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10.1007/s10531-007-9190-6
Biodiversity and Conservation
© Springer Science+Business Media B.V. 2007
10.1007/s10531-007-9190-6
Original Paper
Contribution of cocoa plantations to the
conservation of native ants (Insecta:
Hymenoptera: Formicidae) with a special
emphasis on the Atlantic Forest fauna of
southern Bahia, Brazil
Jacques H. C. Delabie
1, 2
, Benoît Jahyny
1, 3
, Ivan Cardoso do Nascimento
1
,
Cléa S. F. Mariano
1
, Sébastien Lacau
1, 4, 5
, Sofia Campiolo
1, 6
,
Stacy M. Philpott
7
and Maurice Leponce
8
(1) UPA Laboratório de Mirmecologia, Convênio UESC/CEPLAC, Centro de Pesquisas do Cacau,
C.P. 07, 45600-000 Itabuna, Bahia, Brazil
(2) Departamento de Ciências Agrárias e Ambientais (DCAA), Universidade Estadual de Santa
Cruz (UESC), 45650-000 Ilheus, Bahia, Brazil
(3) Laboratoire d’Ethologie Expérimentale et Comparée (LEEC, CNRS UMR 7153), Université
Paris-Nord, 99, avenue J.-B. Clément, 93430 Villetaneuse, France
(4) Laboratório de Zoologia e de Parasitologia Animal, Departamento de Estudos Básicos e
Instrumentais (DEBI), Universidade Estadual do Sudoeste da Bahia (UESB), BR415, Km03, s/
no, 45700-000 Itapetinga, Bahia, Brazil
(5) Laboratoire d’Entomologie, Museum National d’Histoire Naturelle, 45 rue Buffon, 75005 Paris,
France
(6) Departamento de Ciências Biológicas (DCB), Universidade Estadual de Santa Cruz (UESC),
45650-000 Ilheus, Bahia, Brazil
(7) Department of Environmental Sciences, University of Toledo, Toledo, OH 43606, USA
(8) Royal Belgian Institute of Natural Sciences, 29 Vautier Street, 1000 Brussels, Belgium
Jacques H. C. Delabie (Corresponding author)
Email:
delabie@cepec.gov.br
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Benoît Jahyny
Email: jahyny@leec.univ-paris13.fr
Ivan Cardoso do Nascimento
Email: icardoso@hotmail.com
Cléa S. F. Mariano
Email: camponotu@hotmail.com
Sébastien Lacau
Email: slacau@uesb.br
Sofia Campiolo
Email: campiolo@uesc.br
Stacy M. Philpott
Email:
stacy.philpott@utoledo.edu
Maurice Leponce
Email:
Maurice.Leponce@naturalsciences.be
Received: 22 September 2006 Accepted: 5 April 2007 Published online: 31 May 2007
Abstract By maintaining a forest-like structure, shaded cocoa plantations contribute to the
conservation of ants that usually live in the soil, leaf litter or canopy of tropical forests. Here
we synthesize the available information on the diversity and community structure of ants in
shaded cocoa plantations in the Atlantic forest region of Brazil, compare ant assemblages in
cocoa agroforests with forests and other forms of agriculture, and discuss how these shaded
plantations contribute to the conservation of the ants in the Atlantic Forest region. We also
discuss ants of economical importance and of special interest, including Camponotus,
Dolichoderus, Gnamptogenys, Pachycondyla, Pseudomyrmex and other litter dwelling
genera. We discuss the situation of the tramp ant Wasmannia auropunctata in the Bahian
cocoa-producing region where it is considered as native, and that of the two cryptobiotic
genera Thaumatomyrmex and Typhlomyrmex, as well as that of proven and possible
endangered army ant and Ponerini species. A total of 192 ant species from four strata were
found in extensive sampling of a cocoa plantation with a relatively simple shade canopy
(comprised primarily of Erythrina). Species richness in the cocoa plantations corresponded
roughly to that of low diversity native forests, and species composition of cocoa plantations
was most similar to native habitats (forest and mangroves) while ant composition in other
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agricultural habitats was most similar to that of urban areas. Although occurrences of
Wasmannia auropunctata were similar in cocoa plantations and forests, abundance of
Thaumatomyrmex and Typhlomyrmex, generally thought to be rare ants, was relatively high
in cocoa plantations. These results, from cocoa plantations with relatively simple shade,
demonstrate the importance of cocoa for ant conservation in the Atlantic forest region of
Brazil. It is likely that cocoa plantations with a greater number of vegetation strata and
higher tree species richness (such as traditional cabruca plantations) provide even more
important habitat for ants generally and for ant species of conservation concern.
Keywords Agroecosystem - Arboreal ants - Cabruca - Community structure - Erythrina
- Forest - Ground-dwelling ants - Neotropical fauna - Theobroma cacao
Introduction
The Brazilian Atlantic biome is a biodiversity hotspot (Morellato and Haddad 2000,
Galindo-Leal and Camara
2005), with a record endemism rate for plants estimated to be
about 40% for Angiosperms (Thomas et al.
1998; Oliveira-Filho and Fontes 2000), and a
high endemism for insects (Brown
1991), herbaceous plants (Jackson 1978), birds (Haffer
1974) and mammals (Mittermeier et al. 1982; Faria et al. 2006). Yet today, the Atlantic
forest retains only about 8% of pristine vegetation due to an intensive, historical
deforestation that began with the Portuguese colonization in the 16th Century (Dean
1995).
Due to its high diversity and its low forest cover, the region is considered one of the highest
priorities for biodiversity conservation within Brazil and is the site of many conservation
and restoration projects (Ministério do Meio Ambiente, dos Recursos Hídricos e da
Amazônia Legal
1995).
In addition to being an area of high biodiversity, the region is the largest cocoa-growing
area on the eastern coast of Brazil with around 400,000 hectares currently under cocoa
(Theobroma cacao L., Malvaceae). Cocoa is native to the Amazon region and was
introduced into southeastern Bahia in the 18th Century (Delabie
1990). During the cocoa
boom of the 1960’s and 1970’s, approximately 650,000 ha of forest were converted to cocoa
plantations thereby creating a greatly fragmented native forest ecosystem. In the 1980’s
cocoa production was one of the largest exports of Brazil. Yet, the future of the cocoa
economy and the conservation of native forest remnants are increasingly threatened by a
complex phytosanitary situation of the cocoa farms following the introduction of the
witches’ broom fungus (Crinipellis perniciosa) in 1989, and a continuous pressure for wood
extraction in the region, especially for the timber trade (Alger and Caldas
1994; Rocha
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2002).
There are two main cocoa production systems in Bahia which vary in vegetation structure
and management. The traditional cocoa groves, called “cabruca”, are established by planting
cocoa under a thinned forest canopy and are, therefore, shaded by native trees (Rolim and
Chiarello
2004). The vegetation structure and stratification of cabruca plantations are
considered to be similar to, albeit less complex than, that of natural forests (Saatchi et al.
2001), and plant richness is among the highest for agricultural systems (Rolim and Chiarello
2004). The cabruca cocoa agroecosystem has received much recent attention because of its
economic importance for the region, and also because cocoa cultivation in traditional,
shaded systems favors the conservation of a high proportion (but evidently not all) species
of the Atlantic Forest landscape (Delabie et al.
