Download Impact of Argentine ants (Linepithema humile) on an arboreal ant

Biodiversity and Conservation 14: 151–163, 2005.
# Springer 2005
Impact of Argentine ants (Linepithema humile)
on an arboreal ant community in Doñana
National Park, Spain
S. CARPINTERO1, J. REYES-LÓPEZ2,* and L. ARIAS DE REYNA3
1
Department of Ciencias Ambientales (Zoology), University of Pablo de Olavide (Sevilla), Ctra, de
Utrera km 1, E-41013 Seville, Spain; 2Department of Ecology, Faculty of Science, University of Cordoba,
E-14071 Cordoba, Spain; 3Department of Animal Biology, Faculty of Science, University of Cordoba,
E-14071 Cordoba, Spain; *Author for correspondence (e-mail: [email protected])
Received 19 February 2003; accepted in revised form 1 October 2003
Key words: Arboreal ant community, Competition, Doñana National Park, Invasive Argentine ant
Abstract. Due to the invasive character of the exotic Argentine ant (Linepithema humile), its use of
aphids in trees, and the ecological importance of the Doñana National Park (Spain) that is invaded by this
species, we designed a study to analyze the extent of the problem with native species of arboreal ants. By
searching for ‘de visu’ the species that inhabited 182 cork trees, we found out that the structure of the
community of native arboreal ants has been greatly influenced by interspecific competition. The introduced species L. humile and the native species Crematogaster scutellaris and Lasius brunneus are
dominant, while Camponotus lateralis and Camponotus truncatus are subordinate species associated
with C. scutellaris. The distribution of the species in the trees depends on these relationships. Species
richness is determined by tree size, thus, when a tree is large enough all native species may appear
together. However, in areas colonized by L. humile, this is the only species occupying the tree, regardless
of tree size. L. humile is displacing native arboreal ant species as shown by the fact that from 1992 to
2000 the exotic species occupied 23 new cork trees (of the 182 studied) previously inhabited by native
species.
Introduction
Dominant territorial ants typically show mutually exclusive territories, giving rise
to a pachy or mosaic distribution, though dominant ants may tolerate some
‘subordinate’ ant species in their territories, but not others. This fact has been
extensively studied in arboreal ants (Young 1983; Jackson 1984; Savolainen and
Vepsäläinen 1988, 1989; Adams 1994; Andersen and Patel 1994; Perfecto 1994;
Punttila et al. 1994). In consequence, the invasion of aggressive exotic species, such
as the Argentine ant (Linepithema humile Mayr, 1868), may greatly disrupt the
structure of native ant communities.
One of the preferred resources of the exotic Argentine ant is the exudate of
homoptera. This exudate provides a large amount of carbohydrates, which are good
as fuel or for producing defensive compounds and different types of pheromones
(Human and Gordon 1997; Holway 1999). Thus, it is common to find these ants
looking for this food in trees and shrubs. A large number of trees (Quercus suber and
Pinus pinea) were found to be infested with Argentine ants in Doñana National Park
152
(Huelva, Spain). At first sight, this species seemed to remain close to areas inhabited
by humans, although we could not exclude the possibility of finding them in natural
habitats. Trees in Doñana are a scarce and valuable resource for arboreal species
(Fernández 1982); for this reason and because of the invasive character of the
Argentine ant, we designed a study to determine the extent of the problem: first to
identify the structure of the arboreal native ant community; then to analyze the
impact of Argentine ants on this community; and finally, to relate the presence of
different species to some characteristics of the trees (such as their size and situation).
Materials and methods
Study site
Doñana National Park is located at the southwest coast of the Iberian Peninsula and
includes a large area of marshlands at the Guadalquivir and Guadiamar river
mouths (378110 –368470 N, 68100 –68470 W). The park was created in 1969, mainly to
protect aquatic fowl for which it is an important overwintering spot.
