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103
Termites as an Urban Problem in South America
by
Luiz Roberto Fontes1 & Sidney Milano2
ABSTRACT
New data on the distribution and infestation patterns of termites
pests in South American urban areas are presented. This includes
wood-feeding, arboreal, subterranean and soil-dwelling termites. The
evolution of the infestation of the introduced subterranean termite,
Coptotermes havilandi, is studied in the city of São Paulo and four
historic phases are recognized. Changes in the control concepts in each
phase are described. The complex interaction of urban areas, biology of
the pest species, and control operations are discussed and they are
considered decisive in the dynamism of the urban infestation by
termites. The modifications of the original environment by the urban
development, in association with the extinction of the native fauna,
seems to influence strongly the success of pest termites in tropical
environments.
INTRODUCTION
This paper is not a literature review of termite infestations in South
American urban areas. The first three sections present infestation data
for drywood, subterranean and arboreal termites, with case-studies
and literature and original information. The fourth section is a discus-
sion on the concepts of urban infestation by termites and control. The
concepts discussed are not theoretical, but have arisen from, and are
currently being applied to the authors’ routine field work on termite
infestation in Brazil.
The history of studies on termites in urban areas is rather recent in
South America. Before the last 20 years, only scattered reports of
infestation, control procedures and occurrences of termites are found.
But the increased infestation of the early introduced subterranean
termite, Coptotermes havilandi, in the Brazilian southeast region, and
the more recent introduction, and increase in the infestation, of two
species of Reticulitermes into the south region of the continent, have
been starting points in urban termite studies. These took the form of
four meetings and two books, that appeared previously to the XXI ICE.
1Caixa Postal 42043, 04073-970 São Paulo, SP – Brazil. E-mail: lrfontes@uol.com.br
2PPV Controle Integrado de Pragas, Rua Bamboré, 41, 04278-060 São Paulo, SP – Brazil.
E-mail: smilano@cupim.net
104 Sociobiology Vol. 40, No. 1, 2002
The First Meeting of Termitologists of the Countries of the
Mercosul was held December 10 and 11, 1992, in Montevideo, Uru-
guay. Its purpose was to discuss the problems caused by Reticulitermes
lucifugus, which is well established in Montevideo and inflicts severe
damages to buildings and wooden structures. The next 2 meetings were
held in the State of São Paulo, Brazil. The Second Meeting of
Researchers on Termites of the State of São Paulo, Brazil was held
in November 26, 1993, in Rio Claro. Its subject was “Termites as pest
in urban and rural environments in the State of São Paulo”. Despite its
regional approach, it included people coming from distant places in
Brazil. Many pest control operators coming mainly from the large city
of São Paulo attended the meeting and brought to light interesting
questions concerning the control of subterranean termites in urban
areas and their needs for a scientific knowledge on that subject. This
meeting can be considered a historic moment in the relationship of pest
control operators working on urban termite infestations and members
of the scientific community, which, in the near future, will publish
works on some urban issues. The Third Seminar on Termites / Third
Meeting of Researchers on Termites of the State of São Paulo, Brazil
were held February 1 to 3, 1995, in Piracicaba. The Annals of the event
incorporated some papers presented in previous seminars and all
papers presented at the Uruguayan meeting. They appeared as the first
book on termites published in Brazil (Berti-Filho & Fontes, 1995), with
chapters of termites as pest in rural and urban areas and on termite
biology and taxonomy. The Second Symposium of Termitology of the
Countries of the Mercosul was held July 1 to 3, 1996, in Piracicaba.
The papers presented, with the addition of new texts prepared by other
authors, resulted in the second and largest Brazilian book on termites
(Fontes & Berti-Filho, 1998), with chapters on applied termitology,
biology, taxonomy and phylogeny, fossils, archaeology, folklore and a
section about the pioneering termitologists, that was discussed at the
meeting.
The events mentioned above have been strongly directed to the pest
control operators (PCOs), in addition to members of the scientific
community. They have positively contributed to the development of
studies on termite infestations in urban and rural areas, and condensed
much information and many concepts. As an example of the latter, it is
worth mentioning the concept of esthetic pest, introduced by Fernandes
et al. (1998) in the second Brazilian book on termites. Because mound
building termites have always been considered pests of pastures,
without scientific confirmation of their pest status, control has always
been indicated by tradition. The concept of esthetic pest thus expresses
105
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
the authors’ affliction of the psychological inconvenience caused to
farmers and common people, by the simple presence of the mounds in
the pasture landscape. It contrasts with the traditional concept of
economic pest. Indeed, farmers are frightened at the simple thought of
termites, and they do not know that the underground harbors a much
larger numbers of termites than the surface mounds, which are
responsible for maintaining the balance of the soil structure.
The major difficulties for an adequate knowledge of the problems
caused by termites and their control in South America seem to involve
the scarcity of published information on these subjects, the small
number of termitologists (most of them are concentrated in some parts
of Brazil and Argentina), the proliferation of false concepts about
termites among common people, and some older academic and refer-
ence books, that include wrong identification of pest termites, or assign
as pests of certain crops a number of inoffensive termites. Another
major issue, that will be considered ahead in the discussion, is the still
incipient participation of PCOs in the investigation of termites in urban
areas.
Unless otherwise stated, data presented in the following sections are
original studies of the authors. The geographic coordinates of the cities
mentioned are listed after the bibliography.
DRYWOOD TERMITES
The economically most important drywood termites in South Ameri-
can urban areas are three introduced species of Cryptotermes. Few
damages are attributed to the native species of Kalotermitidae. Indeed,
very little has been recorded on the South American urban drywood
termites.
The most important species is Cryptotermes brevis (Walker), origi-
nally described for Jamaica. It is presumed native to the West Indies and
north region of South America. The termite has a large-scale history of
introductions, is now tropicopolitan in distribution, and has extended
its range into subtropical regions too (Edwards & Mill, 1986, Fig. 7;
Bacchus, 1987: 2-5). The distribution map of C. brevis in South America
(Fig. 1) includes previous data obtained from the literature (Araujo,
1970: 539-540; 1977: 12; Araujo & Fontes: 1979: 34; Bacchus, 1987:
42; Bandeira et al., 1998: 78; Fontes, 1998c: 322), except for the
Brazilian Amazon region, for which Mill (1991: 343) quoted no localities,
although he mentioned that the species is one of the commonest
structural pests in domestic buildings. New localities in Brazil are Porto
Alegre and Caxias do Sul, in the State of Rio Grande do Sul, Castro, in
the State of Paraná, Florianópolis, in the State of Santa Catarina,
106 Sociobiology Vol. 40, No. 1, 2002
Bananal, Pindamonhangaba, Ribeirão Preto and Santana do Parnaíba,
in the State of São Paulo, and Ouro Preto and Congonhas, in the State
of Minas Gerais. C. brevis is clearly well distributed in the periphery of
the continent and is present in central Brazil. New collections will
certainly enlarge its geographical distribution, but the species seems to
be absent in some countries, such as Argentina (Torales et al., 1997;
Torales, 1998). In Uruguay, although the termite was listed by Bacchus
Fig. 1. Distribution of
Cryptotermes brevis
in South America.
107
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
(l.c.; sample collected by F. Silvestri in 1920, probably in Montevideo),
it is not mentioned by Aber (1995) and seems to be considered of minor
importance. In Brazil, C. brevis is a serious pest of the structural wood
of historic buildings, and of valuable historic goods in the cities reported
for the States of Minas Gerais (several historic cities, like Ouro Preto,
Mariana and Congonhas), São Paulo and Paraná.
Cryptotermes dudleyi (Banks), apparently of oriental origin, is as-
signed as a pest in Belém, State of Pará, and in the Brazilian Amazon
region (Bandeira, 1998: 89). A species that is probably C. dudleyi is also
pest in João Pessoa, State of Paraíba, in the northeast region of Brazil
(Bandeira et al.: 78). The termite was collected in 1953 in Rio de Janeiro,
in the southeast region of Brazil (Araujo, 1970: 540), but has not been
found again in that city. C. dudleyi was reported from Colombia (Araujo,
1977: 14), although we were unable to find the exact locality. We have
examined a sample of C. dudleyi from Johny Cay, San Andres Island
(12o28’55"N, 81o40’49"W), Colombia, but this is in the Caribbean sea.
Cryptotermes havilandi (Sjoestedt) is an African species, now estab-
lished in northern South America. It was reported from Guyana,
Suriname and Brazil (see Araujo, in Mariconi et al. 1980: 107). The
termite was collected in several regions of Brazil: Santos, State of São
Paulo, and Rio de Janeiro, State of Rio de Janeiro, in the southeast
region (l.c.); Fortaleza, State of Ceará, in the northeast region (Araujo
& Fontes, 1999: 55); Belém and Icoaraci, State of Pará, in the Amazon
region (Constantino & Cancello, 1992: 402). Mill (1991: 343) reported
that C. havilandi is a common structural pest in domestic buildings in
Brazilian Amazonia.