1999; Sperber et al. 2004; Faria and
Baumgarten
2007). In the past 50 years, a new system called “derruba total” (total felling)
where the original vegetation is completely eliminated before planting has been developed.
In “derruba total”, cocoa trees are planted at twice the density of cabruca systems, and
cocoa plants are generally shaded with introduced leguminous Erythrina trees or sometimes
with trees with economic value. There are very few cocoa plantations without shade in
Bahia. Other forms of land use including pasture, coffee and eucalyptus are developing on
the margins of the traditional cocoa production region and eucalyptus in particular has
already expanded 200 km north from where it was reported by Johns (
1999).
Ants are an extremely important component of tropical biodiversity in both natural and
agricultural systems. Ants comprise a large fraction of the animal biomass and are among
the major predators in tropical agroforestry systems. The ecology, diversity, and functional
role of ants as providers of natural biological control of a range of organisms, has been
extensively studied in coffee and cocoa farms (Way and Khoo
1992; Majer 1993; Philpott
and Armbrecht
2006). Implicit in much of this work is that tropical agroforests are
important for conservation of tropical ants. Using both original data and information
collected from the literature, a summary of work on ant diversity, ecology, and conservation
is provided here with a special emphasis on ants of the cocoa plantations of the Atlantic
region of Brazil. First, original work examining species richness and composition of
different components of the ant community in a cocoa plantation in Bahia is presented.
Next, using a separate set of original data from the area around Ilhéus, we compare the
species composition of ants in cocoa plantations and other common habitats in the Atlantic
region. A review of existing literature on ant community organization in cocoa plantations
follows, as does detailed information about the ecology and natural history of important ant
genera found in cocoa plantations (Wasmannia, Thaumatomyrmex and Typhlomyrmex). As
ants may damage crops, but also play extremely important functional roles as predators, we
include a review on the economic importance of ants in cocoa plantations. Finally, we
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discuss the importance of cocoa plantations for the conservation of ant diversity both
generally and for particular threatened genera in the Brazilian Atlantic Forest, at both
habitat and regional scales.
Methodology
Field data collection was conducted in several habitat types in the surroundings and in the
municipality of Ilhéus in Bahia. Ilhéus is situated at 15°S on the coast of the Atlantic Ocean
and the region is covered by secondary and pristine coastal Atlantic forest, “restinga” (the
typical vegetation of the sea shore related to the Atlantic forest), cultivated lands (mainly
shaded cocoa plantations and pastures), mangroves and urban areas. The average
temperature in Ilhéus is between 20°C and 28°C with annual precipitation between 1,300
and 2,000 mm, with decreasing values as the distance to the coast increases.
An extremely exhaustive sampling of the ant community in a cocoa plantation in Bahia was
carried out in 1992 to 1996. First, a 1 ha plot was delimited in a 20 year old cocoa grove
shaded by the introduced legume Erythrina fusca Loureiro (Fabaceae) and then ants were
collected in all strata with 27 different methods over three years (for a presentation of
methods and an analysis of the ground dwelling fauna, see Delabie et al.
2000b).
Hypogeous species were collected in cubes of soil, epigeous species with baits and pitfall
traps, leaf litter species by Winkler and Berlese extraction and by inspection of fallen twigs
and all other favorable microhabitats, and arboreal species by chemical knockdown and
beating of vegetation. The methods used did not always allow determining the actual
activity (nesting, foraging, accidental presence) of the ants collected but were useful for
calculating their frequency of occurrence in the respective strata.
In another study in the same region in the period 1997–2002, the species richness of ants
found in a cocoa plantation shaded by Erythrina fusca was compared with that of three
areas of native forest of low, medium and high ant diversity. These three areas were chosen
as representative of the ant richness in regional forest remnants, out of a set of 60 sampled
forest areas of the same region (Delabie et al., unpublished data). Each forest and cocoa
plantation was sampled with identical methodology and sampling effort. Each forest was
sampled with a series of mini-Winkler traps (50 independent samples of 1 m
2
in each area,
according to the methodology described in Delabie, 1999), aiming to show the typical
variation in ant diversity among forest areas of the Atlantic rain forest of Bahia.
To examine whether species composition varies with habitat type, species lists were created
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for various habitat types using museum collections, and richness and relative abundance of
ant species were compared using the Sorensen index (Southwood 1978). An inventory of all
ants at the collection of the Myrmecology Laboratory of the Brazilian Cocoa Research
Center (CEPEC/CEPLAC) in Ilhéus/Itabuna was made using the biological material
received mostly during the past 15 years (the collection is referred to as “CPDC” in
taxonomic literature). Analyses were limited to those ant species found within a 1,750 km
2
area around Ilhéus and belonging to the genera Camponotus Mayr (Formicinae,
Camponotini), Dolichoderus Lund (Dolichoderinae, Dolichoderini), Gnamptogenys Roger
(Ectatomminae, Ectatommini), Pachycondyla Smith (Ponerinae, Ponerini) and
Pseudomyrmex Lund (Pseudomyrmecinae, Pseudomyrmecini). From its collection history,
each specimen collected in Ilhéus and presently found in the CPDC collection, regardless of
species, was independently categorized into habitat classes (forest, “restinga”, cocoa,
pasture, mangrove, urban) according to the environment where it was found. These genera
were chosen because they are among the most species rich in the cocoa producing region
and because of their distinct characteristics. Most (but not all) species of Camponotus,
Dolichoderus and Pseudomyrmex are arboreal. Dolichoderus and Camponotus commonly
tend sap-sucking Hemiptera (Delabie
2001), and Pseudomyrmex do occasionally.
Gnamptogenys are ground-dwelling and some Pachycondyla (those formerly in the genus
Neoponera, for example) are arboreal while others of the same genus are epigaeic or even
live below ground. Nutritional ecology information about all these ants can be found in
Fowler et al. (
1991). Lists of species belonging to these genera at Ilhéus are available in
Delabie et al. (
1998; 2006), Fraga et al. (1999) and Majer and Delabie (1999). In order to
minimize the overestimation for one or the other habitat due to the disparity of the
collection efforts, the contribution of each species per habitat was recalculated on a
hypothetical basis of 100 occurrences for the whole habitat.
Comparisons were made of the relative abundances of two important ant genera in cocoa
plantations and surrounding habitats. Complete descriptions and justification for using each
genus are given below. First, a dataset on Wasmannia auropunctata was obtained from
standardized Winkler collections in native forest, shaded cocoa plantations, and pastures.
Ants were sampled in 11 plots per habitat where each plot was located in a different
landscape fragment. In each plot, 50 1-m
2
leaf litter samples were taken, each at 50 m
intervals. Samples were randomly distributed in 12.5 hectares of a single fragment (Delabie
1999). In each area, the number of W. auropunctata occurrences was recorded (i.e. one
observation means that one or more workers were found in a single Winkler sample).
Second, comparisons of the frequency of occurrence of Thaumatomyrmex sp.1 were made
in several land uses in the surroundings of Ilhéus. The data were obtained from standardized
mini-Winkler collections in 16 native forest areas, 16 shaded cocoa plantations, and 14
pastures. Samples and plots were distributed as for W. auropuncata studies, and
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comparisons of occurrence done in the same way.
