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Conservative Benefits in an Ant-Hemipteran Association in the
Brazilian Tropical Savanna
by
K. Del-Claro , J. Byk , G.M. Yugue1, & M.G. Morato1
1
2
ABSTRACT
Terrestrial communities based on living plants involve at least three interacting trophic levels: plants, herbivores, and natural enemies of herbivores. Recent
studies have showed that the outcomes of these relationships are essential for
understanding not only insect-plant interactions but also whole communities.
Here, we present results of manipulative experiments (ant-exclusion) in the
field following an ant-plant-hemipteran interaction for eight years in the same
Cerrado vegetation area. We showed that the interaction results in benefits
to the hemipterans in terms of high survivorship and reproduction and to
the host plant in leaf herbivory reduction. The benefits are dependent of ant
presence and endure through time. The studied interaction shows that this
ant-hemipteran interaction is conservative in terms of maintenance of the
related species and outcomes in the same geographical area.
Keywords: ant, hemipteran, plant, interaction.
INTRODUCTION
Most species are collections of genetically differentiated populations, making
each population a small evolutionary experiment and each local interspecific
interaction a potential coevolutionary experiment (Wade & Goodnight 1998,
Thompson 2005). Additionally, interactions are held together over the long
term partly because most species are phylogenetically conservative in their
interaction with other species, and they probably interact with only a small
group of species that have the potential to affect the fitness of the individuals
(Thompson 2005). Ant-hemipteran relationship can represent an excellent
opportunity to search for data corroborating or not to this discussion. Studies have demonstrated that hemipterans (mainly aphids and membracids)
Universidade Federal de Uberlândia, Instituto de Biologia, L.E.C.I., CEP: 38400-902 Uberlândia,
MG, Brazil. [email protected]
2
Universidade Federal de Juiz de Fora, ICB, Departamento de Zoologia, CEP: 36036010, Juiz de
Fora, MG, Brazil.
1
Sociobiology Vol. 47, No. 2, 2006
are able to attract ants through the droplets of honeydew that they flick on
the ground and leaves (Del-Claro & Oliveira 1996), and that ants feeding
on this sugary secretion offer protection to the hemipterans against natural
enemies (Way 1963, Buckley 1987, Del-Claro & Oliveira 2000). Recently,
new studies showed that the outcomes of ant-membracid relationships can be
positive also to the host plant, through reduction of leaf herbivory (Messina
1981, Moreira & Del-Claro 2005) and increase in fruit production (Oliveira
& Del-Claro 2005).
The membracid Enchenopa brasiliensis Strümpel is a common species
feeding on apical meristems and inflorescences of Solanum lycocarpum
(Solanaceae) in the Brazilian tropical savanna. Moreira & Del-Claro (2005)
between 1996 and 1997 performed a series of manipulative experiments in
the Cerrado (the Brazilian tropical savanna) showing that tending ants can
significantly increase survivorship and reproduction of E. brasiliensis and
reduction on the level of herbivory on host plant. Multitrophic interactions
as between ants and hemipterans can present conditional outcomes (see
Bronstein 1998a,b; Del-Claro 2004), that can vary between populations
producing distinct selective patterns of coevolution in different localities (the
“Geographic Mosaic Theory”, Thompson 1999), and perhaps time. Thus so,
the aim of our study was to investigate the outcomes of an ant-hemipteran
relationship through time in the same study site, performing the first step in
an investigation making comparisons between localities. We mainly answered
the questions: Does the interaction between ants and E. braziliensis show
similar results throughout time in the same place? Are the same ant species
present in the relationships a decade later?
MATERIAL AND METHODS
We reproduced after eight years the experiments performed between 1996
and 1997 by Moreira & Del-Claro (2005, see also Moreira 1999) with the
association between ants, E. brasiliensis and shrubs of S. lycocarpum. The
study site was the same area of open cerrado (a tropical savanna like vegetation
with 75% of the grasses covering the landscape, with few trees and shrubs, see
Oliveira & Marquis 2002), in the Gloria’s farm (an experimental farm belonging to the Federal University of Uberlândia), used by Moreira & Del-Claro
(2005). In October of 2004, we tagged 22 individuals of S. lycocarpum with
Del-Claro, K. et al. — Benefits in an Ant-Hemipteran Association
similar phonological state (1-2m high, presenting inflorescences, young and
mature leaves), all of them infested by E. brasiliensis being tended by ants. In
each plant we tagged the two more similar branches, having approximately
the same number of membracids (eggs, nymphs and adults) and by the flip of
a coin each stem was designated as control or treatment. The control branches
were maintained in natural state. The treatment ones had all ants manually
removed and after that they received in their junction with the main trunk
the application of a stick resin (Tanglefoot®) that is known to act as a physical
barrier avoiding ant access to the membracids.