Other drywood termites were reported as pests of structural wood,
fences and furniture, of the genera Cryptotermes, Glyptotermes,
Neotermes and Tauritermes (Fontes & Araujo, 1979: 34; Mill, l.c.;
Bandeira, 1998: 89), but their role in urban areas is unknown.
SUBTERRANEAN TERMITES
Subterranean termites are a serious problem in urban areas. They
are commonly voracious and endogenous in the building structure and
urban trees, showing little or no signs of their presence, except under
severe infestations, when external tunnels are evident.
We recognize two groups of pest subterranean termites, according to
their geographic origin. There are native pest species, of the genera
Heterotermes, Rhinotermes and Coptotermes, for which knowledge is
still incipient. It is difficult to assign their role as urban pests, but in
most cases they seem to act as pests of minor importance or opportun-
ists. A group of major importance is that of the introduced species, that
108 Sociobiology Vol. 40, No. 1, 2002
have arrived from other geographic regions of the world and are now
expanding their range in South America. In this group we mention
Coptotermes havilandi, introduced into the southeast region of Brazil in
the beginning of the last century (or earlier), and two species of
Reticulitermes, whose recent introductions (about the last three or four
decades) in Uruguay and Chile constitute the most spectacular historic
event of the last half of the past century, on South American termites
(Fig. 2).
The tunnels built by subterranean termites are commonly brown to
light brown, with the inner surface lined with a brown to yellowish
mosaic covering of fecal spots. The attacked surfaces commonly are also
Fig. 2. Distribution of
Coptotermes havilandi
,
Reticulitermes lucifugus
and
R. hesperus
in South
America.
111
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
Neotropical Region by Lima (1939: 278, as C. vastator Light), in Rio de
Janeiro, Rio de Janeiro State, Brazil. Subsequently, Araujo (1958: 194;
1970: 542; in Mariconi et al., 1980: 110) remarked that specimens of C.
havilandi (identified by A. E. Emerson; see Araujo, 1958) were first
collected in Rio de Janeiro, Rio de Janeiro State, in 1923, and in Santos,
São Paulo State, in 1934. It was clearly introduced in earlier decades,
since Araujo (in Mariconi et al., l.c.) informed that “... in Rio de Janeiro,
in 1923, ... at the swarming season, the amount of alates in flight looks
like large clouds along entire streets”.
The southeastern coastal cities of Rio de Janeiro and Santos, distant
each other about 500 km, have economically very important harbors
and are historic commercial routes to the inland country. The introduc-
tion of C. havilandi probably occurred in the second half of 19th century,
from infested material unloaded off ships or from swarmings coming
from infested ships (Fontes & Araujo, 1999: 67). Currently, although
rare, ships can house infestations of C. havilandi, as seen in Rio de
Janeiro (Sérgio C. Carvalho/Insetisan Ltd., personal information). No
intermediate infestation has been ever detected in rural places and in
areas of preserved natural vegetation (from open fields to forests) and
it is fairly reasonable to state that the termite has been disseminating
to other cities by human transportation. If the dispersal towards the
west cities has occurred (and still occurs) by transport, it seems most
probable that incipient colonies (from dealate couples to small young
colonies recently established in suitable places, like living plants with
soil, earth with vegetal debris, rubbish and waste material, cardboard
boxes, large paper reels, and other items) are the best candidates to be
dispatched and to establish new infestations into new cities. Such
mechanisms would imply a rather slow emergence rate of new evidently
infested cities, since new colonies grow slowly through several years,
initial swarmings may be discrete and inconspicuous for the common
people, as may also be the pioneering infestations, that can inconspicu-
ously develop in trees, instead of buildings. In fact, the initial dispersal
of the termite was quite slow. The great São Paulo city, only 70 km from
Santos, showed large swarmings about 30 years later, in the ending
60´s or beginning 70´s (Araujo, in Mariconi et al., l.c.: 111; personal
communication of R. L. Araujo to the senior author in 1978). From the
80´s on, the termite has dispersed largely, either in the surroundings
of the mentioned cities as towards the west cities of the country. In
1997, C. havilandi was found in Recife (Fontes & Veiga, 1998; Araujo &
Fontes, 1999: 67), in the Brazilian northeast coast, 2300 km north of
the original introduction cities.
Case 1. Recife, State of Pernambuco, Brazil. Infestations by C.
113
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
large buildings, either connected to the ground or purely aerial infes-
tations, but these issues have not yet been investigated. Infestation of
urban trees has not reached the severity known from cities with a more
ancient infestation history, like São Paulo (Fontes, 1995; 1998a).
According to the biologist and PCO, Mr. Horácio C. Cunha, infesta-
tion by Coptotermes is quite recent in Belo Horizonte. He was first
requested to control a Coptotermes infestation in 1996, in a house.
C. havilandi infests many cities in the southeast region of Brazil, such
as the Rio de Janeiro great metropolitan area, Niterói, Cabo Frio and
Seropédica, in the Rio de Janeiro State, Santos, São Vicente, Guarujá,
São Paulo great metropolitan area, Campinas, Piracicaba, Rio Claro,
Limeira, Porto Ferreira, Taubaté, Jacareí, in the São Paulo State, and
Belo Horizonte, in the Minas Gerais State. In the northeast region, C.
havilandi occurs in Recife, State of Pernambuco. Other locality reports
from the literature should be verified, since the correct identification of
Coptotermes species is not an easy task.
In the end of year 2000, we received from Dr. Enrique Laffont
(University of Corrientes, Argentina) three termite samples from
Asunción, Paraguay. They were collected by him November 22 and 23
in 1998, infesting two living ornamental trees (Flamboyant or Delonix
regia, and Peltophorum dubium) and one dead tree in the University of
Paraguay. The species was identified by L. R. Fontes as Coptotermes
havilandi, and this is the first report of the species outside Brazil in the
South American continental area.
RETICULITERMES
Reticulitermes occurs in the North Hemisphere, with several eco-
nomically important species. The genus has 7 species in the American
continent. Six species are native in the Nearctic region. One of them, R.
flavipes, extends its geographic range as far south as Guatemala, in
Central America, and R. hesperus was introduced in Chile. A seventh
species, R. lucifugus, originated in the Mediterranean area and was
introduced into Uruguay.
Reticulitermes lucifugus (Rossi) was introduced in the city of
Montevideo, Uruguay, probably in the decade of 1960 (Aber & Fontes
1993). The termite is disseminating and extending its geographic range
to the neighbor districts and infestations now occur also in the
downtown area (Aber 1998).
The history of infestation by R. lucifugus in Montevideo is fairly recent
(Aber & Fontes l.c.). Infestations were first noticed in 1968 and became
a social problem in 1976, in the district of Carrasco Norte. This district,
now mainly residential, also has several important national and
114 Sociobiology Vol. 40, No. 1, 2002
multinational manufacturers and factories and is in close vicinity to the
international airport of Montevideo. Any of these could have been
involved in an involuntary importation of the termite. Colonies of R.
lucifugus are common in logs, standing dead trees in private and public
gardens, especially eucalyptus artificial forests in the urban area, all
representing permanent reservoirs of the termite and sources for the
infestation of urban structures.
A voracious pest of structural wood as R. lucifugus was previously an
unknown problem in that temperate country and it represents a real
risk of introduction also into the important neighbor city of Buenos
Aires, Argentina, and into the south region of Brazil, through the
commercial routes to the Rio Grande do Sul State.
Reticulitermes hesperus Banks was reported from Chile in 1986 and
is now an important pest of structural wood and urban trees in the cities
of Santiago and Valparaiso (Cabrera & Camousseight, 1997, 1998). Its
introduction probably occurred earlier than 1986, because in 1998 the
termite was widespread in Santiago, with at least 80 infested areas
occurring in 29 districts, including the downtown area. Cabrera (1997)
attributed the dispersal of the termite inside the urban areas mainly to
the human transportation of construction debris and rubble, plant
debris, packaging, earth and living plants with clods, since it is certainly
faster than by the naturally occurring swarmings. She also reported
damages to plastics, asbestos, aluminum, plaster, polystyrene, card-
board, paper and flax, and attacks to the dead parts of plants in gardens.
HETEROTERMES
Species of Heterotermes are important pests of eucalyptus forests and
the sugar cane culture, in some regions of Brazil. They seem to be casual
pests of rural constructions, poles and fences. Some species cause
urban infestations (Fig. 6), but the damage they inflict to wood
structures is much less important, when compared to that caused by
species of Coptotermes and Reticulitermes.
In some regions, species of Heterotermes are regarded as important
urban pests, as in João Pessoa, State of Paraíba (Bandeira et al. 1998:
79). In Uberlândia, State of Minas Gerais, the agronomist and PCO, Mr.