Finally, a range of new observations on Typhlomyrmex diversity and ecology was made
between 1993 and 2006 in primary and secondary forests in various regions of Brazil and
French Guyana (S. Lacau, unpublished), as well as in shaded cocoa plantations in Bahia.
Results and discussion
Ant diversity in shaded cocoa plantations
A total of 192 species were collected in ant samples in the shaded cocoa plantation sampled
in Bahia (Table
1). A first analysis of the data allowed partitioning the ant species richness
between the strata (Fig.
1). Many species of ants were found foraging and even nesting in
several strata. Species richness reached no plateau at the end of the sampling program even
after combining all samples (n = 1458; Fig.
1). The total species richness of the ant
community of the 1 ha plot was estimated to be around 230 species (Fig.
1). The diversity of
hypogeous and epigeous-foraging ants was similar (rarefied species richness for 212
occurrences [Coleman method] = 54 ± 1 and 55 ± 3, Fisher’s alpha = 23.4 and 24.0,
Simpson index = 20.2 and 27.5, respectively) and was lower than the diversity of leaf litter
and arboreal-foraging species, which were close to each other (Coleman = 70 ± 4 and 71 ±
4, Fisher’s alpha = 39.3 and 35.9, Simpson index = 44.5 and 47.1, respectively; Fig.
1).
Fewer than half (86 out of 192) of the species collected were found only foraging in a single
stratum that corresponded generally to their nesting site: 5 out of 54 species collected in the
soil, 44 out of 126 species collected in the leaf litter, 12 out of 88 species collected at the
ground surface, and 25 out of 107 species found foraging on the cocoa tree (Table
1). Fifty
one species (26%) were collected from two strata and a lesser proportion in three (17%) or
four (11%) strata. Ants collected from all strata were mostly arboreal-nesting dolichoderines
(Azteca spp.), the Neotropical tramp Wasmannia auropunctata (Myrmicinae;
Blepharidattini), and some arboreal-nesting Crematogaster (Myrmicinae; Crematogastrini).
Table 1 Frequency of occurrence (0–100%, n = 54 quadrats) of ant species found in the
hypogeous, leaf-litter, epigeous and arboreal strata in one hectare of a 20 year old cocoa plantation
shaded by Erythrina fusca on the research station of the Brazilian Cocoa Research Center (CEPEC/
CEPLAC), Ilhéus/Itabuna, Bahia, Brazil. The data were collected in 1992–1996 using 27 sampling
methods as detailed in the text
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Hypogeous Litter Epigeous Arboreal
AMBLYOPONINAE
Prionopelta antillana 35 2
CERAPACHYINAE
Cerapachys splendens 4
DOLICHODERINAE
Azteca alfari 2 7
Azteca chartifex spiriti 2 6 6 6
Azteca longiceps 2
Azteca paraensis bondari 2 15 7
Azteca sp.A 4 4 11 17
Azteca sp. nr.fasciata 2
Dolichoderus attelaboides 6 37
Dolichoderus bidens 2
Dolichoderus decollatus 2 4
Dolichoderus diversus 7
Dolichoderus imitator 2
Dolichoderus lutosus 11
Dolichoderus schulzi 2
Linepithema sp.nr.humile 2 6 44 20
Tapinoma melanocephalum 54 17 11
Tapinoma sp.A 7
Tapinoma sp.B 2
ECITONINAE
Eciton burchelli 20
Eciton mexicanum 2
Labidus coecus 2
Labidus praedator 4 30 7
Neivamyrmex pilosus 2
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ECTATOMMINAE
Ectatomma brunneum 6 6
Ectatomma permagnum 2
Ectatomma tuberculatum 22 17
Gnamptogenys annulata 4
Gnamptogenys haenschi 2
Gnamptogenys moelleri 11 11 19
Gnamptogenys sp. nr.horni 2 2
Gnamptogenys sp. 6
Gnamptogenys striatula 4
Typhlomyrmex pusillus 39 4
Typhlomyrmex sp.A 2 2
Typhlomyrmex sp.B 2 2
FORMICINAE
Acropyga berwicki 2
Acropyga sp. nr.berwicki 22 11 2
Acropyga urichi 15 2 2
Brachymyrmex heeri 19 24 9 4
Brachymyrmex pictus 30 9 19
Brachymyrmex sp. 4 2
Camponotus crassus 2 13 17 2
Camponotus atriceps 6 2 19
Camponotus bidens 11
Camponotus blandus 4 24
Camponotus canescens 11 24
Camponotus chartifex 59
Camponotus cingulatus 35 9 30
Camponotus claviscapus 2
Camponotus novograndensis 2 7
Camponotus renggeri 2
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Camponotus sexguttatus 2 2 6
Camponotus sp.A 17
Camponotus sp.B 2
Camponotus trapezoideus 15
Camponotus vittatus 4
Paratrechina fulva 50 11 33
Paratrechina longicornis 20 22 6
Paratrechina sp.A 4 74 9 11
Paratrechina sp.B 6 19 13
Paratrechina sp.C 35 17 4
Paratrechina sp.D 7 31 20 9
MYRMICINAE
Acanthognathus ocellatus 20 2
Acromyrmex subterraneus
brunneus
19 41 9
Apterostigma sp.pilosum complex 4
Cardiocondyla obscurior 2 2
Carebara panamensis 4 22
Carebara urichi 2
Cephalotes angustus 7
Cephalotes atratus 17 33
Cephalotes frigidus 4
Cephalotes maculatus 7
Cephalotes minutus 4 2
Cephalotes pallens 2
Cephalotes simillimus 2
Crematogaster acuta 7
Crematogaster curvispinosa 46
Crematogaster erecta 4 28 19
Crematogaster evallans 6 6
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Crematogaster limata 6 26 13 35
Crematogaster sp. nr.curvispinosa 6
Crematogaster sp. nr.limata 2
Crematogaster victima 4 6 9 7
Cyphomyrmex peltatus 4
Cyphomyrmex rimosus 22 4
Cyphomyrmex transversus 4
Eurhopalothrix clypeata 2
Hylomyrma sagax 2
Lachnomyrmex plaumanni 4
Leptothorax tristani 2 6 4
Megalomyrmex silvestrii 2
Monomorium floricola 11 28 9 6
Mycocepurus smithi 2 22 24 2
Octostruma balzani 11
Octostruma jheringhi 4 11 4 2
Octostruma stenognatha 4
Pheidole cataractae 2
Pheidole cornutula 7 19 6
Pheidole fabricator 4 7 2
Pheidole fallax 4 4 4
Pheidole fimbriata 15 50 70 2
Pheidole megacephala 4 7 13 19
Pheidole mendicula 44
Pheidole midas 28 24 9
Pheidole sp. nr.tristis 15
Pheidole sp.1 15
Pheidole sp.3 2
Pheidole sp.4 2
Pheidole sp.A 2 2
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Pheidole sp.B 2
Pheidole sp.C 2 6
Pheidole sp.D 2 2
Pheidole sp.E 4 4
Pheidole sp.F 2 4 7 2
Pheidole sp.G 2 2 6
Pheidole sp.H 2
Pheidole sp.I 2 61 19 15
Pheidole sp.J 13 9
Pheidole sp.K 4 2
Pheidole sp.L 13 4
Pheidole sp.M 2
Pheidole sp.N 2 2
Pheidole tachigaliae 2 11 7 39
Pheidole transversostriata 2 41 31
Procryptocerus marginatus 2
Pyramica alberti 4 2
Pyramica denticulata 4
Pyramica eggersi 2 2
Pyramica rugithorax 4
Pyramica schulzi 2 6 2
Pyramica subedentata 2 15
Rogeria besucheti 2
Rogeria foreli 2
Rogeria micromma 2 9
Rogeria scobinata 4
Rogeria subarmata 6 2 11
Sericomyrmex bondari 7 33 56 6
Sericomyrmex sp. 2
Solenopsis (Diplorhoptrum) sp.A 24
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Solenopsis (Diplorhoptrum) sp.B 2