In the Park there are different ecotopes (Figure 1). One of those, ‘La Vera’,
located at the edge of the marshlands, is mainly covered by a eutrophic pastureland
with patches of reed beds and scrubland (Juncus spp., Ulex spp., Rubus ulmifolius,
Pteridium aquilinum, etc.). In this ecotope, the area known as the ‘Pajareras’
contains several large cork trees (Q. suber) that have been colonized by numerous
nesting birds (principally of family Ardeidae).
In 1585 a palace was constructed (Doñana Palace) in the heart of the current
Park, close to ‘La Vera’, when the territory was still private and used for hunting.
Today the Palace remains as a residence for researchers and visitors. Other
buildings were subsequently added to be used as offices, laboratories and headquarters of park rangers. A dense population of Argentine ants has been found
surrounding this humanized area and this constitutes one of the principal sources of
infestation of this species in the Park.
Sampling methods
In this work, from June to September 1992, we studied and sampled the ant fauna
of all cork trees (Q. suber) included in a circular area of 1.5 km radius, with
Doñana Palace at the center of the circle. There were a total of 182 trees in this
area. Sampling was repeated in September 2000. In general, arboreal insect communities have been poorly explored, in part due to a scarcity of methods with which
to do so (but see Kaspari 2000). In this study, searches for ants were conducted on
each cork tree at different times of the day (three visits per tree: morning, midday
and evening), each observation during 10 min to detect the ants patrolling trunks
and branches from 0.5 to 2 m in height. The following variables were determined
for each tree: (1) species of ants present; (2) trunk circumference at 1.5 m height;
(3) distance to Palace; (4) distance to nearest road, since the presence of Argentine
153
Figure 1. (Modified from Montes et al. 1998.) (1) Low lands in stable dunes. (2) High humid lands in
stable dunes. (3) High dry lands in stable dunes. (4) Semistable dunes. (5) Wandering dunes. (6) Old
inland marsh. (7) Marsh of the rivers Rocina and Guadiamar. (8) Meadow between marsh and bushland
(‘La Vera’). (9) Beaches. Palace of Doñana, and inside the circle, the studied area.
ants has been associated with the existence of nearby roads in other infested areas
(De Kock and Giliomee 1989).
Secondly, aggressiveness tests were conducted between species to define the
structure of the arboreal ant community. To perform the tests between more
abundant species in cork trees (found in N30 trees), worker ants were confronted
one to one in a 5.5 cm petri dish for 5 min. Details of the species that initiated
encounters and behavioral patterns of both species were registered with a video
recorder. The test was repeated 10 times for each pair of species with different
individuals. Behavioral patterns detected were as follows:
Aggressiveness: (1) Physical attack: when an ant bit another ant’s body, antennae or
legs; (2) Chemical attack: the attacker flexed its abdomen and expelled a repellent
onto the enemy; (3) Threat: the ant opened its mandible and moved its head towards
its opponent.
154
Submission: (1) Retreat: when an ant, following contact, quickly moved away
from another ant; (2) Pupal position: when the ant retracted its antennae and legs
and remained immobile.
Other patterns: Indifference: this occurred when an ant in an encounter did not
demonstrate aggressive or submissive behavior.
In previous observations, two native species (Camponotus lateralis and
C. truncatus) were occasionally seen using trophic trails of another species (C.
scutellaris). In order to determine if this behavior was habitual, 106 C. lateralis and
114 C. truncatus workers were observed to record whether they patrolled along a
C. scutellaris trail or not.
Results
Ants in cork trees
We found 14 species in the surveyed trees (Table 1). Some of the species nested in
trees themselves while others nested in the soil and climbed the trees to forage for
food. Argentine ant and arboreal ants (C. scutellaris, C. truncatus, C. lateralis, and
Lasius brunneus) were the most abundant species (found in N30 trees). Figure 2
shows a dendrogram with the presence of each species in every tree in 1992, to
determine if grouping or segregation occurs between them. The Argentine ant is
segregated from the other species, while the native species C. scutellaris, C.
lateralis, and C. truncatus form a group independent of L. brunneus. C. lateralis
and C. truncatus are not only associated with C. scutellaris because they were in
the same trees, but also because they followed C. scutellaris trophic trails (Table 2)
(although they were more frequently off the trails) (binomial test for C. lateralis:
z ¼ 4.56 p < 0.0001; binomial test for C. truncatus: z ¼ 2.71 p < 0.0001).