Telmo Vinicius (personal communication) reports that infestations of
houses and factories are common in the urban and suburban areas. He
also informs that infestations occur in the upper floors of high buildings
in Uberlândia.
The importance of Heterotermes infestation is clearly underestimated
and deserves the attention of collectors.
Case 3. Brasília, capital of Brazil. The Catetinho Museum, mark of
115
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
the foundation of the city, is a two-stories high building made of wood,
in a suburban park. In 1995, it was severely infested by the common
drywood termite, Cryptotermes brevis. However, the base of the wood
studs and some boards of the walls, at the first floor, were infested by
Heterotermes tenuis and also by H. longiceps. They inflicted severe
damage, restricted to the woods in close proximity to the ground. The
boards attacked also showed damage made by fungi, and the base of the
studs was rotten due to the high degree of humidity under the floor (the
floor was made of a concrete layer, enclosing the base of the studs). The
infestation by Heterotermes seemed opportunist, favored by the exces-
sive humidity under the floor.
Case 4. Porto Feliz, State of São Paulo, Brazil. An old one-story farm
Fig. 6. Distribution of
Heterotermes tenuis
,
H. longiceps
and
H. assu
in South American urban
areas.
116 Sociobiology Vol. 40, No. 1, 2002
house, with brick walls that were cemented with a clay mixture, was
severely infested by H. tenuis. Pieces of the plaster that covered the outer
walls were removed on 4 December, and many alates were collected from
the cavities below the plaster. On 17 December 2000, the plaster was
totally removed and this enabled a careful investigation of the termite
invasion. Chambers and tunnels were excavated in the clayey wall
cement and the termite reached the woods of the roof, about 3.5 m above
ground. Some bricks in the walls and some furniture were also
damaged. The infestation was favored by the high humidity degree in
the soil, below the house.
Case 5. Belo Horizonte, State of Minas Gerais, Brazil. Infestations by
H. longiceps and H. tenuis occur scattered on the urban region. Attacks
to fences seem to be common. Infestations of houses appear to be casual
and commonly of minor importance. One case, however, investigated by
the senior author and the biologist and local PCO, Mr. Horácio C.
Cunha, was remarkable due to the severity of the damages. In the rooms
adjacent to the terrain slope, there was a severe infestation and
destruction of door jambs, thresholds and headers, and of some kitchen
cabinets.
H. longiceps (Snyder) was reported as an important pest of historic
and cultural buildings, their furniture, workmanship, works of art and
books, in the city of Corrientes, Argentina (Torales, 1998: 416). Attacks
are scattered in the city and include also houses. In Brazil, we report
infestations by H. longiceps to the wood structure and furniture of
houses and factories in Belo Horizonte and Uberlândia, Minas Gerais
State, Campo Grande, Mato Grosso do Sul State, Brasília, the capital
of Brazil, Presidente Prudente, Campinas and Itapira, São Paulo State,
and Salvador, Bahia State.
H. tenuis (Hagen) is widely distributed in South America. It was
considered an important pest of structural wood in domestic buildings
in the Brazilian Amazônia (Mill, 1991: 343), but a minor pest in Belém,
Pará State (Bandeira et al., 1989; Bandeira, 1998: 91). We report
infestations in some Brazilian cities, as Aquidauana, Mato Grosso do
Sul State, Brasília, the capital of Brazil, and Uberlândia and Belo
Horizonte, Minas Gerais State. H. tenuis infestations seem to be
common in the rural area of Uberlândia, Minas Gerais State (T. Vinicius,
personal communication) and of Piracicaba, São Paulo State (personal
observations of L. R. Fontes).
Another species of Heterotermes was reported from the large city of
São Paulo (Fontes & Araujo, 1999: 75), the economic heart of Brazil. The
termite fauna of São Paulo and surrounding region has been extensively
collected by Araujo, throughout his profitable scientific life, was also
117
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
visited and explored in 1937 by the Italian termitologist, Filippo
Silvestri, and after 1977 has been investigated by the senior author. It
is a reliable statement that the pest species has been introduced
recently into the urban area of São Paulo (it was first collected in 1995,
according to our records) and is gradually spreading and becoming
more important as a pest of buildings (despite the fact that it is far less
voracious than Coptotermes havilandi and much easier to exterminate).
Fontes (in Fontes & Araujo, l.c.) proposed that it could have been
imported from other regions of the world. That means that a long-term
taxonomic study would be desirable, in order to define its species
status, as is appropriate for any important pest species. The species was
described as H. assu by Constantino (2000), who considered that it is
native from the Brazilian Atlantic forest. Although this issue is not
clear, his opinion is accepted in this paper.
We received a sample of H. assu from Petrópolis, State of Rio de
Janeiro, Brazil. It was collected in 1987 and, according to the collector,
the termite has severely damaged three houses at the city outskirts.
Another sample from the same State came from Cabo Frio, collected on
2001 by Dr. André L. Barbosa, who informed us that it was collected
under the bark of a tree. A sample was collected in São Paulo, São Judas
District, in the beginnings of 2001, in the 18th floor (top floor) of a
residential building. According to biologist Beatriz Gromick, the termite
was installed in structural voids (probably in the floor) and was
attacking cardboard boxes.
RHINOTERMES
Rhinotermes marginalis (L.) was described for Suriname and occurs
in the north of South America, mainly in the Amazon Region. The
species was reported as a minor pest of structural wood in the
Amazonas and Roraima States (Mill, 1991: 343) and in the city of Belém
(Bandeira, 1998: 91), Pará State, Brazil. It was recently reported from
the urban area of the city of Rio de Janeiro (Menezes et al., 2000), State
of Rio de Janeiro, in the southeast Brazilian coast, where specimens
damaged skirtingboards in a mansion highly infested by Coptotermes
havilandi. The mansion received chemical treatment and was moni-
tored with pine stakes in the soil of the surrounding garden. R.
marginalis was not collected again, within the next 6 months. This
seems to be a case of species introduction, but the origin of the termite
is unknown.
We recently received a sample of Rhinotermes marginalis from
Vitória, State of Espírito Santo, Brazil. According to the information of
Mr. Edson D. Rocha, an agronomist and experienced local PCO, the
118 Sociobiology Vol. 40, No. 1, 2002
termite is a pest of buildings in that city.
ARBOREAL NESTING TERMITES
Damages to all kinds of human properties and goods appeared early
in the Brazilian literature, in texts dated from the discovery of the land
in the 16th century (Cunha, 1989). The responsible for such attacks are
species of the native fauna. Probably most were caused by species of
Nasutitermes, common in the country and currently urban pests in
several urban regions.
Despite our termite problems that are connected with the distant
past, it is curious that previous to the rather recent introduction and
increase of Coptotermes havilandi in urban infestation, which have
come from other geographic regions of the world and become a problem
in the last 40 years in the SE region of Brazil, no previous scientific
reports were produced on the native fauna. Thus, there is a gap between
the knowledge of our historically damaging original termites, and the
more studied introduced termites.
NASUTITERMES
Infestations caused by species of Nasutitermes are common through-
out South American urban areas (Fig. 7) but scarcely documented.
Several species are involved, according to the geographic region (Bandeira
et al., 1989, 1998; Mill, 1991; Bandeira, 1998; Torales, 1998; Menezes
et al., 2000). Although some species are clearly opportunistic and infest
badly preserved buildings or man-made structures, a small number are
true pest species and may cause important economic losses and social
disturb.
A noteworthy exception are the studies published by Torales and her
collaborators (revised in Torales, 1998), about the infestation caused by
N. corniger in the city of Corrientes, northeastern Argentina. Their
studies provided a clear account of the damages caused by the termite
in the urban part of Corrientes and revealed a case of introduction,
whose expansion is being monitored by the researchers.
The taxonomy of the Neotropical species of Nasutitermes needs
revision. There are about 70 valid names, some of which may prove to
be synonymous, and several undescribed new species. Description of
the alate caste is not available for many species and could provide a
number of good distinctive characters. Information on nesting site and
nest structure help much in the identification work, but they also lack
for many species. When one compares samples from several colonies
and localities, minor morphological variation (sometimes restricted to
the alate caste) suggest that in some cases cryptic species may be
119
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
involved, and complementary morphological studies (including gut
details) are needed to define their species status. Some identifications
of pest species can change in the course of future taxonomic studies.
Comments on the specific identification of some pest termites are
presented in the following item.
PCOs can contribute greatly to the understanding of the taxonomy
of Nasutitermes and other termites, as they have access to a very wide
range of biological manifestations of the pest species (like nests,
tunnels, damages, habits and particular behaviors) and can thus add
much information to the specimens they collect.
Fig. 7. Distribution of
Nasutitermes corniger
,
N. bivalens
and
N. aquilinus
in South American urban
areas.
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Two patterns of infestation can be recognized, according to the
nesting habit. These patterns were defined in the course of an extensive
study conducted by the senior author in several regions of Brazil, and
also from the interpretation of PCO’s information.