The number of membracids (egg masses, nymphs and adults) was recorded
to both groups of stems in the first (October) and last day of the experiment
(December). Leaf herbivory was evaluated also in the first and last day of
the study following Dirzo & Dominguez (1995). Voucher specimens of ants
and membracids were collected in the field in non experimental plants and
deposited in the Museu de Biodiversidade do Cerrado (MBC). We applied
Mann-Whitney U-Test to verify differences between the median values
obtained.
RESULTS
Eleven ant species were observed tending E. brasiliensis in the study area.
The ant genera Camponotus (4 species) was the most common followed by
Cephalotes (3 species), Crematogaster (1 species), Pheidole (1 species), Pseudomyrmex (1 species) and Ectatomma (1 species). Individuals of different ant
species were seen taking care of membracids in the same host plant, impeding
us to define an ant species as the main attendant of an aggregation. The most
common ant in number of individuals were Camponotus crassus, Camponotus
sericeiventris and an undetermined species of Pheidole. Generally, the most
common ant in a particular plant had nest near (30 cm distant) the host plant
and several times in the roots of the plant.
Membracids in stems with free ant access presented significantly higher
survivorship (Fig. 1A, B) and reproduction (Fig. 1D) than that in stems where
we performed ant exclusion. So ants protect membracids and their egg masses
against the attack of natural enemies. Additionally, stems visited by ants presented a significant reduction in leaf herbivory through time (Fig.1C).
Sociobiology Vol. 47, No. 2, 2006
Fig. 1. Comparison between the average number (X ± 1 SD) of total of individuals of Enchenopa
brasiliensis (A), only nymphs (B) and new egg masses (D) in stems of shrubs of Solanum lycocarpum
between October and December of 2004 in a Cerrado field. The percentage of leave herbivory between
groups with (white bars) and without ant attendance (black bars) in the same shrubs is also presented
(C). The symbols indicate: *(p < 0.05); ***( p < 0.001) – Mann-Whitney U-Test.
DISCUSSION
Comparing our results with those from Moreira & Del-Claro (2005, see
also Moreira 1999) we observed the occurrence of few variations in the final
results of the interactions between ants - E. brasiliensis and S. lycocarpum
through time in the same locality. After almost a decade, with an increase in
the human disturbance in the field site and at Cerrado in general (see Oliveira
and Marquis 2002 for a review) the same ant species continued attending the
hemipterans in the same host plant offering similar quality of benefits.
In fact, the E. brasiliensis- ants -S. lycocarpum system is apparently conditioned by a number of factors (e.g., time, habitat type, identity, abundance,
and behavior of species partners, severity of herbivore damage) that may
influence its final outcomes (Bronstein 1994; Del-Claro 2004; Moreira &
Del-Claro, K. et al. — Benefits in an Ant-Hemipteran Association
Del-Claro 2005). Small variations in biotic or abiotic factors can completely
change the direction of a mutualistic relationship, from positive to negative
and vice-versa (e.g. Oliveira & Del-Claro 2005). However, the conservative
relationship between E. brasiliensis with the guild of tending-ant species in
the study site is apparently the strong selective force maintaining the benefits
of the interaction to the three main trophic levels related. As Thompson
(2005) suggested at the local level, there is strong evidence that there are
coevolutionary dynamics managing the interacting species in a way that the
changes occurring through time are absorbed more quickly than we figured
out, keeping populations viable.
In ant-hemipteran relationships, the ants receive an energy-rich and predictable liquid resource (e.g. Tobin 1994, Davidson et al. 2003), and in turn
increase treehopper survival and reduce herbivore damage to the host plant.
The present study provides additional evidence that the relationship between
ants, honeydew-producing hemipterans and their host plants can result in
positive effects for all participants in the interaction (Messina 1981, Oliveira
& Del-Claro 2005). Additionally, our results support the hypothesis that
benefits can persist throughout years in the same locality. Almost all widespread species that have been studied in detail for their adaptation to other
species show geographic differences in ecological outcomes or traits linked to
interactions (e.g. Travis 1996; Brodie et al. 2002; Benkman 2003). The main
question that still remains is if in the tropical savanna the same mutualistic
interaction, common in several areas with distinct Cerrado physiognomies,
also presents similar outcomes in distinct regions.-
Acknowledgments
K. Del-Claro thanks CNPq for a research grant. G.M. Yugue and M.
Morato also thank CNPq for a Scientific Initiation fellowship. J. Byk thanks
CAPES for a Masters course fellowship. We thank A.P. Korndörfer for
English review.
Please spell out acronyms
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