Behavioral Ecology Vol. 11 No. 4: 396-404
© 2000 International Society for Behavioral Ecology
High surface temperatures select for individual foraging in ants
Departamento de Biología Animal y Ecología, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain
Address correspondence to F. Ruano. E-mail : hormiga @ goliat.ugr.es.
Received 8 March 1999; revised 25 October 1999; accepted 31 October 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Natural selection favors signals, receptors, and signaling behavior that maximize the received signal relative to background noise and that minimize signal degradation. The physical properties of the environment affect rates of attenuation and degradation of the signal, and thus temperature may influence the evolution and maintenance of volatile chemical signals. We tested this hypothesis in ants, where nest mate recruitment to a food source by laying trail pheromones on a surface is a common phenomenon. We collected data on maximal soil surface temperatures during the ants' activity and mode of foraging (recruitment or solitary). By using two different comparative methodologies, we demonstrated a relationship between maximal soil temperature at which species are active and recruitment behavior (which is hypothesized to be related to the presence or absence of chemical signals). The species that were active at lower temperatures proved to be those that used chemical signals to recruit nest mates during foraging. This is also the case when comparing sympatric species and thereby controlling for other environmental factors. Moreover, all seven nonrecruiter species developed from recruiter ancestries, which is consistent with our hypothesis because ample evidence suggests a forest and tropical origin for ants. Thus, contrary to previous hypotheses, species that forage individually cannot be categorically considered primitive, but rather appear to be derived from recruiter species. Therefore, we conclude that temperature influences the evolution and/or stability of chemical signals in ants by determining the recruitment of nest mates.
Key words: ants, chemical-signal evolution, foraging systems, Formicidae, surface temperature, trail pheromones..
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Natural selection favors signals, receptors, and signaling behavior that maximize the received signal relative to background noise and that minimize signal degradation (Endler, 1992
). The environment is spatially and temporally heterogeneous,
and its physical properties affect rates of attenuation and degradation of the
signal (Endler, 1986,
1990 ;
Halliday and Slater, 1983 ;
Lythgoe, 1979 ; Ryan,
1985,
1988 ;
Wiley and Richards, 1982).
Signals should depend on habitat, as has been reported concerning color
pattern in fish (Levine and MacNichol,
1979 ; Lythgoe,
1979). This relationship should also be important in the evolution
and maintenance of chemical signals, mostly in those that have to act for a
long time, because most signaling chemical components are temperature
dependent. For example, Markow and Toolson
(1990) found that two
different populations of Drosophila mojavensis showed different
combinations of epicuticular dienes (used as pheromone to affect mate choice)
varying in volatility in relation to the mean temperature of the two
sites.
In ants, chemical signals allowing recruitment to exploit a food resource
is a well-known phenomenon. Some ant species mark the way to food by laying a
pheromone trail that is followed by nest mates
(Hölldobler
and Wilson, 1990). The use of pheromone trails in ants is
considered an adaptive trait because (1) recruitment species are more
efficient than individual-foraging species
(Baroni-Urbani, 1989,
Jaffe and Deneubourg, 1992) ;
(2) the use of pheromone trails reduces the cost of nest defense because
individual defense of territory is more costly than mass defense
(Hölldobler,
1974) ; (3) the individual foraging system is considered the
ancestral state of the different foraging behaviors in ants
(Baroni-Urbani, 1993) ; and (4)
it has been suggested that the complexity of the foraging system in ants
reflects an evolutionary gradient in the phylogeny of Formicidae (see, e.g.,
Baroni-Urbani, 1993 ;
Dumpert, 1978 ;
Fresneau, 1985 ;
Hölldobler
and Wilson, 1990).
Several ecological factors have been proposed as influences on ant foraging
systems (Ayre, 1958 ;
Crist and MacMahon, 1991 ;
García-Pérez
et al., 1994), such as vegetation structure
(Fewell, 1988), food
availability (Ayre, 1958), food
abundance (Brown et al., 1979
; Davidson, 1977 ;
Steinberger et al., 1991), and
food predictability
(Sundström,
1993) and distribution
(Bernstein, 1975 ;
Whitford, 1978). Temperature
has been proposed as a major factor influencing prey-size selection
(Traniello et al., 1984) and
foraging behavior in ants
(Cerdá et
al., 1998b ; Crist and
MacMahon, 1991 ; Crist and
Williams, 1999). The relationship between recruitment behavior and
soil temperature has been previously suspected
(Carroll and Janzen, 1973 ;
Cerdá et
al., 1989 ; Marsh,
1988 ;
Sundström,
1993 ; Traniello,
1989), but was not considered to be a rule because there are
species that forage individually at cold (Nothomyrmecia macrops,
Hölldobler
and Taylor, 1983) or warm temperatures (Pachycondila
apicalis, Fresneau,
1985).