Solenopsis (Diplorhoptrum) sp.C 43 100 83 30
Solenopsis (Diplorhoptrum) sp.D 35 54 31
Solenopsis geminata 4 11
Solenopsis pollux 24 4 2
Solenopsis saevissima 4
Solenopsis sp.A 2 2
Solenopsis virulens 2
Stegomyrmex vizottoi 2
Strumigenys carinithorax 2
Strumigenys dolichognatha 19
Strumigenys elongata 2 52
Strumigenys louisianae 19 2
Strumigenys perparva 2
Strumigenys smithi 2
Trachymyrmex cornetzi 2
Trachymyrmex relictus 2
Wasmannia auropunctata 24 96 93 76
Wasmannia rochai 2 6 7
PONERINAE
Anochetus mayri 2 2
Anochetus simoni 2
Hypoponera foreli 4
Hypoponera sp.A 4
Hypoponera sp.B 39 2
Hypoponera trigona 4 63
Leptogenys arcuata 4 11 2
Leptogenys bohlsi 2
Leptogenys crudelis 2
Odontomachus haematodus 2 76 76 37
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Odontomachus meinerti 30 7
Pachycondyla apicalis 6 13 2
Pachycondyla arhuaca 2 7 2
Pachycondyla bucki 2
Pachycondyla carinulata 2 7
Pachycondyla constricta 20 9
Pachycondyla crenata 2 15
Pachycondyla harpax 31 56 7
Pachycondyla holmgreni 7
Pachycondyla sp. nr.venusta 2
Pachycondyla striata 2 2
Pachycondyla striatinodis 2 4
Pachycondyla unidentata 2 48
Pachycondyla villosa 2 11 7 46
Thaumatomyrmex sp.1 13
Thaumatomyrmex contumax 2 2
PSEUDOMYRMECINAE
Pseudomyrmex elongatus 2
Pseudomyrmex gracilis 2 4 22
Pseudomyrmex oculatus 4
Pseudomyrmex simplex 2 2
Pseudomyrmex sp.A gp. pallidus 2
Pseudomyrmex sp.Bgp. pallidus 4 4
Pseudomyrmex tenuis 6 11
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Fig. 1 Partitioning of ant species richness between the hypogeous, epigeous, leaf litter and arboreal
strata of a 1 ha sampling plot in a cocoa plantation shaded by Erythrina fusca near Ilhéus, Bahia,
Brazil (see Table
1). Accumulation curves were obtained by rarefaction (Coleman method). The total
species richness for all strata combined was estimated with Chao2 (Colwell
2000)
Applying a similarity coefficient to these data shows a dichotomy between the ground and
the arboreal-dwelling fauna (Fig. 2). The hierarchy of similarities confirms that some soil-
nesting species forage in the leaf litter and some litter ants forage in the soil (i.e.
Sericomyrmex spp.; Myrmicinae; Attini). An even greater number of arboreal-nesting
species were found foraging at the ground surface, explaining the similarity between the
arboreal and epigeous fauna (Fig.
2). The overall high faunal similarity estimated by the
Chao-Sorensen incidence-based index reflects the fact that the majority of species are found
in two or more strata.
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Fig. 2 Similarity between the hypogeous, epigeous, leaf litter and arboreal-foraging ant fauna of a
1 ha sampling plot in a cocoa plantation shaded by Erythrina fusca near Ilhéus, Bahia, Brazil (see
Table
1). Similarities were calculated with the Chao-Sorensen incidence-based similarity index
appropriate for incompletely inventoried assemblages
The ant species richness in the cocoa plantation shaded by only Erythrina fusca
corresponded to that of a native forest of low diversity (Fig. 3). It is reasonable to expect
that the ant diversity of a cocoa grove shaded by native trees (cabruca) in the same region
would be at least equal to that of native forest. However, it is clear that some ant species are
negatively affected by the opening of the forest vegetation to plant cocoa trees, while others,
which are more adapted to clearings or open habitats, benefit. This is highlighted below for
a few ant genera.
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Fig. 3 Comparison of the ant species richness (Coleman method) between a cocoa plantation
shaded by Erythrina fusca (black line) and native forests of Bahia, with low (Canavieiras—area 2
A60, dotted grey line), medium (Uruçuca—Serra Grande A15, continuous grey line) and high
diversity (Canavieiras—Oiticica A55, dashed grey line). Species were extracted from leaf litter with
mini-Winkler traps (50 1 m
2
quadrats collected in each forest plot and 54 quadrats in the cocoa
plantation)
Diversity and composition of selected ant genera in native
and human-managed habitats near Ilhéus, Bahia
Within the 10,000 km
2
surrounding Ilhéus, 442 ant species have been reported, most of
them known from native environments and shaded cocoa plantations (Delabie et al. 1999).
A similarity analysis among the several habitat types (including primary and secondary
forests, restinga, cocoa plantations, pastures, mangroves, and urban areas) showed that the
regional ant fauna is organized in two clusters: the first cluster consists of the native
environments and the shaded cocoa plantations, and the second cluster consists of
agricultural land uses other than cocoa groves and urban areas (Fig.
4). Most of the ants that
contribute to the first cluster (natural habitats and shaded cocoa plantations) are currently
assumed to be native to the Atlantic rain forest, while a large proportion of those of the
second cluster (the more intensively managed areas) are exotic (Delabie
1993) or possibly
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originate from other drier Neotropical biomes, such as cerrado, caatinga or pampa (Delabie,
unpublished data).
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Fig. 4 Similarity between ant assemblages of five genera occurring in various habitats in the region
of Ilhéus, Bahia, Brazil, CPDC collection data. A: Camponotus (n = 32 species); B: Dolichoderus
(n = 9); C: Gnamptogenys (n = 14); D: Pachycondyla (n = 27) and E: Pseudomyrmex (n = 22).
“Unweighted Pair Group Method with Arithmatic Mean” [UPGMA] algorithm.
Among the genera Dolichoderus, Gnamptogenys and Pachycondyla, species found in
shaded cocoa plantations were very similar to those found in native habitats (Fig. 4). By
contrast, Camponotus species in cocoa were more similar to those found in human-managed
habitats or in mangroves. Mangroves are an environment where the terrestrial fauna is
strongly dependent on the surrounding vegetation: if pristine, the ants colonizing the
mangrove trees will belong to the original native fauna; if degraded, most of these ants will
be typical of human-managed (or disturbed) habitats (Delabie et al.,
2006). As mangroves
are well inserted in the urban area of Ilhéus, it is not surprising that a large part of the
species of Camponotus and Dolichoderus are common with these strongly human-managed
habitats (Fig.