To analyze relationships between native arboreal species and Argentine ant,
aggressiveness tests were conducted (Table 3). Among native species, C. lateralis
and C. truncatus are considered submissive since they never attacked and always
retreated. C. scutellaris appeared to be the most aggressive species, although it
modified its behavior depending on the opponent species. Thus, on the rare occasions when it faced C. lateralis or C. truncatus, if an attack occurred, C. scutellaris
behaved aggressively and usually did not retreat. In encounters with L. brunneus, C.
scutellaris was sometimes attacked and occasionally demonstrated submissive
behavior, although in general it was more aggressive than L. brunneus. However,
when facing L. humile, it was less aggressive and it was more often attacked.
Relationships between species and tree characteristics
The following results refer to the relationships found between variables expounded
in methodology (presence of species, trunk circumference, distance to closest road
155
Table 1. Frequency or number of trees occupied by each
species of ant (N ¼ 182 cork trees).
Species
Frequency
L. humile (Mayr, 1868)
C. scutelaris (Olivier, 1792)
C. truncatus (Spinola, 1808)
C. lateralis (Olivier, 1792)
L. brunneus (Latreille, 1798)
Camponotus cruentatus (Latreille, 1802)
Formica subrufa Roger, 1859
Tapinoma nigerrima (Nylander, 1856)
Plagiolepis schmitzii Forel, 1895
Tetramorium ruginode Stitz, 1917
Leptothorax racovitzai Bondroit, 1918
Cardicondyla batesii Forel,1894
Aphaenogaster senilis Mayr, 1853
Leptothorax rabaudi Bondroit, 1918
115
40
34
33
30
17
16
11
6
6
5
3
2
1
Figure 2. Grouping of species in the cork trees, according to Euclidean distance.
Table 2. Frequency of C. lateralis and C. truncatus ants on C.
scutellaris trails.
On trails
Off trails
Total
C. lateralis (%)
C. truncatus (%)
29 (27.3%)
77 (72.7%)
106
42 (36.8%)
72 (63.2%)
114
Aggression
3
Submissiveness 1
Indifference
15
Encounters
37
0
24
9
12
0
23
54
0
33
11
59
8
0
100
16
71
0
13
9
3
48
32
6
5
23
18
1
56
0
35
1
C. scutellaris C. lateralis C. scutellaris C. truncatus C. scutellaris L. brunneus C. scutellaris L. humile L. brunneus C. lateralis
Table 3. Total for aggressive, submissive or indifferent behavior when confronting worker ants=pair of species 1–1 (N ¼ 10 tests).
156
157
Table 4. Spearman’s coefficient correlation (N ¼ 182). All of the
cases are significant with a probability p < 0.005.
Trunk circumference
Distance to palace
Distance to road
Native species
L. humile
0.6025
0.5769
0.3203
0.4136
0.3729
0.2279
and distance to Palace) and most abundant species (found in 30 or more trees:
Argentine ant and native arboreal species) (Table 1).
Species richness of native fauna in trees was positively correlated with trunk
circumference (Table 4 shows results of the tests). Thus, small trees contained only
one species (circumference < 91 cm, maximum one species), while larger trees
(>425 cm in circumference) always had all four native arboreal species (only if
they were not infested with Argentine ants). Although the values for the rest of the
variables are not high (especially regarding distance to nearest road), they are
positively correlated with native species richness.
Tree size and distance to nearest road and Palace are negatively correlated with
the presence of Argentine ant (Table 4). However, the values are low, especially
regarding distance to nearest road and Palace. As to tree size, Argentine ants
occupied both small and large cork trees and were found as the exclusive species in
both smallest and largest circumference trees (19 and 502 cm, respectively).