In response to this environmental variation, many ant species can change
their foraging strategies from collective to individual
(Crist and MacMahon, 1991 ;
Detrain et al., 1990 ;
Traniello, 1989). For
instance, individual foraging can be as efficient as recruitment, or more so,
at low prey densities (Calenbuhr and
Deneubourg, 1992 ; Crist and
Haefiner, 1994) and therefore would be associated with scattered
and unstable food sources (Bernstein,
1975 ; Carroll and Janzen,
1973 ;
Cerdá et
al., 1989 ; Fewell,
1988 ;
Sundström,
1993 ; Wehner et al.,
1983 ; Whitford,
1978). However, the optimal foraging strategy for a colony is best
evaluated only in terms of its effect on colony fitness and should not be
confused with the sum of optimal foraging by individuals
(Carroll and Janzen, 1973 ;
Fewell, 1988 ;
Rissing and Pollock, 1984). In
this sense, there are no comparisons available between species that forage
individually and species that are able to recruit nest mates.
In agreement with hypotheses suggesting that foraging patterns in ants
constitute adaptations by individual species to particular conditions in their
environment
(Hölldobler,
1978 ; Jaffe,
1984), it has been shown that different foraging patterns can
appear or disappear in the phylogenetic tree in a completely random manner
(Baroni-Urbani, 1989 ;
Beckers et al., 1989) and that
the distribution of foraging patterns in the Formicidae taxa do not fit any
conceivable phylogeny
(Hölldobler,
1978 ; Jaffe,
1984).
Pheromones in ants are hydrocarbons and fatty acids, which are volatile
components depending on the temperature
(Morgan, 1984), and their
production should be costly. Moreover, it is known that the duration of a
pheromone trail is crucial for its effectiveness as a signal
(Hölldobler
and Wilson, 1990). However, although different hypotheses have
been proposed (see review by Baroni-Urbani,
1993) for the evolution of recruitment systems (directly related
to ant species being able to lay a pheromone trail), environmental temperature
has never been seen as a factor influencing evolution of recruitment systems
or associated pheromones. In this article, we hypothesize that environmental
temperature should influence the evolution or maintenance of this chemical
signal because the life span of the pheromone trail is likely to depend on the
environmental temperature.
In any case, environmental factors such as those described above are also
related to environmental temperature because it is known that temperature
influences vegetation distribution, as well as food availability and
distribution, in different habitats (Begon
et al., 1987). Therefore, at the level of species, the hypothesis
that temperature could influence the evolution and maintenance of signals,
related to the ability of recruitment to be used in exploiting food resources,
would be as plausible as others related to environmental factors.
Because pheromones deposited on the soil are highly volatile
(Billen and Morgan, 1998), a
high soil-surface temperature would reduce the coefficient of diffusion
(Bossert and Wilson, 1963) and
therefore would diminish the usefulness of these chemical signals. In the
present study, we assessed whether species' ability to use chemical trails
(estimated as the ability to recruit nest mates) is effectively correlated
with soil temperature. Thus, we predict (prediction 1) that species active at
high soil temperatures do not use chemical signals for nest mate recruitment
because these signals are inefficient and are therefore counter-selected.
Because temperature is related to other environmental factors (see above), it is difficult to isolate the temperature effect. However, species that exploit the same resources in the same habitats, but at different times of day, and thereby at different surface temperatures when they forage, can be used to test the importance of temperature in the foraging strategy independently of other environmental conditions. We predict (prediction 2) that for sympatric species those foraging at higher temperature should not use chemical recruitment because pheromones are not effective.
One of the points supporting the idea that the use of different foraging
strategies is related to environmental conditions is that foraging strategies
occur apparently randomly in the ant phylogenetic tree
(Baroni-Urbani, 1993). However,
most of the described foraging strategies use pheromones to recruit nest mates
(see Materials and Methods), and only those foraging solitarily do not use
pheromones and thus do not recruit nest mates. Therefore, if we classify
foraging strategies in two categories, using or not using pheromones, under
the hypothesis presented above, we predict (prediction 3a) that pheromone use
to recruit nest mates does not appear at random in the phylogenetic tree but
is related to temperature. Moreover, ample evidence suggests a forest and
tropical origin for ants (e.g.,
Baroni-Urbani, 1995), and
therefore the colonization of temperate and arid zones must have been a later
event in the evolution of the ants. We then predict that the common ancestry
may have used pheromones to recruit nest mates but derived groups foraging in
high-temperature habitats should not (prediction 3b).
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Focusing on the evolution and maintenance of chemical signals that enable ants to recruit nest mates, we classified ant species according to those able to recruit nest mates (recruiters) and those never detected recruiting nest mates (solitary). We assume that while recruiter species produce chemical signals for recruitment, solitary species do not, or that such signals are ineffective.
Data collection
We collected data from the literature for all ant species for which
information was available on maximal soil-surface temperatures during the
ants' activity and mode of foraging (recruitment or solitary). We considered
recruiter species those using recruitment systems such as group recruitment,
mass recruitment, and trail and trunk-trail species. We have limited our
comparison to species in Formicinae and Myrmicinae, for which ample ecological
and behavioral information is available. We have omitted species that use
tandem running and tandem calling because this recruitment is not based
exclusively on the use of chemical signals, or they do not deposit the signals
on the soil
(Hölldobler
and Wilson, 1990 ; Jaffe,
1984). We analyzed 50 ant species (Table 1) that met the following
conditions : (1) maximal surface temperatures during activity on the soil are
known, although these ants could also forage in other habitats (this condition
excludes most treedwelling and tropical species) ; and (2) diurnal species in
which activity patterns can be influenced by temperature fluctuation. This
latter condition enables us to examine the possible effects of higher
temperatures on ant activity and on possible deposited chemical signals. We
did not use the soil temperature corresponding to the optimum activity range
because such data are scant, and therefore we assumed that species active at
high maximal temperatures in general have high optimal temperatures for
activity.