Exogenous (or arboreal) pattern
This is the common pattern of infestation, characteristic by the
presence of conspicuous nests in posts, fences, walls, roof beams, trees
and other supports made of wood or of brick and concrete. In buildings,
nests are commonly found in the roofs and parametrical walls. The
nests can also be constructed under floors and inside other hidden
structural voids, although this seems to occur mainly under severe
infestation.
The exogenous or arboreal pattern is associated to the infestation of
urban trees, with typical arboreal nests of Nasutitermes seen in trunks
and branches. Although it is not a rule, the urban trees can constitute
an important reservoir of the termite.
This infestation pattern is common in South American urban areas.
The main species involved seems to be N. corniger (Motschulsky). It is
worth remembering that the first identification of N. corniger, from the
city of Corrientes, by the senior author in 1983 (Torales & Armúa, 1985-
86) may change in a future taxonomic study. The same (or a very close)
species was recognized in samples from other cities, in several regions
of Brazil. Thus, the previous accepted identification is convenient and
must be retained until the taxonomic status of the pest species is
clarified.
Case 6. Corrientes, Province of Corrientes, Argentina. The urban
infestation caused by N. corniger is being currently investigated by G.
J. Torales and her collaborators. This is an example of pest introduc-
tion, that probably occurred in the decade of 1950 (Torales, 1998: 417-
419). Corrientes is a plain city in the margin of Paraná river, with few
high buildings in the downtown area. Termite attacks are restricted to
residential areas surrounding the presumable introduction site, but
the distribution is enlarging. Nests are common in trees and roofs.
Attacks are severe and can affect as much as 68.75% of the houses
(Torales, l.c.).
Case 7. Corumbá, State of Mato Grosso do Sul, Brazil. Infestations
caused by N. corniger are common in all urban areas and affect seriously
the historic buildings of that previously important harbor city in the
margin of Paraguay river. Trees are the main urban reservoir of the
termite (Fig. 9). They are severely attacked and arboreal nests reaching
as much as 70-100 cm in height are common in the main branch of the
126 Sociobiology Vol. 40, No. 1, 2002
rooms and passages, in the large chambers below the stands, and are
common in hidden cavities in the walls, floors and ceilings (Figs. 11-12).
Two large and high buildings (Sion District) have a common base-
ment in a steep incline. Inside that enormous artificial cavern, humid,
warm and inhabited by bats and American cockroaches, there are more
than 15 enormous nests of the termite (some have been removed and
only their dark spots remain in the walls), at variable heights in the walls
and concrete columns (Fig. 13). Some nests are about 4 meters above
ground level, while a few are near the ground. Three nests, at great
height, measured about 2 m in height, 1.5 m in width and project about
0.5 m from the walls. They have a coarse and dark surface. Tunnels in
the walls near the nests can be as broad as 8 cm. The five basal floors
of the buildings are infested by the termite. Biologist Horácio C. Cunha,
an experienced local PCO, informed that in a close neighbor high
building, in that the basement is not sealed by walls and the steep
terrain is exposed, several nests of the termite have been removed. All
nests had been found in hidden places, away from daylight.
According to Mr. Horácio C. Cunha, infestation by Nasutitermes is
recent in Belo Horizonte. His first request to control a Nasutitermes
infestation dates from 1993, in the Sion District. As a biologist, he loves
observing urban pests and he remembers clearly that the first notice-
able swarming of alates, remarkable by the large amount of specimens
in flight along many streets in the Sion District, occurred in October
2000.
Case 11. Piracicaba, State of São Paulo, Brazil. Infestation by N.
bivalens is restricted to few areas, excluding downtown. In the Vila
Resende District, infestation in houses and trees are common. Accord-
ing to information of an ancient local resident, the problem arose about
6 years ago. He attributed the introduction of the pest to the work of
sawmills that existed in the area until the beginning of the 90’s and
would had imported infested timbers.
Infestation by opportunistic species of Nasutitermes
Native species of Nasutitermes can be opportunist pests and attack
structural timber under favorable circumstances. This is more frequent
in rural buildings, and severe damage to historic farm houses is
reported (Paiva, 1998).
We identified N. aquilinus (Holmgren) damaging the roof beams of a
badly preserved historic farm house in Americana, State of São Paulo.
The same species causes damage to rural properties in Corrientes,
Argentina (Torales, 1998: 420).
In São Paulo, State of São Paulo, the greatest urban area in South
128 Sociobiology Vol. 40, No. 1, 2002
America, there have been sporadic attacks of N. ehrhardti (Holmgren),
to wood shelves, door frames and papers (Vila Mariana District), to
fences and poles (Conceição District), and to the structural timber of a
floor (Tamboré District, collected by Mr. E. Sayegh). Damages are of
minor importance.
MICROCEROTERMES
Infestations by species of Microcerotermes in South America are
scarcely documented. In the northeast and north regions of Brazil, they
appear to be mainly opportunistic pests, invading buildings mostly from
colonies located in urban trees and causing more damage to fences and
pieces of wood exposed to direct sunlight (Bandeira, 1998: 91-92;
Bandeira et al., 1998: 82). Mill (1991) reported that M. exiguus (Hagen)
and M. arboreus Emerson are domestic pests and attack wood struc-
tures in the Brazilian Amazon region.
In some regions, M. strunckii (Soerensen) can play a role as major
urban pests, as in the northeast region of Argentina, building nests on
roofs and walls and causing severe damages to structural wood and
paper (Torales et al. 1995; Torales 1998: 422-423).
We examined with PCO Alexandre P. Vasconcelos an attack to a brick
house in Fortaleza, State of Ceará, Brazil, by a species of Microcerotermes.
The termite has invaded the house by tunnels in a perimeter wall and
from the soil in a few other points. It has damaged roof wood beams and
a kitchen cabinet, excavated the plaster of some walls and attacked the
nearby baseboard, and explored the small hollows behind the tiles of the
kitchen walls. Its arboreal nest was found in a tree trunk, in a close
neighbor’s property. The infestation looks opportunist.
SOIL DWELLING AND MOUND BUILDING TERMITES
Mound building and soil dwelling termites are sometimes opportun-
ist pests of buildings, although in some regions they are reported as
important pests. They are frequent in urban gardens, and sometimes
can extensively destroy lawns in yards and football fields, as reported
for Syntermes nanus Constantino and S. praecellens Silvestri in Santo
André and São Paulo, State of São Paulo (Fontes 1998b: 215). Also
Neocapritermes opacus (Hagen) can cause some harm to large yards in
the cities of Ibiuna and São Paulo, State of São Paulo.
In the genus Amitermes, major damages to structural wood is
attributed to A. excelens Silvestri in Boa Vista, State of Roraima, in the
Brazilian Amazonian region (Bandeira, 1998: 92), and to A. amifer
Silvestri in seaside houses in João Pessoa, State of Paraíba (Bandeira
et al. 1998: 82). A. amifer is also a minor opportunist pest in the urban
132 Sociobiology Vol. 40, No. 1, 2002
house foundations that cracks appeared in the walls. The other case
evolved similarly to the latter and was reported in 1999, in a house built
at a slope in Jacarepaguá District, Rio de Janeiro city.
DISCUSSION
Some topics must be pointed out, in order to understand the
problems caused by termites in South American urban areas. We will
refer to our experience in Brazil, which may be a good example to other
countries.
South America is a large continent, mostly within tropical limits, and
with a diverse fauna of termites. Many species are remarkably abun-
dant and may be a distinctive landscape feature in some regions, like
the common mound building termite of the pastures and open lands of
the southern half of Brazil, Cornitermes cumulans (its popular name is
“the little mound-dwelling termite”). Termites are adapted to a great
variety of habitats, either natural or modified by man, like agriculture,
forestry and pasture lands, including any kind of built structures added
to them, and urban areas. ‘Urban area’ is just a general term, because
these areas are not homogeneous. Indeed, the variety of urban pictures
reflects the great diversity of human cultural patterns, scattered in so
many geographically distinct places, as well as, historically speaking,
of building and landscape gardening concepts and techniques that have
succeed in the last century decades. Cities are thus a dynamic
environment within each physiographic and climatic regions, tempered
with paste and present, and with the social, economic and cultural
aspects of the people living there.
The termite fauna adds a double component to the urban infestation
issue. The species of the native fauna are commonly benefic to the urban
environment (as to other man-modified environments; see the short
account presented by Fontes & Araujo, 1999: 44-48), although some
species may become pests or act as opportunist pests under favorable
circumstances. Differently, the foreign species that have been intro-
duced into the continent are all destructive pests, voracious and well
adapted to the urban environment, and ruinous to man-made struc-
tures. Species of the latter group seem to be typically “urban termites”.
Of course, it is not a so simple picture, as components of the native
fauna can also be aggressive to the city organism and can be introduced
into other regions, gradually expanding their geographic limits.