When analyzing in detail the presence of Argentine ant and native species
richness with regard to distance to Palace (Figure 3), Argentine ant segregated
from native species (Spearman’s correlation coefficient rs ¼ 0.7049, N ¼ 182,
p < 0.001). L. humile principally gathered in the area surrounding the Palace up to a
distance of 350 m, beyond which it disappeared. It then reappeared at a distance of
580 m from the Palace and disappeared at 920 m. Cork trees at this second point of
infestation are located in the area known as Lynx Cage which continues along the
Vera to the Pajareras area. This second point of infestation explains why the correlation value between distance to Palace and presence of L. humile is not as high as
expected. In 1981 Alberto Tinaut (personal communication) found that one cork
tree in the Pajareras area was infested by L. humile. However, after searching
another nine cork trees in the area (currently all infested with Argentine ants)
he only found native species (C. scutellaris, C. lateralis, C. truncatus and L.
brunneus).
Results from the year 2000
Twenty-three trees occupied by native species in 1992 (with a mean of 2.52 species,
standard deviation ¼ 1.44) were exclusively occupied by Argentine ants in
the year 2000. These cork trees were both small and large (circumference in centimeters: mean ¼ 214.1, standard deviation ¼ 139.9, minimum ¼ 35, maximum ¼
470) and both near and far from the Palace (distance to Palace in meters:
158
Figure 3. Presence of L. humile (axis Y1) and richness of native species (axis Y2), with respect to
distance to the Palace.
mean ¼ 550.4, standard deviation ¼ 278.3, minimum ¼ 70, maximum ¼ 1100).
Argentine ants had continued to invade the contaminated areas around the Palace
and the Lynx Cage and increased notably in cork trees located in another area quite
distant from the Palace (distance to Palace in meters: mean ¼ 591.8, standard
deviation ¼ 66.0). In 1992 only one cork tree in this last area was found with
Argentine ants and was also occupied by C. lateralis and C. truncatus, while in
2000 ten cork trees were found with high densities of Argentine ants and with no
other species. Any of the studied cork trees occupied by Argentine ants in 1992
were recovered by native species in the year 2000.
Discussion
We have found a community of arboreal native formicids in Doñana National
Park, whose structure has been largely influenced by interspecific competition. C.
scutellaris and L. brunneus have features that are characteristics of dominant
species (and the same for the exotic L. humile), such as aggressive behavior and
high densities of individuals (Bernard 1968; Hölldobler and Wilson 1990; Human
and Gordon 1996; Holway 1999) (Table 3). Thus native species are represented by
two dominant species (C. scutellaris and L. brunneus) that are segregated, except in
largest trees, and two subordinate species (C. lateralis and C. truncatus) that are
related to one of the dominant species (C. scutellaris) (Figure 2). All native species
are grouped in trees according to these relationships. Moreover, similar to what
occurs in island biogeography where island size is a determining factor for species
richness (McArthur and Wilson 1967; Simberloff 1978), plant size is usually
159
closely correlated with richness of arthropods (Southwood et al. 1982; Basset and
Kitching 1991; Majer and Delabie 1999). We found that ant species richness depended on tree size, hence, when a tree was large enough, as many as four different
native species were found together (Table 4).
Relationships between C. scutellaris, C. lateralis and C. truncatus have been
described by several authors since the 19th century. Although C. lateralis and C.
truncatus may be found without C. scutellaris, this last species attracts founding
females of both Camponotus, so it is quite usual to find them in the same trees. It has
been suggested that C. lateralis and C. truncatus, which are chromatic mimics of C.
scutellaris, use C. scutellaris trails to protect themselves from myrmecophages which
are repelled by this aggressive species (see revision in Baroni Urbani 1969). In this
study we show how both species of Camponotus were frequently associated with C.
scutellaris and often, although not always, used its trophic trails (Table 2). Batesian
mimicry has been observed in other invertebrates associated with ants, such as spiders and hemipters, and has also been found in other species of subordinate ants and
their dominant ants (Greenslade and Halliday 1983; Baroni Urbani 1969). It is still
unknown if C. scutellaris gains some advantage from this relationship or simply
tolerates it because C. lateralis and C. truncatus are not usually aggressive and their
colonies are small. In the agonistic encounters observed, C. scutellaris was initially
hostile to both Camponotus, which accepted this aggressive behavior in the characteristic manner of subordinate species (Table 3). Anyway, both species continued
patrolling together following the encounter. In Doñana we have even found worker
ants of both species attending the same group of aphids.