4).
Ant community organization in shaded cocoa plantations
Ant community organization in cocoa plantations has been the subject of many publications
because of the ecological dominance of ants in this agroecosystem and the relative ease with
which ants can be studied in cocoa plantations compared to native ecosystems. Many
researchers have examined characteristics of the ant fauna of cocoa plantations in several
producer countries including Brazil, Cameroon, Ghana, Papua New Guinea, and Trinidad.
Much of the research in cocoa plantations examines the community structure of arboreal-
nesting species, and a few recent studies have examined the completely different
organization of ground-nesting colonies (Belshaw and Bolton 1993; Delabie et al. 2000a;
Fisher et al.
2000). The study of the leaf litter ant communities has been greatly facilitated
over the last years due to the adaptation of the Winkler collector, initially developed for the
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collection of soil fungi and beetles, to a smaller version, the mini-Winkler (Fisher 1998).
Mini-Winkler use has become widespread as the traps are recognized as extremely efficient
in capturing ground and litter-dwelling ants (Bestelmeyer et al.
2000; Delabie et al. 2000b;
Parr and Chown
2001; Longino et al. 2002; Underwood and Fisher 2006).
Studies of the structure of arboreal ant communities in cacao plantations have formed the
basis for much work examining the community assembly of ants. Cocoa plantations of
Africa, Oceania, Mesoamerica and South America have provided perfect experimental
fields for myrmecologists. In particular, many experiments have been carried out in the
experimental plots of shaded cocoa plantations of the Brazilian Cocoa Research Center
(CEPEC/CEPLAC) in Ilhéus/Itabuna, Bahia, beginning in the 1970’s (Leston
1978; Winder
1978) and continuing to the present day. Only recently have these studies been extended to
other forms of agriculture and to natural environments. The general pattern discovered is
that a few competitively interacting ant species become numerically dominant in a given
site or habitat, therein generating a horizontal and/or vertical stratification or mosaic formed
by their non-overlapping territories (see the reviews of Majer
1993; Dejean et al. 2003; and
the criticisms by Sanders et al.
2007). Furthermore, each dominant species often tolerates a
series of non-dominant species, generating positive associations among dominants and non-
dominants. Such mosaic patterns have been found in cocoa plantations across a wide range
of producing countries. Yet, there are some doubts about whether mosaic patterns occur in
the rainforest canopy because of changes in ant composition (complex community
interactions), habitat complexity or resource availability, all of which may have strong
effects on insect interactions. The mechanisms of species co-occurrence and maintenance of
ant territories and mosaic patterns, which are much more discreet in the ground layers
(Fowler and Delabie
1995; Delabie et al. 2000a), appear to be particularly complex on
vegetation and may include competition, resource partitioning, or stochastic events (Majer
et al.
1994; Sanders et al. 2007). Probably much of the variation in mechanisms results from
the fact that each species may possess its own strategy for maintaining its status in the
mosaic (see discussion in Ribas and Schoereder
2002). For example Wasmannia
auropunctata Roger (Myrmicinae; Blepharidattini) can establish itself in extensive areas of
cocoa plantations, occupying continuous areas of leaf litter (its natural habitat) and
extending up to the tree canopy, where it acquires characteristics of a dominant arboreal ant
(Majer and Delabie
1993; Majer et al. 1994; Souza et al. 1998). Its ecological and
reproductive characteristics make Wasmannia, more than all other ant species that occur in
cocoa plantations, the most successful competitor able to quickly fill an empty niche in the
agroecosystem. Another interesting case is that of Azteca chartifex spiriti Forel
(Dolichoderinae; Dolichoderini), which is extremely territorial and exhibits original
defensive behaviors, inhibiting colonization by other ant species and competing for territory
and tree resources by means of allomones (Medeiros and Delabie
1991). In contrast to
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canopy species in cocoa plantations, leaf litter ant species, although apparently sometimes
positively and negatively associated, do not seem territorial (Delabie et al. 2000a).
The tramp Wasmannia auropunctata in Bahian shaded
cocoa plantations
The Neotropical Myrmicinae Wasmannia auropunctata Roger is common in Bahia, where it
can occur in any environment, including forests, urban areas, farms and beaches. This
competitive ant is invasive in many tropical and subtropical countries (Le Breton et al.
2004; Errard et al. 2005), especially on islands where it has a strong negative effect on
native fauna (Passera and Aron
2006). It can influence the mesofauna community structure
discreetly in habitats in which it is native (Majer and Delabie
1993; Souza et al. 1998) and
has stronger influences in areas where it has been introduced (Le Breton et al.
2003; Passera
and Aron
2006). In the cocoa producing region of Bahia, the nests of this ant are found in
rotten pieces of wood and other vegetation materials in the litter. In natural habitat, it is
seldom found on arboreal vegetation (i.e., bark cavities, hanging soil associated with
epiphytes) but in shaded cocoa plantations, the ant climbs on the cocoa trees where it forms
a mutualistic association with the mealybug Planococcus citri Risso (Hemiptera;
Auchenorrhyncha; Pseudococcidae; Delabie et al.
1994; Delabie 2001). The mealybug is
apparently not associated with the ant in natural habitats (if associated, it must be very
discreet) when the ant only lives in the litter, but the mealybug appears and its population
strongly increases with the growth of the W. auropunctata population (information about
the dynamics of the mealybug colonies on cocoa trees is given in Delabie et al.
1994). The
effect of W. auropunctata on mealybug populations is more obvious when the mosaic of
dominant ant species has been disturbed by abusive use of pesticides: W. auropunctata
colonies frequently divide such that ants recolonize niches left empty by other ants
regardless of the effect of pesticide on its own population (Delabie
1990).
A comparison between the number of occurrences of W. auropuncata in leaf litter in
pasture, cocoa fields and forest areas showed few statistical differences among habitats
(Fig.
5) [forest vs. cocoa plantation: t(20) = 0.07, p = 0.30; cocoa plantation vs. pasture: t
(20) = 1.41, p = 0.18; forest vs. pasture: t(20) = 0.16, p = 0.87]. Although a strong
difference between its occurrences in human-managed and in natural habitat was expected,
these results show that this ant is distributed all over the region more or less independently
of the land use. Nevertheless, W. auropunctata is less frequently encountered in natural
habitat, where it forms smaller populations normally limited to the litter layers (Delabie,
pers. obs.), than in disturbed habitat where it also inhabits plants and tends Hemiptera. This
situation corresponds to what should be expected in many wet forest areas of the
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Neotropical region although the ant impact is drastically stronger in remote non-native areas
(Jourdan 2003). The recently demonstrated peculiar reproductive system of this ant
(Fournier et al.
2005) suggests that genetic mechanisms underlie the differentiated behavior
and ecological aggressiveness in native and non-native areas of distribution.