With a so great diversity of cities and termites, it is clear that the
problems caused by termites are typical of each region, even within a
same country. Generalizations about pest termite concepts and control
techniques are not necessarily applicable to regional problems and may
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act, indeed, as deleteriously as the pest termites.
Understanding the Problems Caused by Termites in South
American Urban Areas
Historically, termite control in Brazil has focused on three main
wrong guidelines. First, control is based mainly on concepts imported
from European countries and USA, that have been developed for
different termite species, climates, physiographic features, and differ-
ent urban and social realities. Another error is to focus control activities
mainly on the building, as if termite infestation was a “building disease”
or a “disease of wood in man-made structures”. Finally, a crucial error
is to consider that termites are enemies of mankind and to spread (or
to be omitted in correcting it) such a stupid idea among the population,
PCOs and in some scientific and academic milieu.
When we started thinking seriously about urban infestation by
termites in Brazil, we have not considered the termites themselves as
a problem, but the urban area and its constellation of variable
conditions (Fontes 1995; 1998a: 112-113). The latter includes geo-
graphic, climatic and pedological features, building practices and
patterns of building structures (soil declivity, texture and humidity;
leveling and excavations at the building site; site landscape; founda-
tions; discharge of wastes inside structural voids; use of wastes in the
structure, as to fill up cavities in the soil; building materials; slabs;
walls; wood forms; structural voids; isolating layers or isolating struc-
tures; hydraulics, electric and telephone fittings; architectonic solu-
tions, and many other), proximity between buildings, patterns of use of
the urban soil (subterranean structures; building in steep slopes and
in river plains covered with compacted earth and debris), management
of demolition debris, landscape gardening practices, planting and
management of urban trees, paving, pollution of soil, water and air, all
of these changing in space and time intervals and combined with the
also changing social and economic levels of the local people and their
cultural practices (including the practices of pest control companies).
The listed subjects are not complete within the urban complexity, but
give an idea of it. Termites are just one more ingredient within this
universe. They are not only passive of urban stress, but actively
contribute for the construction of that dynamic universe.
The concepts presented by Fontes & Araujo (1999: 47-48) will spare
us a longer explanation about the title subject. In the sections named
“termites in the man-modified environment” and “termites in urban
areas”, they remarked that the termites are beneficial, although
some species of termites are pests, and, considering the pest
134 Sociobiology Vol. 40, No. 1, 2002
termites, that the drywood termites interact with the food, whereas
the subterranean termites interact largely with the environment.
Now it is clear that the latter concept should include also the arboreal
pest termites. The environmental termite interaction includes all
subjects listed in the above paragraph, that is, with the physical and
biological elements, with the human practices in a broad sense, and it
occurs according to the ability of the termite to respond to the urban
organism stimuli.
Understanding the two concepts presented above, within the com-
plexity of the urban organization, is fundamental to achieve a clear view
of the urban infestation by termites in tropical environments (and
perhaps in any environment). It is not the simple knowledge of aspects
of termite biology, of control techniques and products, or the transport
of laboratory information to the urban field reality. Understanding the
body of complex interactions among termites, humans, and man-made
and man-modified structures and habitats, comprises what we termed
the dynamic of the urban infestation. To put it in a few words, we
study the dynamic of the termite urban infestation by a simple method:
we look at the termite, and watch what it makes. This means that no
foregone conclusion is acceptable: the termite is the protagonist and
reveal us what it makes. What a better place to do it, but in the urban
environment?
São Paulo City, Brazil, as a Case Study on the Evolution of
Subterranean Termite Infestation and Control Concepts
The large city of São Paulo, in the Brazilian southeast region, is a
great laboratory for urban termite studies. Both authors have always
lived there and have witnessed the initial manifestations of the exotic
subterranean termite, Coptotermes havilandi. We will outline the evo-
lution of the control concepts in that complex urban environment.
Prior to the appearance and rise of the subterranean termite,
damages were caused by the common drywood termite, Cryptotermes
brevis. Infestations by other termites, like Heterotermes and Nasutitermes,
have always been rare and regarded as minor problems.
We recognize four historic phases. They are more recent and have not
evolved linearly, so that dates are just approximate. In the future
decades, it will perhaps be possible to look at a more “distant past” and
to obtain a clearer historic view.
Phase 1 or Pre-Cognition Phase
In its early times (before 1970), urban pest control was performed by
few companies, that exploited a little known subject and whose
technicians were not cognizant about pest biology. Control was based
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mainly on the application of chemicals. The words of one of the
pioneering PCOs (Silva, 1987) summarize very well what happened: “...
there were 3 or 4 companies ... the client did not know what he wanted,
we did not know what he wished or needed ... [the client] requested an
application [of chemicals] ...”. The control of urban pests was a very
secondary activity, performed by weakly prepared people and whose
economic and social significance were unknown. Clients and PCOs
valued the power of the “chemical toxicants” (then considered the main
tool in pest control), mainly of the organochlorines, and the concept of
pest eradication. To work on urban pest control was not regarded as an
honorable career, especially by the academic and scientific staffs
(indeed, this has changed only very recently in Brazil, in the last 7 or
8 years).
The experience of the local PCOs was restricted to the control of
drywood termites and infestations were regarded as wood problems.
Chemical treatments were directed to wood, independent of the infest-
ing termite. PCOs did not collect the pests they were trying to control,
so that, when the subterranean termite appeared in scene, control
continued to be directed to the wood in buildings and furniture. No
research institution then worked on the control of urban termites.
As stated in the species section, large swarmings in São Paulo were
noticeable in the ending 60´s or beginning 70´s. Introduction evidently
occurred in early decades, most probably in the downtown area and its
surroundings. Swarmings were restricted to that region, that then
concentrated the most intense city commerce, including the provision
market and other. This historic phase extended approximately until
1986.
Phase 2 or the Subterranean Termite as a Soil-Dwelling Termite
The subterranean termite appeared as a major problem in some
areas of the city. Attacks affected, in the beginnings of the infestation
period, the downtown area, a crucial and economically important
region, with many offices, banks and trade activities.
In 1975, Institute of Technological Research (IPT, where the junior
author worked from 1974 to 1986), in São Paulo, the Brazilian
pioneering research institute on wood technology, started investiga-
tions of termite control in buildings. The first training courses on wood
preservation and termite control were ministered in the end of the 70’s
and beginning of the 80’s. These courses commonly were attended by
few PCOs. IPT was also the pioneer in the edition of the first book, in
Portuguese language, with a large chapter on wood destroying agents,
including also non-biological agents (Oliveira et al., 1986), and a
chapter on their control, focused mainly, but not exclusively on termites
136 Sociobiology Vol. 40, No. 1, 2002
(Lepage et al., 1986). This book marked the beginning of historic phase
2. Control has finally been based on scientific information, explained in
the book published by IPT. The technological approach then adopted to
control the termite infestation was based mainly on the traditional
concepts and practices. Control methods were adapted from the
literature on subterranean termite infestations in European countries
and USA. As a rule, it was recommended chemical treatment of the soil
for controlling the infestation, and of the wood for preventing return of
infestation. It was a generally accepted idea that all infestations come
from the ground or had obligatory contact with the ground. The
methods used to control Reticulitermes infestations in USA and Europe
were accepted and chemical treatment of the soil was obsessively
recommended for eradicating all cases of C. havilandi infestations, even
those installed in the upper floors of high buildings. In addition to soil
treatment, chemical treatment of the wood was universally adopted as
a tool for preventing reappearance of infestation, if the termite was able
to surpass the soil chemical barrier.
In this period, the subterranean termite has extended its geographic
range in the urban area of São Paulo, far beyond the downtown and
surrounding region. The new infestations radiated out from the central
introduction region, what suggests strongly a slow dispersion by
swarmings. This was confirmed by Milano (unpublished) in 1999. He
had previously studied two urban buildings that he knew exactly when
they became infested by C. havilandi, and this enabled him to estimate
the dispersion rate of the infestation between the two buildings as 250-
300 meters/year. Such a result agrees with a swarming dispersion
pattern. He also calculated that, if the termite had been originally
introduced in the downtown area, then it happened in ending 1950’s or
beginning 1960’s. These dates are also compatible with the first
noticeable swarmings, known from beginning 1970’s (Araujo, in Mariconi,
l.c.: 111; personal communication of R. L. Araujo to the senior author
in 1978).
A malappropriate term arose in the beginnings of phase 2 and
resulted (and still results) in much confusion and misinterpretation of
urban infestation issues. That is the designation of the subterranean
termite as “soil termite” (meaning soil-dwelling termite). Despite the
efforts of the authors, this term is still much in use, either by common
people as by applied technological and scientific researchers, among
who incredibly it has found defenders! This historic phase expired
around 1990.