Thus, like many communities of ants, this community is greatly influenced by
interspecific competition, making it especially sensitive to any disturbance, such as
the introduction of exotic species (Suarez et al. 1998; Kaspari 2000). Native species
richness, for example, was proportionally related to tree size (Table 4). Nevertheless, L. humile occupied both small and large trees on its own. The fact is that
the variable that most affected native species richness was the presence of
Argentine ant (Figure 3). Similar results have been found in other areas invaded by
Argentine ants and several authors have therefore suggested that Argentine ant is
the principal agent of local extinction of native ants, more important than other
variables such as fire, habitat fragmentation or the presence of exotic vegetation
(Ward 1987; De Kock et al. 1992; Suarez et al. 1998).
As we found that native species were not affected by the proximity of humanized
areas (Table 4), Argentine ant had to displace these established species to occupy
their trees. This has happened in many other infested areas where Argentine ant has
displaced the majority of native species and other arthropods and has even had a
negative impact on certain populations of vertebrates (Newell 1908; Newell and
Barber 1913; Barber 1916; Chopard 1921; Fluker and Beardsley 1970; Erickson
1971; Lieberburg et al. 1975; Tremper 1976; Ward 1987; Porter and Savignano
1990; Cole et al. 1992; De Kock et al. 1992; Majer 1994; Holway 1995; Human and
Gordon 1997; Holway 1998; Suarez et al. 1998, 2000; Human and Gordon 1999;
Delibes 2001; Sanders et al. 2001; Suarez and Cole 2002; Fisher et al. 2002). The
displacement of native ant species is demonstrated by the fact that from 1992 to
160
2000 Argentine ant occupied 23 new cork trees that were previously inhabited by
native species, even dominant ones such as C. scutellaris and L. brunneus (Figure
3). This ability has been explained by their social structure, especially the establishment of large continuous unicolonies (Passera 1994; Human and Gordon 1997)
and its competitive abilities, in particular its aggressiveness, a feature which is
characteristic of dominant species (Table 3) (Hölldobler and Wilson 1990; Human
and Gordon 1996).
With regard to habitats that are sensitive to invasion, successful species such as
L. humile are usually generalist and therefore not restricted by habitat features
(Passera 1994). Anyway, they benefit from humanized areas because man is its
principal spreading agent (Woodworth 1910; Crowell 1968; Majer 1994; Passera
1994). In the present study, as expected, the species was abundant in the trees
around the Palace. But to what extent did it depend on habitats disturbed by man?
How did these areas affect native species? Argentine ant was described by Pisarski
and Kulesza (1982) as eusinantropic (a strict category of man-associated species);
however, in other parts of the world, L. humile has not only infested areas that have
been disturbed by man but also natural areas (Fellers and Fellers 1982; Ward 1987;
De Kock and Giliomee 1989; Cole et al. 1992; Suarez et al. 1998).
In Doñana, the presence of Argentine ant is negatively correlated with Palace
distance, as said before, although less than expected (Table 4) as the humanized
area around the Palace is the main source of infestation of L. humile in the Park.
This is due to the existence of a second point of infestation in a fenced area where a
wounded lynx (Lynx pardellus) lived for some years. The food for the lynx came
from the Palace and frequently contained Argentine ants, the most likely reason for
infestation. It is possible that L. humile first appeared in the Palace or any of the
adjacent buildings and began to disperse from there, not radially but along the Vera
line. This is believed to be due to three factors: (1) buildings that surround the
Palace are mostly located along this line; (2) The Lynx Cage, although further
away, is also located here; (3) the extensive pasture of the Vera with a relatively
large number of cork trees that facilitate the movement of ants from one tree to
another in contrast to the dense vegetation in the west of the Palace. It is possible
that the Argentine ant reached the Lynx Cage and became established there due to
the continual transportation of ants by man. But what happened when this transportation stopped? In 1994 the lynx was removed from the cage (information
provided by Rafael Laffitte), cutting off the flow of ants from the Palace. However,
the Argentine ant continued to spread along the area and colonized new cork trees
around the cage.
