chaiiguinola
Assuriiiis AR 482249 Ovbivirtis Clianguinola
Bacajai AR 482267 Orbiviriis Changu inola
Bacuri AR 496008 Orbiviriis Clianguiiiola
Balbina AR 478620 Orbivirils Changuiiiola
Canoa1 AR 433317 Orbivinw Changui noI a
Carajas AR 411391 ksictiloviriis v. s. v.
Catete AR 495605 Orbivirils Cliaiiguinola
Coari AR 433343 Orbivirtrs Clianguinola
Cupixi AR 502545 Orbiviriis Changuinola b

Gorotire AR 48225 1 Orbivirils Clianguiiiola

Gurupi AR 35646 Orbioiriis Clianguinola
Inhangapi AR 177325 ksiciiloviriis NG ”
”
Ipixaia AU 490496 Orhiviriis Cliangu inola
Iriri AR 4080.95 NC NG f
Iruana AU 496021 Orbivirils Cliangu inola
Itaboca AR 496034 Orhiviriis Changu inola
Janianxi AR 243090 Orhiviriis Cliaiiguinola
Jandia AR 440489 Orbivirits Clianguinola
Jatuarana AR 440497 Orbiviriis Changuinola
Joa AR 371637 I%leboviriis Phlebotomus
Jutai AR 397374 Orbivirtrs Changuinola
Kararao AR 447024 Orbivirus Clianguinola
Maraba AR 4 11459 fisiciiloviriis v. s. v.
Munguba AR 389707 Plilcboviriis Plilcbotomus
Oriximina AR 385309 I’hleboviriis Phlcbotomus
Oureni AR 4 1067 Orhiviriis Changuinoln
Pacaja AR 440503 Orbivinrs Changu iliola
Papura AR 450572 NC NG
Parauapebas AR 415962 OrbiviriIS Clianguinoh
Paru AR 397370 Orbivirus Changuinola
Pependana AR 440504 Orbiviriis Changuinola
Pindobai AR 482675 Orhivirus Chaiigu i no la
Piratuba AR 47878 1 Orbivirils Changuinola
Saraca AR 385278 Orbiviriis Changuiiiola
Serra Norte AR 49,8935 Orhivirils Changuinola
Surubim AR 440507 Orhiviriis Cliangu inola
Tapirope AR 434080 Orhiviriis Changuinola
Tekupeu AR 505(169 Orbivirus Chaiiguiiiola
Timbozal AR 44054 1 Orbiviriis Cliangu inola
Tocantins AR 486776 Orbiviriis Chaiigu iliola
Tocam AR 505170 Orbiviriis Changuinola
Tuere AR 484704 Orbiviriis Changuinola
Tumucumaque AR 397956 Orbivirta Changu iiiola
Turuna AU 352492 IWebo virils Phlebotomus
Uatuma AR 478626 Orbiviriis Changuinola
Uriuraiia AR 479776 NC NG
Uxituba AR 452652 Orbiviriis Changuinola
Xaraira AR 490492 Orbiviriis Changu iliola
Xiwanga AR 505171 Orbivirits Changuiriola

60
 An overview of
Arbovirology in Brazil and
neighbouring countries.

L ,.
Edited by:

Anzélia l? A. Travassos da Rosa

Pedro I;: C. Vasconcelos
Jorge R S. Travassos da Rosa

BELÉM
INSTITUTO EVANDRO CHAGAS
1998
. O 1998 by the Evandro Chagas Institute

Published by the Evandro Chagas Institute

P.O. Box 1128
Belém, Pará, Brazil
CEP 66090.000
0055 (091) 226-5262

All rights reserved. Printed in Brazil

This book was printed by

Gráfica Santo aiitonio
Tv. Rui Barbosa, 1080
Belém, Para, Brazil.

An overview of arbovirology in Brazil and neighbouring countries;

edited by Ainélia P.A. Travassos da Rosa, Pedro F.C.
Vasconcelos, Jorge F. S. Travassos da Rosa. Belém: Instituto
Evandro Chagas, 1998.
29Gp.

Includes bibliographies and index

ISBN 85-86784-01-X

1 ..Arboviruses 2. Arbovirus infections I. Travassos da Rosa, .

A.P.A.II. Vasconcelos, P.F.C. III. Travassos da Rosa, J.F.S.
. r

CDD 576.64 n
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