Others factors besides the temperature, such as vegetation structure,
resource availability, resource abundance, and resource predictability, have
also been suggested to influence foraging systems in ants (see introductory
section). However, humidity, as well as temperature, determines these
ecological factors (Begon et al.,
1987), and it is difficult to distinguish between the effect of
such factors and temperature in the foraging system used by ants. One way to
distinguish between the effects of temperature and other environmental factors
is to experimentally manipulate soil temperature. However, if the ability to
recruit nest mates is a fixed character in ant species and nonrecruiter
species have lost the ability to produce pheromones for recruitment,
interspecific experiments will not clarify the evolution of this character,
and thus comparative methodology is the only feasible way to study the factors
influencing the evolution of recruitment. A second possibility is to compare
foraging behavior of sympatric species that share the same habitat and thus
habitat structure, food availability, and other variables but that have
different activity patterns at different temperatures. In these cases we
recorded data on time of maximum activity in summer of several sympatric ant
species and temperature at which ants reach the highest activity, or
percentage of ants active at maximal temperatures.
Statistical analyses
To avoid biased analyses due to the fact that two species may share common
ancestry and thus have many characters in common, we used available
comparative methodologies that account for the effect of common phylogenetic
ancestry when studying possible relationships between two different
characters. First, we used the pairwise comparative method
(Møller and Birkhead,
1992) between pairs of species from the same genus that differ in
the variable expected to influence the variable of interest (soil temperature
and presence or absence of recruitment, respectively). For polytomies in a
genus, we used mean soil temperature values for recruiter and solitary
foraging species in the polytomy. Second, we used a comparative methodology
based on Felsenstein's (1985)
logic, modified to search for correlated evolution between a continuous trait,
Y (maximal soil temperature at which species are active), and one
independent trait, X, occurring only in two discrete states :
presence or absence of recruitment, assigned 1 or 0, respectively (categorical
variable). This methodology was applied using a computer program (CAIC 2.0.0)
written by Purvis and Rambaut
(1995), which finds a set of
independent, pairwise differences or contrasts, assuming that changes along
the branches of the phylogeny can be modeled by a Brownian motion process
(successive changes are independent of one another) and that the expected
total change (i.e., the sum of many independent changes) is zero
(Harvey and Pagel, 1994). In
this case, we assumed a punctuational model of evolution. We could not use
Grafen's method, which assumes that the ages of taxa are proportional to the
number of species they contain (Purvis and
Rambaut, 1995), because the number of species we could use in
analysis depends on the available information pertaining to recruitment and
activity rhythm. The computer program CAIC performs the analyses reasonably
well, even with grossly inaccurate branch lengths, and certainly performs much
better than any method that treats species values as independent
(Purvis et al., 1994).
We have reconstructed a phylogeny based on Agosti
(1991), Agosti and Bolton
(1990), Tinaut and Ruano
(1998), and Hasegawa et al.
(unpublished manuscript) for the subfamily Formicinae. The reconstructed
phylogeny of subfamily Myrmicinae was derived largely from Shultz and Meier
(1995), but the location of
tribes Crematogastrini, Solenopsidini, and Tetramorini, as well as the genus
Messor were from Bolton
(1976,
1982,
1987). The phylogeny was based
almost exclusively on morphological characters, and therefore we have no data
on branch lengths. Therefore, we set all branch lengths equal to 1. This means
that the dichotomous character (presence or absence of chemical signals for
recruitment) can be modeled by a process that allows the character to change
from one state to the other with a specified probability per unit of time. The
probability of a change is therefore assumed to be the same in all branches of
the phylogeny (Harvey and Pagel,
1991).
To reconstruct character states of hypothetical ancestors throughout the
phylogenetic tree (character evolution), we used the MacClade (3.0) computer
program written by Maddison and Maddison
(1992) that uses parsimony. We
assume unordered change and interpret polytomies as uncertainties in
resolution (soft polytomies).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Maximal soil temperature and nest mate recruitment
In agreement with prediction 1, species foraging individually are active at a statistically significant higher mean maximal soil temperature (mean = 52.6°C, SE = 1.9) compared to species that use chemical recruitment (mean = 42.4°C, SE = 1.3 ; Mann-Whitney U test, Z = 3.68, N1 = 35, N2 = 15, p =.00023). However, this result could be confounded by phylogeny because we treat species as independent data points (see Materials and Methods). To solve this possible phylogenetic drawback, we took into account the phylogenetic tree of the group and used two different comparative methodologies.