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Phase 3 or the Subterranean Termite as a Building Disease
Time is up and the city greatly increased its population and geo-
graphic area. The urban picture changed to a vertical profile of large and
dense high buildings. Some building construction techniques, adopted
in the two previous decades, were noted to favor infestations strongly
by subterranean termites. By reason of economy, much of the construc-
tion wastes, that should have been discharged, were inside the building
structure, accumulated under the ground floor, under the kitchen and
bathroom slabs in upper floors, or in other structural voids. Also, there
were too many structural voids, added to the building for esthetic or
other reasons, and high humidity was favored by closed voids and metal
hydraulic pipes. All of these enabled termite colonies to be installed
inside the building, from the ground to the top floor, to favor high
infestation levels and they caused serious trouble for control activities.
Soil infestation still was a concept universally adopted, but the
control strategies were strongly focused on the nests inside the building
structure. Aerial infestations were common inside structural voids and
these nests should be found and removed, in order to control the
infestation.
Despite the scientific approach, subterranean termites were re-
garded basically as a disease of buildings. Their occurrence outside
buildings, like in street and garden trees, was recognized, but the real
problem was considered to be the close interaction of termite versus
building.
PCOs were much interested in the problem of urban termite infesta-
tion, considered by them a promising working field, although difficult
and requiring specialized knowledge and skill.
In the meantime, Reticulitermes lucifugus has arisen as a problem in
the city of Montevideo, Uruguay (Aber & Fontes, 1993) and a scientific
meeting was organized there in 1992. A second meeting, despite its
regional scope, was organized in 1993 in the city of Rio Claro, near São
Paulo, and was attended by dozens of PCOs from São Paulo city, that
were looking for information on the control of Coptotermes infestations.
This historic phase continued until around 1998.
Phase 4 or the Subterranean Termite as an Environmental
Component
From 1993 onwards, a new set of environmental concepts, related to
subterranean termite infestations, was communicated in lectures and
published in 1995 (Fontes, 1995). Additions were presented in further
texts (Fontes, 1996; 1998a; Fontes & Araujo, 1999).
The first step was the introduction of the urban trees in the termite
138 Sociobiology Vol. 40, No. 1, 2002
problem. In São Paulo, as is true for many other cities, urban trees are
an important reservoir of C. havilandi. Living trees, stumps and tree
subterranean remains can contribute to the prime infestation of
buildings, to the return of infestation to treated buildings, and to
unsuccessful control operations. Trees are also subjected to infestation
that comes from infested buildings. But trees are only part of a major
organism, and the complete concept included a trinominal composed of
termite biology, urban complexity and pest control operations.
Termite biology expresses the potential of the species as a pest. It
determines the full range of damage and activities of termites in urban
areas, some of which have initially surprised experts on termite control
and scientific researchers. As an example, we mention the ability of C.
havilandi to consume (or, more correctly and updating previous biologi-
cal information, the avid or enthusiastic consuming of) gypsum arti-
facts and other calcium rich products, like the plaster covering of brick
walls. Another example is the capacity of the termite in excavating
bitumen used to seal floor slits.
Urban complexity includes the set of characteristics presented in the
previous item, subjected to spatial diversity (heterogeneity of habitats
and of building patterns in a same city) and to historic diversity of
methods, materials and urban practices in the course of time.
Pest control operations can encourage a termite infestation, if it is
underestimated and receives partial treatments (if only chemical treat-
ment is considered, treatment is also partial). Conversely, an overesti-
mated infestation adds excessive cost, client disturbance and environ-
mental or building contamination with chemical products.
The trinominal or environmental scope express a more comprehen-
sive concept on the urban termite subject. It means that complex
interactions determine the success of the termite in the urban habitat,
as well as of the control operations. It means also that tradition, either
from scientific studies of the pest biology, as from skill obtained from
field control activities, is unsatisfactory and cannot determine the
major control guidelines. Control is not dependent exclusively on
scientific knowledge and practical skills, or on the sum of these factors.
It is essential to add a broad urban view, in its full spatial and time
dynamic and complexity. A broad urban universe approach, consider-
ing buildings and their complete surroundings, all kind of man-made
structures, termites, previous control operations, history and culture,
is required to harmonize a serious control work. Termitologists are
especially requested to assimilate this broad view.
From that time on, a series of urban investigations was and is being
conducted by the authors in São Paulo and other cities. They consoli-
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dated previous ideas about the environmental role of subterranean (and
also arboreal) termites in urban areas, and the complexity of the
human, termite and city interactions. The research tool employed in
understanding such complex problem is the study of the dynamic of the
urban infestation by termites, which concept was explained in a
previous item.
Conclusive Remarks on the Historic Study
The introduction and dispersal of the subterranean termite in São
Paulo appeared as a disruption in the urban organization. Control has
been a major challenge for local PCOs. But PCOs and scientists have
benefited from that apparently unfortunate fact, because many urban
concepts had to be revised and are changing. It was a power for good,
if we consider that there is a slow, but gradual evolution of concepts
related to building engineering and architecture, landscape gardening,
preservation of historic and cultural goods, and urban pest control.
In practical terms, currently many PCOs in São Paulo still develop
their control work as described for historic phases 1 and 2. The control
performance of most of those classified within phase 3 is not yet in full
accordance with the concepts required by phase 3. But great progress
was obtained in the last 10 years and Brazilian PCOs take advantage
of the São Paulo experience. Phase 4 is just beginning.
A deleterious hindrance on control course, however, still survives in
Brazil. It is the wrong concept of C. havilandi as a soil-dwelling termite
(vulgarly named “soil termite”), referred in historic phase 2. We list five
good reasons to banish that nonsense and refer correctly to C. havilandi
as a subterranean termite. Subterranean termites (1) compose a well-
defined taxonomic group (family Rhinotermitidae), what (2) common
designation is readily recognized worldwide. (3) They explore the soil
(excavate tunnels and use soil particles as modeling material, but these
are not obligatory tasks) in their search of wood, while soil-dwelling
termites are dependent on the soil for food, water and shelter. The
wrong concept (4) induces common people to consider soil-dwelling
termites, common in gardens and lawns, as pests of buildings, and
causes a behavior that ranges from the simple fear of termites to an
unbalanced and obsessive fright of termites. It also (5) causes PCOs to
assimilate the false idea that any termite found in the soil is a pest, so
that they propose costly and unnecessary chemical treatments to their
clients.
Why has Coptotermes havilandi Evolved as a Major Urban Pest
in Southeastern Brazil?
It is not a creative input to ecology to state that termites are the main
140 Sociobiology Vol. 40, No. 1, 2002
decomposers of wood in southeastern Brazil. But is worth remembering
that the urbanization process affected very strongly the harmonious
composition of the original fauna in the places now occupied by
metropolises in that tropical region. Cities like Rio de Janeiro and
mainly São Paulo have too many people, buildings and areas covered by
concrete and paving. This has not happened suddenly, but composes a
process in the course of the last 30 or 35 years, intensified in the last
20 years. The urban profile changed drastically and, for a long time past,
Syntermes praecellens and S. nanus were captured by the authors from
their holes in the soil surfaces with the aid of a delicate grass stem, in
the open fields of the then suburban districts of Jabaquara (type locality
of S. praecellens), Congonhas and Ipiranga, in São Paulo city.
Details of the historic evolution of Coptotermes havilandi in São Paulo
are presented in the species section and in the previous item. However,
why has it become a so important urban pest? Obviously, the changes
in the natural ecosystem, the strong urbanization, the biology of the
termite, and our previous wrong concepts about the species, all have
contributed to the success of the termite. But the specific contributions
of each of those subjects is merely speculative. For example, is the lack
of predators in the urban environment an important cause of C.
havilandi success? Or the lack of lawns and gardens in the general
urban landscape? Again, the city of São Paulo is our domestic field
laboratory and we have made a series of field observations that furnish
some hints about this issue. Two illustrative cases are presented below.
Case 13. The senior author worked for 18 months, in years 1995 and
1996, at the University of São Paulo mayor office (Butantan District), as
advisor on termite infestation and control. The campus has large
buildings, separated by extensive lawns with many trees. Trees are
commonly isolated, but in many places their crowns touch each other
and constitute a canopy. Birds, spiders and a great variety of insects are
common, and the campus is a really enjoyable place, despite the
existing vegetation is totally divorced from the original vegetation that
covered that area. Infestations of C. havilandi were diagnosed in
buildings and trees, and it was surprising that trees in some extensive
and nice lawns were also infested. In some places, trees were important
reservoirs of the termite and exchanged infestation with buildings (see
Fontes, 1998a).
It is clear that the simple presence of extensive urban lawns, trees
and diverse fauna do not interpose a serious obstacle to the introduced
subterranean termite.