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Fig. 5 Occurrence of Wasmannia auropunctata (n = 11 plots per habitat) and Thaumatomyrmex
sp.1 (n = 14–16 plots per habitat) in a series of 50 1 m
2
quadrats of leaf litter collected with a
Winkler apparatus in the three ecosystems (native forest, shaded cocoa plantation, and pasture)
The cryptic ant genus Thaumatomyrmex at Bahia: forest
vs. shaded cocoa plantation and pasture
The ants of the genus Thaumatomyrmex Mayr (Ponerinae, Thaumatomyrmecini) have a
noteworthy cephalic morphology in the family Formicidae. They have long mandibles
forming fine sickles with three or four pin-shaped teeth (Kempf 1975). This architecture of
their mouthparts represents a unique adaptation in the animal world for their specialized
feeding habit: Thaumatomyrmex is among the rare arthropods known to predate Penicillata
(Myriapoda; Diplopoda; Brandão et al.
1991) and able to circumvent their mechanic
defenses. The genus Thaumatomyrmex includes eleven species (Baroni Urbani and De
Andrade
2003; Jahyny et al. unpublished) or more, not taking into account Longino’s
(
1988) revision of the ferox group. At least four of them occur in Brazil. These ants have
been seldom collected because of their cryptic (sensu Andersen
1991) habits and their very
small colonies; for that reason, their biology is little known. For most species, only the
worker form has been described and no information is published for the gynes. Several
hypotheses tentatively explain the small colony size and the reproduction system of these
ants—they are assumed to be produced exclusively by fertilized egg-laying workers called
“gamergates” (sensu Peeters and Crewe
1984). Except the cited taxonomic and specialized
preying habit studies, only one study has been published on the genus’ ecology, analyzing
its frequency in shaded cocoa plantations and forest remnants of the southeastern Atlantic
Forest of Bahia (Delabie et al.
2000c). The recent practice of studying the leaf litter ant
communities with the Winkler extractor showed that the apparent rarity of these ants was in
fact a sampling artifact at least for one species.
Three Thaumatomyrmex species are currently known in Bahia. Thaumatomyrmex sp.1
(formerly named Thaumatomyrmex atrox Weber in Brandão et al. (1991) and Delabie et al.
(
2000c)) is by far the most frequent species of the genus in the various ecosystems and
agroecosystems of Bahia, while the larger Thaumatomyrmex contumax Kempf and
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Thaumatomyrmex mutilatus Mayr are seldom collected. These ants are generally found in
the litter layer where their prey is abundant. At the local scale, two sympatric species occur:
a small one (Thaumatomyrmex sp.1) and a second, much larger one. For example, in shaded
cocoa plantations and Atlantic Forest remnants from Itabuna to Itororó, Thaumatomyrmex
sp.1 and T. contumax are always found together (Brandão et al. 1991; Delabie et al. 2000c).
Near the coast at Ilhéus or in the west transitional region (Itambé region), T. mutilatus
coexists with Thaumatomyrmex sp.1 (Jahyny et al., unpublished).
Thaumatomyrmex sp.1 occurred significantly less in pasture compared to forest and shaded
cocoa plantations where its occurrence was statistically similar (Fig. 5) [forest vs. cocoa
plantation: t(30) = 0.13, p = 0.90; cocoa plantation vs. pasture: t(28) = 1.58, p = 0.12; forest
vs. pasture: t(28) = 3.20, p < 0.05]. These results show that shaded cocoa plantations may
represent a favorable environment even for highly specialized species since they can
certainly find their prey in abundance in the plantations. The frequent occurrence of
Thaumatomyrmex sp.1 can be considered as evidence of the efficiency of native or managed
ecological corridors, at least at the soil mesofauna scale.
The rare Typhlomyrmex ants in Bahian shaded cocoa
plantations
Typhlomyrmex Mayr, 1862 (Ectatomminae, Typhlomyrmecini) is a small genus of
Neotropical ants, currently under revision (S. Lacau, unpublished). It is seldom represented
in museum collections. The genus includes seven species for which the workers have a
robust but elongated morphology, with a pale yellow to brown reddish color and an overall
length from 1.5 to 5 mm (Lacau et al. 2004; unpublished). A few species have a wide
distribution all over the Neotropics, while others are endemic to very small geographical
areas. The biology of the genus remains very poorly known; however, the few available data
show a great heterogeneity in the ecology of the species (Lacau et al.
2004). All species are
cryptic. Some are general predators, while others practice specialized predation on several
arthropods.
Observations of Typhlomyrmex diversity and ecology in primary and secondary forests
revealed that the taxonomic knowledge of this small genus is not representative at all of its
diversity. Furthermore, although these ants were previously considered rare, it is now
believed they are in fact common in some microhabitats (rotten wood, tree rhizosphere) of
the cocoa plantations (Lacau et al., unpublished). For example, just in the cocoa fields of the
Cocoa Research Center at Ilhéus, Bahia, four species of Typhlomyrmex can be found, two of
them undescribed.
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The less rare species, Typhlomyrmex rogenhoferi Mayr, presents a singular autoecology: in
forest, as well as in the shaded cocoa plantations, this epigaeic species nests exclusively in
the rotten trunks of fallen trees or in large branches on the ground (Lacau et al. 2001; 2004).
Adult colonies include two to three thousand individuals and most colonies are established
inside the hardest parts of the trunk. Typhlomyrmex rogenhoferi can be relatively abundant
in pristine or secondary forest areas of Bahia and other regions but is much rarer in shaded
cocoa plantations. A logical explanation is that there is a low availability of fallen rotten
trunks compared with the forests. The vegetation is obviously much denser and diversified
in forest than in shaded cocoa plantations and only the dynamics of natural regeneration of
forest allow the maintenance of this kind of micro-habitat. It was also observed that this ant
is more abundant in cabruca groves than in plantations where the original vegetation was
completely eliminated before planting. Cabruca ensures a constant renewal of the fallen
wood according to the aging of the shade trees, whereas where vegetation is constantly
removed, there is no dead wood on the ground leading to a lack of nesting opportunities for
this ant. A major concern about this component of ant diversity in the traditional cabruca
plantations is that forest trees are increasingly being substituted by pioneer vegetation or
early secondary species (Rolim and Chiarello
2004) that possibly will not provide habitat
for this ant genus over the long term.
Another characteristic of T. rogenhoferi is that it is associated with larvae of several species
of lampyrid beetles. These live inside ant nests, directly in contact with the ant larvae,
constituting the framework of a narrow biotic association that is still not well understood
(Lacau et al. 2001; Lacau, 2005). Lampyrid diversity is larger in forest than in the cocoa
fields (Lacau, unpublished), but their overall abundance has a similar range in forest and
cocoa fields.
It is noteworthy that the endemic Typhlomyrmex meire Lacau, Villemant and Delabie was
recently described from the cocoa region of Ilhéus. This hypogeous species is locally found
in the cocoa plantations, being even relatively frequent in cabruca, but was collected only
once in a forest fragment. This interesting species always nests a few centimetres away from
colonies of Acropyga berwicki, another dominant soil dwelling ant in the cocoa plantation,
on which it is a specialized predator (Lacau et al. 2003). Considering the high density of A.
berwicki nests in cocoa plantations (Delabie et al.
1991), this is one possible explanation for
the high frequency of T. meire. Cocoa plantations therefore provide valuable habitat to
maintain the diversity of certain hypogeous ants and their trophic interactions.