The 50 ant species analyzed (Table
1) provide a phylogenetic tree with 80 branches
(Figure 1). Some species
belonging to the same genus had different foraging systems
(Table 1). This occurred in
four different genera : (1) Tetramorium (T. sericeiventre forages
individually, whereas T. caespitum and T. semilaeve lay
chemical signals on the soil), (2) Monomorium (M. alamarum and M.
vatranum forage individually and M. minimum uses pheromones),
(3) Camponotus (C. cruentatus uses chemical recruitment and C.
detritus forages individually), and (4) Formica (F. subrufa
forages individually and F. ravida uses chemical recruitment). In
these four genera, species that forage individually do so at higher
temperatures than do species using pheromones for recruitment [pairwise
comparisons (Møller and Birkhead,
1992), paired t test, differences in soil temperatures
between recruiter and nonrecruiter pairs of species = -7.0, t = 4.76,
df = 3, p =.018]. Moreover, species that forage individually are
typical of desert or arid habitats (Marsh,
1988). There are other genera with an absence of chemical
recruitment (e.g., Melophorus, Ocymyrmex, and Cataglyphis ;
Table 1). Most of these taxa
that forage individually have two traits in common : they typically live in
arid environments and show higher maximal temperature of activity than do
related species from different genera, which use chemical signals for
recruitment.
|
|
When using phylogenetic independent-contrast methodology, we obtained seven negative, independent, standardized linear contrasts and zero positives. Among the taxa being contrasted, higher values of the maximal soil temperatures at which the species are active were consistently found in those that forage individually (two-tailed sign test, p =.0156).
However, temperature is related to other environmental factors, and thus
previous results could be the consequence of these relationships. To isolate
temperature effects on recruitment behavior in ants, we collected information
from the literature on foraging behavior, as well as variables related to
temperature during maximal activity in several sympatric ant species. We found
three studies with this kind of information (see
Table 2). In accordance with
prediction 2, in the first study
(Crós et
al., 1997), the only solitary foraging species (Cataglyphis
cursor) differs from the other recruiter species. Maximal activity of the
solitary species spanned from 1200 h to 1500 h, when temperature reached its
maximu. More-over, more than 90% of the individuals detected over the entire
day were found at this time. This difference between the solitary and the
recruiter species in foraging activity was statistically significant (Wilcoxon
test, t = 0, N = 7, p =.018 ;
Table 2). Data from the second
study (Heatwole and Muir,
1989) demonstrated that solitary ant species (Cataglyphis
bombycina and Cataglyphis aurata) are active at maximum
temperatures, whereas recruiter species are not. Moreover, temperatures during
maximal activity were significantly higher for solitary ant species
(Mann-Whitney U test, U = 0, N1 = 2,
N2 = 6, p =.046 ;
Table 2). Finally, data from
Marsh (1988) also supported
prediction 2 because ant species foraging solitary were active at mid-day, and
temperatures coinciding with maximal activity were higher for solitary species
(Mann-Whitney U test, U = 0, N1 = 4,
N2 = 2, p =.06 ;
Table 2). Therefore, the
hypothesis that temperature influences the use of chemical signals to recruit
nest mates is supported by behavior of sympatric ant species, with solitary
species being active at higher temperatures than recruiter species.
|
Reconstruction of nest mate recruitment in the phylogenetic
tree
Reconstruction of character evolution using parsimony reveals that,
notwithstanding two unresolved branches concerning the subfamily Formicinae,
the ancestral state of foraging system is recruitment
(Figure 1), in agreement with
prediction 3b. Furthermore, when the number of branches in the tree was
reduced according to the evolutionary changes detected in the foraging system,
the ancestral state also proves to be recruitment, and no unresolved branches
appear (Figure 2).
|
To test prediction 3b, we also used phylogenies from Baroni-Urbani
(1993) studying the evolution
of ant recruitment behavior, who concluded that the ancestral state of
foraging systems in ants is solitary. However, he did not address the use of
pheromones in nest mate recruitment, but rather in the evolution of the
different types of foraging behavior, using different degrees of nest mate
recruitment (trail laying, mass recruitment, and army ant behavior) as
independent discrete characters. When we classified species used by
Baroni-Urbani (1993) into
solitary or recruiter species (see Methods for criteria), using the same
phylogenies that he used for reconstructing character evolution using
parsimony, the resulting ancestral state in all six trees is recruitment
(Figure 3). In other words, the
common ancestor used pheromones to recruit nest mates.
|
Furthermore, in agreement with prediction 3a, the use of pheromones to recruit nest mates did not appear randomly in the phylogenetic trees. In all cases, regardless of the phylogenetic tree for reconstructing character evolution, all detected changes in foraging system were from nest mate recruitment to individual foraging (Figures 2 and 3). In addition, all calculated contrasts were negative. That is, a change in foraging system (from recruiter to solitary) corresponded to a significant increase in maximal soil temperature (see above).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
In this study, we hypothesized that environmental temperature influences the evolution or maintenance of foraging systems by changing the effectiveness of the associated pheromones. We established two different groups of predictions, the first assessing whether species' ability to use chemical trails correlated with soil temperature (predictions 1 and 2), and the second related to the evolution of this character in the Formicidae phylogenetic tree (predictions 3a and 3b).