Case 14. An urban park at the back of the Paulista Museum (Ipiranga
District), in spite of being affected by the urban influence and by people,
141
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—Termites as an Urban Problem in South America
still preserves a fragment of the original Atlantic forest environment,
inside the city area. It is crossed by cleared passages for walking and
sports, but outside the passages the ground is covered by a litter layer
of decaying fallen leaves and humus. Trees are high and relatively
dense, the canopy results in a shady environment, and direct sunlight
only reaches the floor in small, local flecks and only during the middle
hours of the day. The shrub layer is, however, very poorly represented
and is being constantly cut down. The forest is surrounded by buildings
and streets, and its margins are exposed to sunlight or influenced by
surrounding buildings and walls. It exemplifies a typical forest frag-
ment under strong urban influence. Large swarmings of C. havilandi
occur in that district at least since 1990, according to the observations
of the junior author, who has lived there since his birth. Such
swarmings can easily cover all the forest area. In middle 2001, we
explored the area and noted that the soil-dwelling termite, Procornitermes
lespesii is very abundant, followed by Neocapritermes opacus. The
density of P. lespesii appears impressively high and this is probable the
result of the urban influence on the forest. It is very interesting that C.
havilandi, despite infesting many trees in the Museum gardens and in
all the nearby streets, invaded only the trees at the forest margins. Some
of the infested trees had their trunks hollowed out by the termite, and
some have been removed, because of the risk that they could fall and
hurt people or destroy perimeter walls.
Although it is not conclusive, it seems more likely that the dominant
soil-dwelling termites are strong competitors and prevent invasion of
their habitat (including the trees inside the forest) by the introduced
subterranean termite.
Very few has been studied about urban ecology in Brazil. These two
cases raise the issue that the native species in the soil and woods are
strong competitors, that can make difficult or avoid the proliferation of
pest species. The same mechanism should also prove to be important
in culture lands and pastures. In strongly modified urban areas, the
construction of high buildings, that are necessarily preceded by the
removal of the top soil, sometimes to considerable depths, and its
substitution by extensive areas of new soil, artificially covered by lawns
and trees, results in the extinction of the original soil environment and
its termite fauna. The vacant niche can be occupied by the pest
subterranean termite, C. havilandi. Perhaps does this process explain
the recent proliferation of the same pest termite in Recife (see Case 1)?
Does the Occurrence of Termites in the Building Area and its
Surroundings Represent Risk of Damages?
142 Sociobiology Vol. 40, No. 1, 2002
The cities in tropical regions can preserve part of the original fauna
of termites. Although the stress represented by the urbanization
process probably forced the disappearance of several native species,
others can survive in vegetation preserved areas and other are adapted
to the new conditions represented by urban parks, gardens and
buildings with preserved green areas. As an example, in the city of São
Paulo, the greatest urbanized area in South America, very polluted,
densely populated and with few green areas, 18 species of termites were
identified (Fontes, 1995: 59). These include the introduced pests,
Cryptotermes brevis and Coptotermes havilandi, but the other 16 are
native species. In addition, there is a number of unidentified soldierless
termites, of the subfamily Apicotermitinae.
In São Paulo, excluding the most dramatically urbanized areas that
eliminated every trace of exposed soil surface, native species commonly
survive, occasionally in close proximity to buildings. For example, in
areas surrounded by trees, gardens and extensive lawns, the mound
building termite, Cornitermes cumulans, the grass foragers Syntermes
nanus and S. praecellens, and the ground dwelling Embiratermes
festivellus are common and specimens eventually can be found inside
buildings, mainly bellow boarded floors at ground level degraded by
humidity and fungi.
Case 15. In the 80’s, at the Forest Research Institute, placed in a very
well preserved urban park and vegetation reserve, the boarded floor of
a one-story building was frequently invaded by a foraging column of a
species of Syntermes, despite the efforts of the civil-servants working
there, that plugged several times the few emerging holes between the
floor boards (Dr. Edson P. Teixeira, personal communication, observed
also by L. R. Fontes).
In other residential areas in São Paulo, much more urbanized but still
with gardens and lawns, we mention Neocapritermes opacus,
Procornitermes lespesii, Cornitermes cumulans and soldierless termites,
which are common in the soil of gardens (commonly under stones and
concrete tiles on the soil surface) and sometimes invading bellow rotten
and humid boarded and inlaid floors.
Case 16. In 1997, the senior author visited a nice one-story house in
the Brooklin District, city of São Paulo, infested by Coptotermes
havilandi. In the front part, around the entrance door, the termite
obstructed some electroducts and damaged the wood frames of some
doors. In the front garden, a tree fell down and the remaining stump was
infested. No sign of infestation nor damages were found at the back
rooms and the backyard. The proprietor, however, was anxious because
she had removed the inlaid wooden floor of a back study room and
143
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et al.
—Termites as an Urban Problem in South America
discovered some termite tunnels below the floor. According to the
previous evaluation of three pest control companies, it would be
necessary to treat chemically all the building and to apply a chemical
barrier in the perimetral inner and outer walls. She disapproved such
proposal, since no evident damages were found at the back rooms and
she was afraid of chemical contamination by odor in the backyard and
at her studying room. Indeed, what happened is that Neocapritermes
opacus, common among the roots of grass tussocks and below paving
stones in the backyard, decided to invade the rotten woods of the humid
floor and constructed tunnels made of dark earth. She was then
recommended to treat chemically the area infested by Coptotermes, and
to correct the water infiltration in the back of her house, without no
further treatment in that area. The termite problem was solved, as well
as the previously undiagnosed humidity problem.
Case 17. A large house surrounded by an extensive garden with
many high trees and shrubs. In 1996, a tree, 10 m away from the house,
fell down and it was infested by termites. In the words of the proprietor,
“termites were swarming from the ground, almost daily after rains. Pest
control companies have recommended a complete chemical barrier around
the house to avoid termite invasion, and removal of the soil of the garden,
followed by chemical treatment of the residual soil and also of the new
substitution soil”. He was very worried about the insecticide inundation
around his house and the health risk this would cause to his family,
about the risk of termite infestation of the main house, and about the
monetary costs of such enterprise. In 28 September, 1997, the senior
author visited the house and was lucky because he arrived at 10 AM at
a drizzle and the proprietor, surrounded by some of his relatives, was
desperately crying because termites were swarming from dozens of
small holes in the ground of that lovely garden. That “swarming in the
rain” scene would really be delightful for a termitologist, if it was not for
that embarrassing picture of familiar desperation. A careful inspection
all over the area revealed that the stump was infested by Coptotermes
havilandi, but no other sign of subterranean termite infestation was
found. The swarming termite was a species of Aparatermes
(Apicotermitinae). Control recommendations included the removal of
the tree stump and its roots, followed by chemical treatment of the root
remains, and the care about the garden against Coptotermes, with the
aid of discrete soft wood stakes applied in the soil. Concerning the
swarmings and the presence of termites in the soil, the proprietor was
told about the beneficial role of soil-dwelling termites in the soil ecology.
The problem was solved.
It is clear that our knowledge about the biology of termites in urban
144 Sociobiology Vol. 40, No. 1, 2002
areas is incipient. The invasions of buildings by Cornitermes cumulans,
in the city of Rio Claro (see Case 12), show that even in the absence of
typical mounds there may exist wholly subterranean colonies of C.
cumulans, which mature and produce alates and explore the soil largely,
including under large buildings. C. cumulans colonies are polycalic
(Fontes 1998b), a feature that probably enables the termite to explore
large territorial areas. Colony maturation without building the typical
mound was previously unknown for this termite. Such behavior
demonstrates that even under high injurious pressures, meaning
destruction of all visible mounds, the termite can successfully survive
and adapts to the new condition represented by urban sites. Indeed, this
may be true for other situations, like extensive sugarcane plantations
in southern Brazil, where Cornitermes cumulans is common in the soil,
consumes plant debris on the surface, and swarms in the proper
seasons, but no mound is visible anywhere (Fontes & Pizano, unpub-
lished).
Mound building and ground-dwelling termites are common in the soil
surrounding buildings and can act as opportunist invaders of buildings.
They commonly inflict no true damage and only few, probably foraging
specimens, are found. These occurrences deserve the particular atten-
tion of PCOs. Besides those cases reported above, we know of several
chemical control treatments that have been immoderately indicated
because inoffensive termites had been confused with the harmful
species of subterranean termites (mainly Coptotermes havilandi). Such
errors mean high economic and environmental costs, and reveal a
suspicious competence of many PCOs.
The Role of Brazilian Pest Control Operators (PCOs) in the
Scientific Knowledge of the Pest Termites
PCOs have contributed with many specimens and much of the
valuable information presented in this paper. They have also selected
interesting case studies, to be discussed or inspected by the authors in
the opportunity of their visits, courses and lectures.
The meetings and literature referred in the introduction of this paper
were intended for scientists and also PCOs, as the latter were previously
deprived of scientific background and instructions. It is the authors’
opinion that this professional class represents the eyes and arms of
urban scientists. They must be encouraged to collect specimens and
information, to request scientific investigation of infestation problems,
and to publish the results of their field investigations and routine work,
if convenient in association with scientists. Brazilian PCOs have proved
that this association is profitable.
145
Fontes, L.R.
et al.