The surroundings of Doñana Palace and the Lynx Cage are the most infested
areas of the study site. But in 1992 an isolated cork tree located 590 m from the
Palace was also found to be occupied by Argentine ants. A pair of black kite
(Milvus migrans) also nested in the tree. These birds are not very strict in their
feeding habits and often feed in dumps that are sometimes infested with Argentine
ants. At that time Argentine ants shared the cork tree with C. lateralis and C.
truncatus, however, in 2000 only Argentine ants were found and 10 additional
nearby cork trees were completely infested by this species.
161
As to the proximity of roads, in other invaded areas, the entrance of Argentine
ants in natural areas depends on the presence of access roads used by humans,
especially asphalted roads. Thus, in a large area both the internal and the external
edges of the roads may be dangerous routes of infestation (De Kock and Giliomee
1989). In Doñana the distance to the nearest road did not seem to affect the
presence of the Argentine ant, nor the richness of native species (Table 4). Although
in the present study we did not find a relationship between roads and Argentine
ants, open areas could facilitate the expansion of the species by providing access
between infested and suitable habitats.
In conclusion, in this study we have found that Argentine ant was able to displace
every native arboreal species in Doñana National Park, even dominant species and
in natural areas. We have also pointed out that it can be dispersed not only by man
but also by animals that carry infested food. Therefore, because relationships are
continually established between natural and humanized areas by animals that feed
on human waste, such as kites or foxes, and by the numerous visitors, scientists and
rangers that patrol the National Park, we may ask ourselves if there is any area of
Doñana that is truly free of Argentine ant influence.
Acknowledgements
We thank Mariló Bosch, Antonio Priego and Xim Cerda for their collaboration in
the field work, David Williams for providing much of the reference material,
Alberto Tinaut for his remarks and for clarifying our doubts on taxonomy, and
Carmen Ortega and Alfonso Carpintero for their help. We are grateful to all of the
staff and colleagues at Doñana for the help and support they provided and to the
anonymous reviewers for valuable comments. This study was possible thanks to an
F.P.I grant awarded to S. Carpintero by the Andalusian Autonomous Community.
References
Adams E.S. 1994. Territory defense by the ant Azteca trigona: maintenance of an arboreal ant mosaic.
Oecologia 97: 202–208.
Andersen A.N. and Patel A.D. 1994. Meat ants as dominant members of Australian ant communities: an
experimental test of their influence on the foraging success and forager abundance of other species.
Oecologia 98: 15–24.
Barber E.R. 1916. The Argentine ant: distribution and control in the United States. Bulletin US
Department of Agriculture 377: 1–23.
Baroni Urbani C. 1969. Trail sharing between Camponotus and Crematogaster: some comments and
ideas. Process of VIth Congress of International Union for the Study of Social Insects, Bern 1: 11–17.
Basset Y. and Kitching R.L. 1991. Species number, species abundance and body length of arboreal
arthropods associated with an Australian rainforest tree. Ecological Entomology 16: 391–402.
Bernard F. 1968. Les fourmis (Hymenoptera Formicidae) d’Europe occidentale et septentrionale. Faune
de l’Europe et du Bassin Méditerranéen. Ed. Masson, Paris, France.
Chopard L. 1921. La fourmi d’Argentine Iridomyrmex humilis var. Arrogans Santschi dans le midi de la
France. Annales des Epiphyties 7: 237–266.
162
Cole F.R., Medeiros A.C., Loope L.L. and Zuehlke W.W. 1992. Effects of the Argentine ant on arthropod
fauna of Hawaiian high-elevation shrublands. Ecology 73: 1313–1322.
Crowell K.L. 1968. Rates of competitive exclusion by the Argentine ant in Bermuda. Ecology 49: 551–555.