By using two different comparative methodologies, we have demonstrated a
relationship between maximal temperature at which species are active and the
presence or absence of nest mate recruitment
(Figure 1), which is
hypothesized to be related to the presence or absence of chemical signals for
recruitment. Moreover, when comparing sympatric species from three different
studies (Table 2), differences
in foraging activity at maximum temperature appeared between recruiter and
solitary species. However, it could also be that those chemical signals occur
in species without recruitment, but, because temperature is negatively related
to their effectiveness (Bossert and
Wilson, 1963), chemical signals disappear quickly, not enabling
recruitment at high soil temperatures. Hence, because soil temperature appears
to determine the effectiveness of chemical signals
(Billen and Morgan, 1998 ;
Bossert and Wilson, 1963 ;
Hölldobler,
1976,
1978), which in terms of
resource allocation are costly produce, it can be predicted that, for ants
active with high soil temperature, natural selection should favor individuals
that do not allocate resources in a noneffective chemical product. This should
be the case in our data because species classified as nonrecruiters never have
been detected foraging in groups (see Materials and Methods), and therefore it
is likely that these species do not have the ability to produce chemical
recruitment signals.
At high temperatures, the most efficient foraging system appears to be
individual foraging because it offers certain advantages, such as reduced
competition for resources with other mass-recruiter species
(Cerdá et
al., 1998a). We have found cases of closely related species having
opposite kinds of recruitment (see Table
1) but that are active at different maximal soil temperatures (see
Results). Species with strict physiological impositions can adapt activity
cycles to only the most favorable soil temperatures, their recruitment system
being related to their optimal temperatures. This occurs, for example, in
species belonging to the genus Messor, which lives in desert or
subdesert habitats and invariably restricts its activity periods during the
hot season to early morning and late afternoon
(Baroni-Urbani and
Aktaç, 1981 ;
Delalande and Lenoir, 1984 ;
Heatwole and Muir, 1989 ;
Steinberger et al., 1991). All
this confirms the relationship between temperature, foraging system, and
guild, and thus it is not a coincidence that when temperatures rise, the
foraging system changes.
Our hypothesis of temperature forcing the evolution or maintenance of
foraging systems in ants on the basis of a temperature habitat for a
Formicidae ancestry (see Introduction) predicted a recruiter ancestry because
of the absence of high temperature. In insects, trial use has evolved twice
among ground-dwelling social insects (ants and termites), and once in a
species of bees (Bombus transversalis)
(Cameron and Whitfield, 1996).
Thus, trail use appears to be related to social behavior. In fact, a
relationship has been suggested among colony size, communication, and foraging
strategy in ants because ant species with solitary foraging have small colony
sizes (Beckers et al., 1989).
This is the case for Myrmecia
(Jaffe, 1984 ;
Wilson, 1971),
Neoponera (Fresneau,
1985), and Nothomyrmecia species
(Hölldobler
and Taylor, 1983 ; Jaffe,
1984). Moreover, ant species with small colony sizes are
considered more primitive than species with large colony sizes
(Beckers et al., 1989) because
of the hypothetical nonsocial ancestry of the true Formicidae group
(Baroni-Urbani, 1989 ;
Grimaldi et al. 1997). Based
on these two assumptions, a prevalent view is that "primitive"
ants (with small colony size) should be unable to recruit or able to recruit
only a few individuals, whereas more advanced ant species should have
developed pheromonal and anatomical means to enable the recruitment of larger
numbers of individuals simultaneously
(Baroni-Urbani, 1993, and
references therein).
However, the association between colony size and foraging strategy in ants
is not clear because several recruiter species (Pogonomyrmex, for
instance) have smaller nest populations than do some solitary species (e.g.,
some Cataglyphis species with more than 2000 workers) (see other
examples in
Hölldobler
and Wilson, 1990 ; Wehner et
al., 1983). Moreover, modern ant phylogenies
(Grimaldi et al., 1997 ;
Schultz and Meier, 1995) do
not support the interpretation of ant evolution reflecting the complexity of
the foraging system, and it is not clear whether primitive species are in fact
nonrecruiters with small colony sizes.
In our phylogenetic tree, the appearance of individual foraging in different tribes points to a nonphylogenetic explanation for the foraging systems in the majority of ants we studied (Figures 1-3). Furthermore, our results (Figure 3) demonstrate that, when reconstructing evolution of foraging systems (recruiter versus solitary), the ancestral state in ants is recruitment, and all seven cases of nonrecruiter species developed from recruiter ancestries. Thus, in accordance with our hypothesis, recruitment must have appeared very early in the ant phylogenetic tree, and it is the most parsimonious state of the ancestry of the true Formicidae groups in our phylogenetic trees (Figures 2 and 3).
A nonadaptive explanation could also match our results. That is, solitary species may not have evolved from recruiter ancestries but, being better able to exploit resources under high temperature, could colonize desert environments. However, we have recorded no case where recruiter species appeared from nonrecruiter ancestry (Figures 1-3). Moreover, desert environments harbor both recruiter and solitary species, and their activity correlates with the temperature, with solitary species being active at higher temperatures. Thus, it is unlikely that differences in the ability to colonize desert environments explains the relationship between maximal soil temperature and foraging behavior in the two groups of ants. From this perspective, species that forage individually cannot be categorically considered primitive but rather derived from recruiter species.