—Termites as an Urban Problem in South America
Future Trends of Termite Control
Control of termites is a major challenge in tropical urban areas, as
it is also in agriculture lands. There is a great deal of chemicals, ranging
from the old organochlorines of the 50’s to the modern very low dosage
products and the non-contaminating baits. Diagnosis and control
operations also combine a simple screwdriver and modern technology
implements. The authors understand that all kind of products and
equipment are merely tools for termite control. All have had their time
in history and all can be currently used, if they are correctly indicated.
This issue is not a frequent concern and, indeed, it is disconcerting to
know that scientists and technology researchers sometimes viciously
assume that new developments in control technology are the ultimate
answers to control. Although seemingly most unintentional, this biased
attitude toward an oversimplification of control is injurious to most
PCOs, that are not so instructed and look for a standard control
prescription.
An environmental approach to control concepts, from our stand-
point, is more appropriate to the complexity of the urban universe. The
trinomial delineated in the above section is an effort in that direction.
Urban areas must incorporate harmony between their physical and
biological constituents. PCOs need much orientation on control con-
cepts and practices. Termites are not invited guests, but they appreciate
living in urban areas and can teach us much about the urban nature.
The dynamic study of the urban infestation by termites gives a more
comprehensive idea of the problem and the guidelines of control.
Short to long-term changes of the urban landscape and urban
components must be considered within the scope of a Termite Control
Program (Fontes & Araujo, 1999: 78-79), instead of an eradication goal.
A control program is adequate for drywood termites, as incipient
colonies are hardly diagnosed and can cause return of the infestation.
It is undoubtedly more effective for the control and follow up of
subterranean and arboreal termites. A control program is instructive to
the client and also will reduce the risks of damage caused by the
unexpected return of the infestation, reduce costs if new treatments are
indicated, and enable the PCO to operate properly in case the building
or its surroundings are to be remodeled.
ACKNOWLEDGMENTS
Aventis Crop Science Brazil contributed greatly to the field research
conducted by L. R. Fontes throughout Brazil, and he is particularly
grateful to the agronomists Pedro Lopes, Daniel D’Andrea and Nilton
Souza Santos. Many PCOs contributed with specimens, valuable
146 Sociobiology Vol. 40, No. 1, 2002
information and help. We mention Alexandre P. Vasconcelos (APV
Desinsetização Ltd.), Daniel Lopes (Verum Saude Ambiental Ltd.),
Eduardo Sayegh (Tecsan Ltd.), Edson D. Rocha (Detisan Controle de
Insetos e Roedores Ltd.), Ginival D. Dantas (Bahia Controle de Pragas
Ltd.), Horacio C. Cunha (Ambiente Controle de Insetos e Roedores Ltd.),
Itiel Genes, Daniel Schor and Estefanio Pontes (F.Genes Saúde Ambiental
Ltd.), João V. Almeida (DDSul Saneamento Ltd.), Joaquim Porto and
Rudval Ramos (CPN Ltd.), Márcia R. Mauro (University of São Paulo,
Pest Control Division), Miguel L. Gouveia (Nova Pioneira Controle de
Pragas Ltd.), Paulo C. J. A. Pinto (DDBala Ltd.), Sérgio C. Carvalho
(Insetisan Ltd.), Sergio M. Florindo (Magno Saneamento Ltd.), Telmo
Vinicius (Praga Engenharia de Controle e Saneamento Integrado Ltd.)
and Walter Amorin (Sani System Ltd.). We thank also Dr. Enrique
Laffont (University of Corrientes) for information and specimens of C.
havilandi from Paraguay, Dr. Edson P. Teixeira (Agronomic Institute of
Campinas) and biologists Beatriz Gromick (Dow Agrosciences), André L.
Barbosa and Francisco J. C. Ferreiro, for information and specimens.
We hope that other PCOs and scientists are not disappointed if their
names are not listed here. We apologize, because they are too many to
call to mind, but we heartily acknowledge all the help and information
we have received from them.
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150 Sociobiology Vol. 40, No. 1, 2002
LIST OF GEOGRAPHIC COORDINATES OF CITIES
Alcântara 02º 24´ 32´´ S; 44º 24´ 53´´ W
Americana 22º 44´ 21´´ S; 47º 19´ 53´´ W
Aquidauana 20º 28´ 16´´ S; 55º 47´ 14´´ W
Asunción 25º 18´ 00´´ S; 57º 37´ 00´´ W
Bananal 22º 41´ 01´´ S; 44º 19´ 24´´ W
Belém 01º 27´ 21´´ S; 48º 30´ 16´´ W
Belo Horizonte 19º 55´ 15´´ S; 43º 53´ 16´´ W
Blumenau 26º 55´ 10´´ S; 49º 03´ 58´´ W
Boa Vista, RR 02º 49´ 11´´ N; 60º 40´ 24´´ W
Brasilândia de Minas 16º 59´ 52´´ S; 46º 00´ 50´´ W
Brasília 15º 46´ 47´´ S; 47º 55´ 47´´ W
Buenos Aires 34º 36´ 00´´ S 58º 27´00´´ W
Cabo Frio 22º 52´ 46´´ S; 42º 01´ 07´´ W
Campinas 22º 54´ 21´´ S; 47º 03´ 39´´ W
Campo Grande 20º 26´ 34´´ S; 54º 38´ 47´´ W
Castro 24º 47´ 28´´ S; 50º 00´ 43´´ W
Caxias do Sul 29º 10´ 05´´ S; 51º 10´ 46´´ W
Congonhas 20º 29´ 59´´ S; 43º 51´ 28´´ W
Corrientes 27º 27´ 00´´ S; 58º 46´ 00´´ W
Corumbá 19º 00´ 33´´ S; 57º 39´ 12´´ W
Florianópolis 27º 35´ 48´´ S; 48º 32´ 57´´ W
Fortaleza 03º 43´ 02´´ S; 38º 32´ 35´´ W
Guarujá 23º 59´ 35´´ S; 46º 15´ 23´´ W
Icoaraci 01º 17´ 20´´ S; 48º 28´ 00´´ W
Ilhéus 14º 47´ 20´´ S; 39º 02´ 58´´ W
Itabuna 14º 47´ 08´´ S; 39º 16´ 49´´ W
Itapira 22º 26´ 10´´ S; 46º 49´ 18´´ W
Jacareí 23º 18´ 19´´ S; 45º 57´ 57´´ W
João Pessoa 07º 06´ 54´´ S; 34º 51´ 47´´ W
Limeira 22º 33´ 56´´ S; 47º 24´ 06´´ W
Manaus 03º 06´ 07´´ S; 60º 01´ 30´´ W
Montevideo 34º 53´ 00´´ S; 56º 11´ 00´´ W
Niterói 22º 53´ 00´´ S; 43º 06´ 13´´ W
Ouro Preto 20º 17´ 15´´ S; 43º 30´ 29´´ W
Petrópolis 22º 30´ 18´´ S; 43º 10´ 43´´ W
Palhoça, SC 27º 38´ 43´´ S; 48º 40´ 04´´ W
Pindamonhangaba 22º 55´ 26´´ S; 45º 27´ 42´´ W
Piracicaba 22º 43´ 31´´ S; 47º 38´ 57´´ W
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—Termites as an Urban Problem in South America
Porto Alegre 30º 01´ 59´´ S; 51º 13´ 48´´ W
Porto Feliz 23º 12´ 56´´ S; 47º 31´ 26´´ W
Porto Ferreira 21º 51´ 14´´ S; 47º 28´ 45´´ W
Presidente Prudente 22º 07´ 32´´ S; 51º 23´ 20´´ W
Recife 08º 03´ 14´´ S; 34º 52´ 52´´ W
Ribeirão Preto 21º 10´ 39´´ S; 47º 48´ 37´´ W
Rio Claro 22º 24´ 41´´ S; 47º 33´ 41´´ W
Rio de Janeiro 22º 54´ 10´´ S; 43º 12´ 27´´ W
Salvador 12º 58´ 16´´ S; 38º 30´ 39´´ W
Santana do Parnaíba 23º 26´ 39´´ S; 46º 55´ 04´´ W
Santiago 33º 28´ 00´´ S; 70º 39´ 00´´ W
Santo André, SP 23º 29´ 50´´ S; 46º 32´ 18´´ W
Santos 23º 57´ 39´´ S; 46º 20´ 01´´ W
São Paulo 23º 32´ 51´´ S; 46º 38´ 10´´ W
São Vicente 23º 57´ 47´´ S; 46º 23´ 31´´ W
Seropédica 22º 44´ 38´´ S; 43º 42´ 27´´ W
Taubaté 23º 01´ 35´´ S; 45º 33´ 19´´ W
Uberlândia 18º 55´ 09´´ S; 48º 16´ 38´´ W
Valparaiso 33º 01´ 00´´ S; 71º 33´ 00´´ W
Vitória 20º 19´ 10´´ S; 40º 20´ 16´´ W