De Kock A.E. and Giliomee J.H. 1989. A survey of the Argentine ant, Iridomyrmex humilis (Mayr),
(Hymenoptera: Formicidae) in South African fynbos. Journal of the Entomological Society of
Southern Africa 52: 157–164.
De Kock A.E., Giliomee J.H., Pringle J.L. and Majer J.D. 1992. The influence of fire, vegetation age and
Argentine ants (Iridomyrmex humilis) on ant communities in Swartboskloof. In: Van Wilgen B.W.,
Richardson D.M., Kruger F.J. and Van Hensbergen H.J. (eds) Fire in South African Fynbos: Ecosystem,
Community, and Species Response at Swartboskloof. Springer-Verlag, Berlin, Germany, pp. 203–215.
Delibes M. 2001. Vida. In: Temas de Hoy (ed) La naturaleza en peligro. S.A. (T.H.), Madrid, Spain.
Erickson J.M. 1971. The displacement of native ant species by the introduced Argentine ant Iridomyrmex
humilis Mayr. Psyche 78: 251–266.
Fellers J.H. and Fellers G.M. 1982. Status and distribution of ants in the Crater District of Haleakala
National Park. Pacific Science 36: 427–437.
Fernández J.A. (ed.) 1982. Guı́a de campo del Parque Nacional de Doñana. Ed. Omega, Barcelona, Spain.
Fisher R.N., Suarez A.V. and Case T.J. 2002. Spatial patterns in the abundance of the Coastal Horned
Lizard. Conservation Biology 16: 205–215.
Fluker S.S. and Beardsley J.W. 1970. Sympatric associations of three ants: Iridomyrmex humilis,
Pheidole megacephala and Anoplolepis longipes in Hawaii. Annals Entomological Society of America
63: 1290–1296.
Greenslade P.J.M. and Halliday R.B. 1983. Colony dispersion and relationships of Meat ants
Iridomyrmex purpureus and allies in an arid locality in South Australia. Insectes Sociaux 30: 82–99.
Hertzer L. 1930. Response of the Argentine ant (Iridomyrmex humilis Mayr) to external conditions.
Annals Entomological Society of America 23: 597–600.
Hölldobler B. and Wilson E.O. 1990. The Ants. Springer-Verlag, Berlin, Germany.
Holway D.A. 1995. Distribution of the Argentine ant (Linepithema humile) in Northern California.
Conservation Biology 9: 1634–1637.
Holway D.A. 1998. Effects of Argentine ant invasion on ground-dwelling arthropods in Northern
California riparian woodlands. Oecologia 116: 252– 258.
Holway D.A. 1999. Competitive mechanisms underlying the displacement of native ants by the invasive
argentine ant. Ecology 80: 238–251.
Human K.G. and Gordon D.M. 1996. Exploitation and interference competition between the invasive
Argentine ant, Linepithema humile, and native ant species. Oecologia 105: 405–412.
Human K.G. and Gordon D.H. 1997. Effects of Argentine ants on invertebrate biodiversity in Northern
California. Conservation Biology 11: 1242–1248.
Human K.G. and Gordon D.M. 1999. Behavioral interactions of the invasive Argentine ant with native
ant species. Insectes Sociaux 46: 159–163.
Jackson D. 1984. Competition in the tropics: Ants on trees. Antenna 8: 19–22.
Kaspari M. 2000. Do imported fire ants impact canopy arthopods? Evidence from simple arboreal pitfall
traps. The Southwestern Naturalist 45: 118–122.
Lieberburg I., Kranz P.M. and Seip A. 1975. Bermudian ants revisited: the status and interaction of
Pheidole megacephala and Iridomyrmex humilis. Ecology 56: 473–478.
Majer J.D. 1994. Spread of Argentine ants (Linepithema humile), with special reference to western
Australia. In: Williams D.F. (ed) Exotic Ants. Biology, Impact, and Control of Introduced Species.
Westview Press, Oxford, UK, pp. 161–173.