In conclusion, our results confirmed the hypothesis that temperature influences the evolution and maintenance of chemical signals related to the ability of recruitment to exploit food resources in ants. This is because (1) species active at high soil temperature do not recruit nest mates, even after controlling for environmental variables other than temperature ; (2) the use of pheromones to recruit nest mates disappears in the phylogenetic tree in relation to temperature increases ; and (3) recruitment is the ancestral state of solitary foraging. This temperature effect on pheromones represents another facet of the importance of temperature in the structure of the ant communities.
|
ACKNOWLEDGEMENTS |
|---|
A. Hefetz made helpful comments on different versions of the manuscript and always encouraged us publish our results. X. Cerdá, J. Retana, A. Lenoir, and two anonymous reviewers provided valuable comments on the manuscript. A. N. Andersen gave us unpublished information on Melophorus. R. Requerey provided us with some bibliographic references. D. Nesbitt corrected the translation of the manuscript to English. This research was partially financed by the Dirección General de Investigación Científica y Técnica, project number PB94-0768.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Agosti D, 1991. Revision of the oriental ant genus Cladomyrma, with an outline of the higher classification of the Formicinae (Hymenoptera : Formicidae). Syst Entomol 16 : 293-310.
Agosti D, Bolton B, 1990. New characters to differentiate the ant genera Lasius F. and Formica L. (Hymenoptera : Formicidae). Entomol Gaz 41 : 149-156.
Ayre GL, 1958. Some meteorological factors affecting the foraging of Formica subnitens Creighton (Hymenoptera : Formicidae). Insect Soc 5 : 147-157.
Baroni-Urbani C, 1989. Phylogeny and behavioural evolution in ants, with a discussion of the role of behaviour in evolutionary processes. Ethol Ecol Evol 1 : 137-168.
Baroni-Urbani C, 1993. The diversity and evolution of recruitment behaviour in ants, with a discussion of the usefulness of parsimony criteria in the reconstruction of evolutionary histories. Insectes Soc 40 : 233-260.
Baroni-Urbani C, 1995. Invasion and extinction in the West Indian ant fauna revised : the example of Pheidole (Amber Collection Stuttgart : Hymenoptera, Formicidae. VIII : Myrmicinae, partim). Stuttgarter Beitr Naturk 222 : 1-29.
Baroni-Urbani C, Aktaç N, 1981. The competition for food and circadian succession in the ant fauna of a representative Anatolian semi-steppic environment. Bull Soc Entomol Suisse 54 : 33-56.
Beckers R, Goss S, Deneubourg JL, Pasteels JM, 1989. Colony size, communication and ant foraging strategy. Psyche 96 : 239-256.
Begon M, Harper JL, Townsend CR, 1987. Ecology : individuals, populations, and communities. Oxford : Blackwell.
Bernstein RA, 1975. Foraging strategies of ants in response to variable food density. Ecology 56 : 213-219.
Billen J, Morgan ED, 1998. Pheromone communication in social insects : sources and secretions. In : Pheromone communication in social insects (Vander-Meer RK, Breed MD, Espelie KE, Winston ML, eds). London : Westview Press; 3-33.
Bolton B, 1976. The ant tribe Tetramorini (Hymenoptera : Formicidae) constituent genera, review of smaller genera and revision of Triglyphotrix Forel. Bull Br Mus Nat Hist (Entomol) 34 : 283-278.
Bolton B, 1982. Afrotropical species of the Myrmicinae ant genera Cardiocondyla, Leptothorax, Melissotarsus, Messor and Cataulacus (Formicidae). Bull Br Mus Nat Hist (Entomol) 45 : 307-370.
Bolton B, 1987. A review of the Solenopsis genus group and revision of Afrotropical Monomorium Mayr (Hymenoptera : Formicidae). Bull Br Mus Nat Hist (Entomol) 54 : 263-452.
Bossert WH, Wilson EO, 1963. The analysis of olfactory communication. J Theor Biol 5 : 443-469.[ISI][Medline]
Brown JH, Reichman OJ, Davidson DW, 1979. Granivory in desert ecosystems. Annu Rev Ecol Syst 10 : 201-227.[ISI]
Calenbuhr V, Deneubourg JL, 1992. Pattern formation via chemical communication : collective and individual hunting strategies. In : Biology and evolution of social insects (Billen J, ed). Leuven : Leuven University Press; 343-345.
Cameron SA, Whitfield JB, 1996. Use of walking trails by bees. Nature 379 : 125.[Medline]
Carroll CR, Janzen DH, 1973. Ecology of foraging by ants. Annu Rev Ecol Syst 4 : 231-257.
Caviá-Miralles V, 1988. Formica subrufa Roger, 1859 (Hymenoptera, Formicidae) : aportación al estudio de su etología y ecología (Memoria de Licenciatura). Barcelona : Universitat Autónoma de Barcelona.
Cerdá X, Retana J, Bosch J, Alsina A, 1989. Daily foraging activity and food collection of the thermophilic ant Cataglyphis cursor (Hymenoptera, Formicidae). Vie Milieu 39 : 207-212.
Cerdá X, Retana J, Cros S, 1998a. Critical thermal limits in Mediterranean ant species : trade-off between mortality risk and foraging performance. Funct Ecol 12 : 45-55.