Economic importance of ants in Bahian shaded cocoa
plantations
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Several ant species are economically important in the shaded cocoa plantations of Bahia
either because they act as biological control agents of cocoa pests or because they damage
the cocoa crop (Delabie 1990). Of those groups considered pests to cocoa are the leaf-cutter
ants and the fungus garden ants, each problematic for distinct reasons. Several species of
leaf-cutting ants (Myrmicinae; Attini) such as Atta cephalotes Latreille, Atta sexdens
Linnaeus and Atta laevigata Smith (Delabie et al.
1997), as well as Acromyrmex balzani
Emery, Acromyrmex rugosus Smith and Acromyrmex brunneus subterraneus Forel (Delabie
1990) occur in cocoa plantations. All of these ant species are considered pests because they
cut cocoa leaves, bark and small pods, especially on young plants (Delabie
1990; Delabie
et al.
1993). Nevertheless, their impact on Bahian cocoa plantations is minimal, and in a
certain manner, even beneficial, since these ants certainly contribute to the nutrient
recycling in the cocoa farms, as well as in forests (Moutinho et al.
2003). They reportedly
also attack shade trees in cocoa plantations but such damage is normally limited to a small
number of plants. It can be inferred that, because leaf-cutters have a low diversity of plants
from which to choose in cocoa plantations, they frequently do predate more on cocoa tree
resources.
Azteca paraensis bondari Borgmeier (Dolichoderinae; Dolichoderini) is common both in
cocoa groves and in natural forests of Bahia. This arboreal ant creates polydomous
(multiple-nest) colonies that form “ant-gardens” with the epiphytic Gesneriaceae
Codonanthe uleana Fritsch. In this mutualistic association—the only one of this kind
recorded in the region—the ants disperse the epiphyte seeds to appropriate nest sites such
that the epiphytes grow and flourish, thereby creating the ant nest structure through the
development of their roots. This ant has long been considered the main pest of cocoa
plantations in Bahia, due to strong physical damage inflicted to the trees by the ants as they
rasp the plant buds in the upper levels of the trees to extract a gum used as a nest cement
(Delabie
1990). This ant was extremely common in the cocoa region until the middle of the
20th century when intensive eradication campaigns were carried out regionally through
mechanical elimination and insecticide application (Silva
1955; Delabie 1990). However,
the species is becoming more common in the region as a result of the recent crisis of the
regional economy, which caused many farmers to abandon their active control of this
species.
Ants of the genus Acropyga (Formicinae; Plagiolepidini) live strictly belowground. They
complete almost their entire life cycle inside their nests which consist of a series of galleries
constructed along the superficial roots of several species of cultivated or native trees of the
region (Delabie et al. 1991). The most commonly encountered species in Bahia is Acropyga
berwicki Wheeler. Acropyga spp. tend minute mealybugs of the genus Neochavesia
(Hemiptera; Auchenorrhyncha; Pseudococcidae) in their nest galleries in a mutualistic
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association (Delabie 2001; Johnson et al. 2001). During the nuptial flights, mated ant
queens in search of new nest sites carry newly mated mealybug females that start the
underground hemipteran colonies (Johnson et al.
2001). This kind of behavior exists
convergently between a few other ant species and mealybugs (Delabie
2001). Acropyga
berwicki is very abundant in shaded cocoa plantations and research on its biology was
motivated by still unconfirmed reports from the first half of the 20th century that another
species of Acropyga spreads coffee disease elsewhere in Brazil (Delabie
1990).
Azteca, Acropyga and many arboreous species in the genera Camponotus, Dolichoderus,
Wasmannia and others (Delabie
2001) tend several species of Hemiptera (Auchenorrhyncha
and Sternorrhyncha) on the cocoa pods or peduncles and young leaves. In some cases, this
behavior can cause strong economic damage, although in Brazilian cocoa plantations this
damage usually affects relatively small areas. This is not the case in cocoa producing
countries on other continents, where the tending by ants of capsids (Miridae) or the
Hemiptera that transmit the Swollen-Shoot-Virus cause producers enormous losses.
Nevertheless, associations between ants and Hemiptera do not always have negative
economic impacts. They may even benefit the host trees if the presence of the Hemiptera
increases the ant activity and permanence on the trees, and if the ants act as predators
against other phytophages (Delabie
2001; Philpott and Armbrecht 2006).
In fact, two ant species have a high potential for the biological control of cocoa pests in
Bahia, thereby exerting a positive influence on cocoa production. Azteca chartifex spiriti
Forel (Dolichoderinae; Dolichoderini) and Ectatomma tuberculatum Olivier
(Ectatomminae; Ectatommini) can protect the cocoa plants from thrips Selenothrips
rubrocinctus (Giard) (Thysanoptera; Thripidae) and mirids (Hemiptera) [A. chartifex
spiriti], while the principal prey of E. tuberculatum are chrysomelid beetles, leaf-cutter ants,
and caterpillars (Delabie
1990; Majer and Delabie 1993). It is to be noted, however, that the
former species also facilitates the dissemination of the economically important black pod
disease (Phytophthora spp.; Fungi, Oomycota, Pythiaceae; Medeiros et al.
1999; Delabie,
unpublished), so the presence of this ant may involve some sort of trade-off from a
production standpoint. Farmers in Bahia have promoted this species of Azteca in their
plantations for its biological control activity since the beginning of the 20th century, in lieu
of the mechanical and chemical control recommendations made by regional extension
services over half a century, which have now been abandoned (Delabie
1990; Medeiros
et al.
1999).
The positive influences of these and other ant species greatly benefit cocoa production. It is
a fact that the Brazilian cocoa plantations are generally only little affected by insect pests.
Contrary to the severe effects of diseases on the cocoa trees (mainly the witches’ broom
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Crinipellis perniciosa), insect pest problems are at most local and limited. There are no
recent reports of severely damaging pests of the cocoa tree or any special entomological
problems in Bahia, and pesticide use continues to be limited. As an example, during the
most recent economic crisis of cocoa production in Bahia, producers almost completely
abandoned insecticide use but continued using fungicides (Ruf et al. 1994). The scarcity of
insect pests is probably in part due to the predatory function exercised by many ant species
on other organisms that are potentially damaging to cocoa production. Among the main
groups of physical ecosystem engineers (Gutiérrez and Jones
2006), ants are certainly not
the most diverse animal group in the tropical landscape, but they are the most constant and
individually abundant and have the greatest impact on the habitat structure and the other
organisms that live there. The ant abundance and diversity in shaded cocoa plantations of
Bahia helps maintain the quality of the final product, usually without pesticide use, and is
for the producer testimony to the equilibrium and health of this type of agriculture.
Ant conservation problems in a landscape composed of a
mosaic of native habitats, cocoa plantations and
agriculture
As shown, the shaded cocoa plantations, and especially the cabruca, contribute to
maintaining a high diversity of ants in the cocoa-producing region of Bahia. This is
especially important for the conservation of numerous species that need large territories to
survive. A classic case are the army-ants of the genus Eciton (Ecitoninae) which need very
large areas to forage, since they are very active predators, have nomadic habits and form
very large populations with strong necessity for a constant supply of small prey items
(mostly invertebrates) (Hölldobler and Wilson 1990). The fragmentation of the native
forest, even as a rural landscape that forms a mosaic of cocoa plantations, forest remnants,
pastures and other crops, is not particularly favorable to the maintenance of long-term viable
populations of this type of ants (Freitas et al.