Majer J.D. and Delabie J.H.C. 1999. Impact of tree isolation on arboreal and ground ant communities in
cleared pasture in the Atlantic rain forest region of Bahia, Brazil. Insectes Sociaux 46: 281–290.
McArthur R.H. and Wilson E.O. 1967. The Theory of Island Biogeography. Princeton University Press,
Princeton, New Jersey.
Montes C., Borja F., Bravo M.A. and Moreira J.M. (coordinadores) 1998. Reconocimiento Biofı́sico de
Espacios Naturales Protegidos. Doñana: Una aproximación Ecosistémica. Junta de Andalucı́a,
Consejerı́a de Medio Ambiente, Seville, Spain.
163
Newell W. 1908. Notes on the habits of the Argentine or ‘New Orleans’ ant, Iridomyrmex humilis Mayr.
Journal of Economic Entomology 1: 21–84.
Newell W. and Barber T.C. 1913. The Argentine ant. Bulletin Bureau of Entomology, US Department of
Agriculture 122: 1–98.
Passera L. 1994. Characteristics of tramp species. In: Williams D.F. (ed) Exotic ants. Biology, Impact,
and Control of Introduced Species. Westview Press, Oxford, UK, pp. 23–43.
Perfecto I. 1994. Foraging behavior as a determinant of asymmetric competitive interaction between two
ant species in a tropical agroecosystem. Oecologia 98: 184–192.
Pisarski B. and Kulesza M. 1982. Characteristics of animal species colonizing urban habitats. Memorabilia Zoologica 37: 71–77.
Porter S.D. and Savignano D.A. 1990. Invasion of polygene ants decimates native ants and disrupts
arthropod community. Ecology 71: 2095–2106.
Punttila P., Haila Y., Niemelä J. and Pajunen T. 1994. Ant communities in fragments of old-growth taiga
and managed surroundings. Annales Zoologici Fennici 31: 131–144.
Sanders N.J., Barton K.E. and Gordon D.M. 2001. Long-term dynamics of the distribution of the invasive
Argentine ant, Linepithema humile, and native ant taxa in northern California. Oecologia 127:
123–130.
Savolainen R. and Vepsäläinen K. 1988. A competition hierarchy among boreal ants: impact on resource
partitioning and community structure. Oikos 51: 135–155.
Savolainen R. and Vepsäläinen K. 1989. Niche differentiation of ant species within territories of the
wood ant Formica polyctena. Oikos 56: 3–16.
Simberloff D. 1978. Using island biogeographic distribution to determine if colonization is stochastic.
American Naturalist 112: 713–726.
Southwood T.R.E., Moran V.C. and Kennedy C.E.J. 1982. The richness, abundance and biomass of the
arthropod communities on trees. Journal of Animal Ecology 51: 635–649.
Suarez A.V. and Case T.J. 2002. Bottom-up effects on persistence of a specialist predator: ant invasions
and horned lizards. Ecological Applications 12: 291–298.
Suarez A.V., Bolger D.T. and Case T.J. 1998. Effects of fragmentation and invasion on native ant
communities in coastal Southern California. Ecology 79: 2041–2056.
Suarez A.V., Richmond J.Q. and Case T.J. 2000. Prey selection in horned lizards following the invasion
of Argentine ants in Southern California. Ecological Applications 10: 711–725.
Tremper B.S. 1976. Distribution of the Argentine ant, Iridomyrmex humilis Mayr, in relation to certain
native ants of California, physiological, and behavioral aspects. Ph.D. Thesis, California University,
Berkeley, California.
Ward P.S. 1987. Distribution of the introduced Argentine ant (Iridomyrmex humilis) in natural habitats of
the lower Sacramento Valley and its effects on the indigenous ant fauna. Hilgardia 55: 1–17.
Woodworth C.W. 1910. The control of the Argentine ant. Bulletin Agricultural Experiment Station,
College of Agriculture, Berkeley, University of California 207: 51–82.
Young A.M. 1983. Patterns of distribution and abundance of ants (Hymenoptera: Formicidade) in three
Costa Rican cocoa farm localities. Sociobiology 8: 51–76.