Cerdá X, Retana J, Manzaneda A, 1998b. The role of competition by dominants and temperature in the foraging of subordinate species in Mediterranean ant communities. Oecologia 117 : 404-412.
Crist TO, Haefner JW, 1994. Spatial model of movement and foraging in harvester ants (Pogonomyrmex) (II) : the roles of environment and seed dispersion. J Theor Biol 166 : 315-323.
Crist TO, MacMahon JA, 1991. Foraging patterns of Pogonomyrmex occidentalis (Hymenoptera : Formicidae) in a shrub-steppe ecosystem : the roles of temperature, trunk trails, and seed resources. Environ Entomol 20 : 265-275.
Crist TO, Williams JA, 1999. Simulation of topographic and daily variation in colony activity of Pogonomyrmex occidentalis (Hymenoptera : Formicidae) using a soil temperature model. Environ Entomol 28 : 659-668.
Crós S, 1995. Explotació dels Recursos Alimentaris en Tres Communitats Mediterrànies de Formigues (PhD dissertation). Barcelona : Universitat Autónoma de Barcelona.
Crós S, Cerdá X, Retana J, 1997. Spatial and temporal variations in the activity patterns of Mediterranean ant comunities. Ecoscience 4 : 269-278.
Christian KA, Morton SR, 1992. Extreme thermophilia in a central australian ant, Melophorus bagoti. Physiol Zool 65 : 885-905.
Davidson DW, 1977. Foraging ecology and community organization in desert seed-eating ants. Ecology 58 : 725-737.
Delalande C, Lenoir A, 1984. Exploitation de sources de nourriture par Messor structor. Interaction avec deux autres espéces de fourmis (Hym. Formicidae). Act Coll Insect Soc 1 : 49-56.
Detrain C, Pasteels JM, Deneubourg JL, Goss S, 1990. Prey foraging by the ant Pheidole pallidula : decision making systems in food recruitments. In : Eleventh International Congress IUSSI, India, 1990. New Delhi : Oxford & IBH Publishing; 550-551.
Dumpert K, 1978. The social biology of ants. London : Pitman.
Endler JA, 1986. Defense against predation. In : Predator-prey relationships, perspectives and approaches from the study of lower vertebrates (Feder ME, Lauder GV, eds). Chicago : University of Chicago Press; 109-134.
Endler JA, 1990. On the measurement and classification of colour in studies of animal colour pattern. Biol J Linn Soc 41 : 315-352.
Endler JA, 1992. Signals, signal conditions, and the direction of evolution. Am Nat 139 : 125-153.
Felsenstein J, 1985. Phylogenies and the comparative method. Am Nat 125 : 1-15.
Fernández Escudero I, Tinaut A, 1998. Heat-cold dialectic in the activity of Proformica longiseta, a thermophilous ant inhabiting a high mountain (Sierra Nevada, Spain). Int J Biometeorol 41 : 175-182.
Fewell J, 1988. Variation in foraging patterns of the western harvester ant, Pogonomyrmex occidentalis, in relation to variation in habitat structure. In : Interindividual behavioral variability in social insects (Robert J, ed). London : Westview Press; 257-258.
Fresneau D, 1985. Individual foraging and path fidelity in a ponerine ant. Insectes Soc 32 : 109-116.
Gamboa GJ, 1976. Effects of temperature on the surface activity of the desert leaf-cutter ant, Acromyrmex versicolor versicolor (Pergandei) (Hymenoptera : Formicidae). Am Midland Nat 95 : 485-491.
García-Pérez JA, Rebeles-Manríquez A, Peña-Sánchez R, 1994. Seasonal changes in trails and the influences of temperature in foraging activity in a nest of the ant Pogonomyrmex barbatus. SW Entomol 19 : 181-187.
Grimaldi D, Agosti D, Carpenter JM, 1997. New and rediscovered primitive ants (Hymenoptera : Formicidae) in Cretaceous amber from New Jersey, and their phylogenetic relationships. Am Mus Nov 3208.
Halliday TR, Slater PJB, 1983. Communication. New York : W.H. Freeman.
Harvey PH, Pagel MD, 1991. The comparative method in evolutionary biology. Oxford : Oxford University Press.
Heatwole H, Muir R, 1989. Seasonal and daily activity of ants in the pre-Saharan steppe of Tunisia. J Arid Environ 16 : 49-67.
Hölldobler B, 1974. Home range orientation and territoriality in harvesting ants. Proc Natl Acad Scienc USA 71 : 3274-3277.
Hölldobler B, 1976. Recruitment behavior, home range orientation and territoriality in harvester ants, Pogonomyrmex. Behav Ecol Sociobiol 1 : 3-44.
Hölldobler B, 1978. Ethological aspects of chemical communication in ants. Adv Study Behav 8 : 75-115.
Hölldobler B, Taylor RW, 1983. A behavioural study of the primitive ant Nothomyrmecia macrops Clark. Insectes Soc 30 : 384-401.
Hölldobler B, Wilson EO, 1990. The ants. Cambridge, Massachusetts : Belknap Press.
Jaffe K, 1984. Negentropy and the evolution of chemical recruitment in ants (Hymenoptera : Formicidae). J Theor Biol 106 : 587-604.