2006), chiefly for two reasons. First,
agricultural areas do not support the large biomass of epigaeic invertebrates in the upper
layers of the soil that could feed these ant colonies all year long, and second, fragmentation
generates barriers (open places) that these ants cannot pass. In Panamanian coffee
plantations, Roberts et al. (
2000a, b) found that army ants only occur in shaded coffee
plantations and forests, but not in sun coffee. At Bahia, cabrucas and the other types of
cocoa plantations are certainly the only form of agriculture that can be used by these ants as
ecological corridors, but only if they are adjacent to forested areas, or if individual blocks of
plantations are large enough to harbor populations of these ants, consisting of several
colonies. Of the three species of Eciton [E. burchellii (Westwood),E. mexicanum Roger and
E. vagans (Olivier)] living in the cocoa producing region of Bahia, some may become
endangered over the long term. Although these ants are not as common in Bahia as they are
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in the Amazon Basin where the forest is still largely continuous, they are still regularly
observed. It is not known if other army-ants of the more diverse genus Neivamyrmex also
occur frequently in the cocoa producing region, although there is no species in that genus
with populations as large as those of Eciton. With eleven reported species, the Ilhéus region
is exceptionally rich in Neivamyrmex (Delabie et al. 1998, Nascimento, in prep.).
Unfortunately, no data about Neivamyrmex biology are available as most of these ants have
a cryptic nomadic life in soil galleries. Regardless, there is little doubt about the importance
of army-ants on the regulation of populations of most of the soil surface invertebrates
(Franks
1989) and their interactions with other animals, such as birds (Willis and Oniki
1978; Roberts et al. 2000b).
Other ants living in shaded cocoa plantations offer also specific conservation problems. The
Ponerinae Simopelta minima Brandão, described from two series of samples collected in
1986–1987 on one experimental field of CEPEC/CEPLAC in Ilhéus, was recently inserted
in the Brazilian official list of (presumably) extinct species, since its habitat, an old cabruca
with no phytosanitary application for decades (located in a zone of regularly managed cocoa
plantations), was irreversibly logged. The endangered giant ant Dinoponera lucida Emery
(Ponerinae), also reported on the Brazilian red list, has been found on rare occasions in
cabrucas in Bahia in the northern part of its natural geographic range (Campiolo et al., in
prep.). However, these occurrences seem to depend on connectivity of the sampled cocoa
plantations with areas of native habitat. This ant species, like the whole genus, has no gynes
and the reproductive function is assumed exclusively by mated workers or
“gamergates” (Peeters and Crew
1984). Gene flow depends thus only on males, which are
the only winged individuals in the nest and apparently unable to fly in open habitats. New
colony foundations occurs exclusively through fission of the mother colony in their
immediate neighborhood. The fragmentation of the forest appears then unfavorable to the
maintenance of viable populations of D. lucida for similar reasons to those discussed for the
species of Eciton. Perhaps by leaving more cabruca habitat, these forest fragments could
provide a suitable habitat at least for male dispersal.
Contributions of shaded cocoa plantations in the
maintenance of regional diversity
The disruption of original connectivity in any landscape due to fragmentation has numerous
implications for biological diversity, although it is obvious that each species has a particular
response to habitat fragmentation (Wiens 1996). One implication is that gene flow can be
limited due to the difficulty or inability of individuals to recolonize areas of other
populations. Fragmentation thus contributes to the erosion of the genetic diversity of
populations by increasing inbreeding, promoting local extinctions and possibly
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compromising the long-term viability of some species (Coyne et al. 2004). For most ants,
shaded cocoa plantations appear adequate for species maintenance. The forest-like structure
of this agroecosystem (even if extremely simplified as in plantations shaded by the exotic
Erythrina fusca) offers a range of niches for most species, for several reasons. First, in the
case of cabruca plantations, there is traditionally only limited use of fire to clear the
understory of the native forest, so most of the original soil fauna where most of the ant
diversity is represented (cryptic species living underground and soil-dwelling species) is
preserved. This was the case when the use of native forest to install cabrucas was permitted.
Today the Atlantic forest biome is protected by law. Second, the diversity of trees
maintained in the plantation favors the diversity of Hemiptera (Auchenorrhyncha and
Sternorrhyncha) as well as many other phytophageous insects, thereby guaranteeing the
food supply for arboreous ants which mutualistically depend on the honeydew produced by
many of these organisms (Delabie
2001). Third, the forest or introduced trees used to shade
the plantations retain diverse and abundant populations of epiphytes, (often with their own
dependent fauna) that form hanging soil layers where many arboreal and soil ant species
live. Fourth, contrary to most other crops, not all of the vegetation strata of a cocoa
plantation are simultaneously affected by pesticide application so that at least some of the
insect diversity will survive even under pesticide abuse. For all these reasons, the
fragmentation of the Atlantic forest of Bahia, if inserted in a matrix of cabrucas or other
cocoa plantations with a forest-like structure, appears to have a relatively small effect on the
native ant diversity. The high heterogeneity of the ant communities found in cabruca areas,
not detailed here, is poorly understood and requires further research. The contribution of
shaded cocoa plantations to the conservation of ant communities depends on the landscape
characteristics (such as size of forest remnants and agroforestry plots and landscape
connectivity) as well as on the range of climatic, pedological or other ecological factors that
make the Bahian cocoa producing region unique.
Conclusions
The patterns of ant diversity in cocoa landscapes may reflect to a certain degree the patterns
of many other organisms (Freitas et al. 2006), including organisms that are not directly
dependent on ants but are in some way affected by the surrounding ant activities. Many
organisms (such as birds, spiders, mites, most of the soil invertebrates, parasitoids and other
wasps, most of the phytophagous insects and plants) are in one way or another strongly
dependent on ants for their feeding or protection, for their own population regulation, and
even in rare cases, for pollination (Fowler et al.
1991). Shaded cocoa systems, especially
cabruca systems, protect a large number of ant species from several different components of
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the ant community. The species found therein are generally of more similar composition to
forest assemblages than are ants in other agricultural systems. Further, many ant species in
cocoa systems may have beneficial effects on the cocoa crop. Cocoa plantations in the
Atlantic region of Brazil have been extremely important for the study of several interesting
and rare genera, and for examining ant community assemblages. Finally, because of their
forest-like structure and because they are the most complex cropping systems in Bahia,
cocoa plantations make an ideal natural laboratory for studying the effects of human
influence on rainforest ecosystems.
Acknowledgments The authors acknowledge the help of the following persons at one step
or another to the experiments that were used in the preparation of this paper: Ana Lúcia
Biggi, Antônia Marli Vieira da Encarnação, Antônio Batista Casimiro, Gilmar Batista
Costa, José Crispim Soares do Carmo, José Eduardo Silveira, José Raimundo Maia dos
Santos, Lucimeire de Souza Ramos and Michela Fürst. The authors particularly
acknowledge Goetz Schroth who kindly assumed a large part of the edital work on this
paper. This study benefited by several grants of CNPq, FAPESB, Fundação O Boticário De
Proteção À Natureza and the PRONEX-CNPQ/FAPESB program.
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