Jaffe K, Deneubourg JL, 1992. On foraging, recruitment systems and optimum number of scouts in eusocial colonies. Insectes Soc 39 : 201-213.
Kay CAR, Whitford W, 1978. Critical thermal limits of desert honey ants : possible ecological implications. Physiol Zool 51 : 206-213.
Levine JS, MacNichol EF Jr, 1979. Visual pigments in teleost fishes : effects of habitat, microhabitat, and behavior on visual system evolution. Sens Process 3 : 95-131.
Lythgoe JN, 1979. The ecology of vision. Oxford : Oxford University Press.
MacKay EE, MacKay WP, 1984. Biology of the thatching ant Formica haemorrhoidalis Emery (Hymenoptera : Formicidae). Pan Pacif Entomol 60 : 79-87.
Maddison WP, Maddison DR, 1992. MacClade : analysis of phylogeny and character evolution, version 3.0. Sunderland, Massachusetts : Sinauer Associates.
Markow TA, Toolson EC, 1990. Temperature effects on epicuticular hydrocarbons and sexual isolation in Drosophila mojavensis. In : Ecological and evolutionary genetics of Drosophila (Baker JSF, Starmer WT, MacIntyre RJ, eds). New York : Plenum Press; 315-331.
Marsh AC, 1985. Microclimatic factors influencing foraging patterns and success of the thermophilic desert ant, Ocymyrmex barbiger. Insect Soc 32 : 286-296.
Marsh AC, 1988. Activity patterns of some Namib Desert ants. J Arid Environ 14 : 61-73.
Møller AP, Birkhead TR, 1992. A pairwise comparative method as illustrated by copulation frequency in birds. Am Nat 139 : 644-656.
Morgan ED, 1984. Chemical words and phrases in the language of pheromones for foraging and recruitment. In : Insect communication (T. Lewis ed). London : Academic Press; 169-194.
Purvis A, Gittleman JL, Luh HK, 1994. Truth or consequences : effects of phylogenetic accuracy on two comparative methods. J Theor Biol 167 : 293-300.
Purvis A, Rambaut A, 1995. Comparative analysis by
independent contrasts (CAIC) : an Apple Macintosh application for analysing
comparative data. Comput Appl Biosci 11
: 247-251.
Rissing SW, Pollock GB, 1984. Worker size variability and foraging efficiency in Veromessor pergandei (Hymenoptera : Formicidae). Behav Ecol Sociobiol 15 : 121-126.
Ruano F, Tinaut A, 1999. Raid process, activity pattern and influence of abiotic conditions in the slave-making ant Rossomyrmex minuchae (Hymenoptera, Formicidae). Insectes Soc 46 : 343-347.
Ryan MJ, 1985. The Túngara frog : a study in sexual selection and communication. Chicago : University of Chicago Press.
Ryan MJ, 1988. Constraints and patterns in the evolution of anuran acoustic communication. In : The evolution of the amphibian auditory system (Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W, eds). New York : Wiley; 637-675.
Shultz TR, Meier R, 1995. A phylogenetic analysis of the fungus-growing ants (Hymenoptera : Formicidae : Attini) based on morphological characters of the larvae. Syst Entomol 20 : 337-370.
Steinberger Y, Leschner H, Shmida A, 1991. Chaff piles of harvester ant (Messor spp.) nests in a desert ecosystem. Insectes Soc 38 : 241-250.
Sundström L, 1993. Foraging responses of Formica truncorum (Hymenoptera : Formicidae); exploiting stable vs spatially and temporally variable resources. Insectes Soc 40 : 147-161.
Tinaut A, Ruano F, 1998. Implications phylogenetiques du mechanisme de recrutement chez Rossomyrmex minuchae. (Hym. Formicidae). Act Coll Insect Soc 11 : 125-132.
Topoff H, LaMon B, Goodloe L, Goldstein M, 1985. Ecology of raiding behavior in the western slave-making ant Polyergus breviceps (Formicidae). SW Nat 30 : 259-267.
Traniello JFA, 1989. Foraging strategies of ants. Annu Rev Entomol 34 : 191-210.[ISI]
Traniello JFA, Fujita MS, Bowen RV, 1984. Ant foraging behavior : ambient temperature influences prey selection. Behav Ecol Sociobiol 15 : 65-68.
Wehner R, Harkness RD, Schmid-Hempel P, 1983. Foraging strategies in individually searching ants Cataglyphis bicolor (Hymenoptera : Formicidae). Information processing in animals, vol. 1 (Lindauer M, ed). Stuttgart : Gustav Fisher Verlag.
Wehner R, Marsh AC, Wehner S, 1992. Desert ants on a thermal tightrope. Nature 357 : 586-587.
Whitford WG, 1978. Foraging in seed-harvester ants Pogonomyrmex spp. Ecology 59 : 185-189.
Wiley RH, Richards DG, 1982. Adaptations for acoustic communication in birds, vol 1. New York : Academic Press.
Wilson EO, 1971. The insect societies. Cambridge, Massachusetts : Belknap Press.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  E. M. Buchkremer and K. Reinhold Sector fidelity--an advantageous foraging behavior resulting from a heuristic search strategy Behav. Ecol., May 19, 2008; (2008) arn057v1. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||