Download Mutualism between Thisbe irenea butterflies and

Biological Journal of !he Linnean Sociep ( 199I ) , 43: 179- 195
Mutualism between Thisbe irenea butterflies
and ants, and the role of ant ecology in the
evolution of larval-ant associations
P. J. DEVRIES
Department of <oology, Uniuersily of Texas, Austin, Texas 787812 and Smithsonian
Tropical Research Inst., Box 2072, Balboa, Panama
A facultative mutualism between the riodinid butterfly Thisbe ircnca and the ponerine ant Ectafomma
ruidurn is described from Panama. Ants protect larvae against attacks of predatory wasps, but not
against tachinid parasitoids. Several potential sources of ecological variation affecting the larval
survival of Thisbe irenea are noted. A preliminary means of testing the ability of larvae to appease
ants is described that may be applied to all butterfly-ant systems. Observations and literature
records indicate that ant taxa which tend butterfly larvae are the same taxa that tend extrafloral
nectaries and Homoptera. A general hypothesis for the evolution of myrmecophily among
butterflies suggests that ant taxa which utilize secretions in their diet are major selective agents for
the evolution of the larval ant-organs, and hence, ant-larval mutualisms. This idea is extended to
suggest how appeasement of predaceous ant taxa through the use of larval ant-organs can influence
an ant-larval relationship, eventually leading to mutualism.
KEY WORDS:-Butterflies - rnyrmecophily - Riodinidae - Lycaenidae - mutualisms - Vespidae predation - ants - extrafloral nectaries - Homoptera - evolution - larval ant-organs.
CONTENTS
Introduction . . . . .
Natural history of Thisbe irenea .
Materials and methods.
. .
Results
. . . . . .
Discussion . . . . . .
Acknowledgements
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References
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INTRODUCTION
The facultative habit of insects associating with ants (termed myrmecophily) is
well established among the insect orders Homoptera and Lepidoptera (Way,
1963; Cottrell, 1984). Although facultative myrmecophiles can complete their
life cycles without ants, benefits can be gained from associating with ants,
including: protection against predators and parasitoids; faster growth rates;
higher reproductive success; and safer aestivation sites (Bartlett, 1961; Banks &
Nixon, 1958; Cottrell, 1984; DeVries, 1987; Pierce el al., 1987; Thomas et al.,
1989; Wheeler, 1910; Way, 1963; Wilson, 1971). All myrmecophilous insects are
distinguished from their non-myrmecophilous relatives by morphological and
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0 1991 The Linnean Society of London
180
P.J. DEVRIES
behavioural adaptations for living among ants, one common adaptation being
the possession of specialized secretory organs which either produce food that is
imbibed by the ants or chemicals that modify ant behaviour (see Wheeler, 1910;
Way, 1963; Wilson, 1971; Maschwitz, Wurst & Schurian, 1975; Cottrell, 1984;
DeVries, 1987, 1988, 1990, 1991; Fiedler & Maschwitz, 1987, 1988, and
references therein).
Among butterflies only larvae of the monophyletic lycaenoids (the Lycaenidae
plus Riodinidae) are known to possess specialized secretory organs for associating
with ants. The widespread taxonomic occurrence of these organs on larval
lycaenids (see Downey, 1961; Cottrell, 1984; DeVries, Harvey & Kitching,
1986), suggest that myrmecophily was an integral part of the evolutionary
history of the lycaenoids (Hinton, 1951; Vane-Wright, 1978; Pierce et al., 1987),
and probably played a n important role in promoting wide larval hostplant
breadth and high species diversity (Pierce, 1984, 1987; Pierce & Elgar, 1985).
Although riodinids and the lycaenids share a close relationship (Ehrlich, 1958;
Kristensen, 1976; Harvey, 1987), it is likely that myrmecophily evolved
independently in the two groups (DeVries, 1990, 1991).
All riodinid and lycaenid larvae (myrmecophilous and non-myrmecophilous)
have epidermal pits called pore cupolas that are considered important indicators
of ancestral myrmecophily in lycaenoids (see Downey, 1961; Malicky, 1970;
Cottrell, 1984; Pierce, 1987). However, the possession of pore cupolas by larvae
of the completely non-myrmecophilous family Hesperiidae (Franzl, Locke &
Huie, 1984) suggests that they may be inappropriate characters for assessing the
evolution of myrmecophily in butterflies (DeVries, 1991). Nonetheless, only
myrmecophilous larvae of many lycaenids and riodinids possess derived organs
(hereafter termed ant-organs) that have clearly evolved in response to selection
by ants. These specialized ant-organs provide ant food and chemicals that
modify ant behaviour (see Ross, 1966; Malicky, 1970; Maschwitz el al., 1975;
Henning, 1983; Pierce, 1984; Fiedler & Maschwitz, 1988, 1989; DeVries, 1988;
DeVries & Baker, 1989), as well as sounds that function to attract ants (DeVries,
1988, 1990b).
Two ideas have been advanced to explain the evolution of specialized antorgans and the nature of myrmecophily in butterflies. The ‘mutualism’
hypothesis (Thomann, 1901) holds that ants protect larvae from predators and
parasitoids in exchange for secretions provided by the larval ant-organs. The
‘appeasement’ hypothesis (Lenz, 1917) maintains that, because ants are
generally marauding predators and abundant in many habitats (e.g. Smiley,
1985; Koptur, 1984; Jones, 1987), larvae offer appeasement rewards to them via
the ant-organs to avoid being killed.
Support for the mutualism hypothesis comes from experimental studies on
several lycaenid species (Atsatt, 1981a; Pierce & Mead, 1981; Pierce et al., 1987;
Fiedler & Maschwitz, 1988; Thomas et al., 1989) and two riodinids (Ross, 1966;
DeVries, 1987). These studies showed that ants protect larvae against enemies.
In contrast, the observations of Malicky (1969, 1970) on a large sample of
European lycaenid taxa support the appeasement hypothesis. He found that
lycaenid larvae have a thick cuticle (as armour against ant attacks), that
parasitoids were undeterred by ants, and argued that since many ants are
predators on small arthropods, the secretions produced by larval ant-organs are
used as ‘bribery’ to avoid being attacked or killed by ants.
THISBE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS
181
Various authors have discussed theoretically the contributions of both
mutualism and appeasement to the evolution of larval ant-organs and butterfly
myrmecophily (Malicky, 1969, 1970; Pierce & Mead, 1981; Pierce, 1987; Fiedler
& Maschwitz, 1988), and Cottrell (1984) pointed out that the two ideas may be
difficult to separate. However, no published studies have attempted to evaluate
both of them experimentally.
In general, studies on larval-ant associations have not considered the feeding
biology of ants. I suggest that important ecological relationships common to
facultative myrmecophiles have been overlooked by previous studies considering
the evolution of ant-organs and butterfly myrmecophily. Although there is
overlap among taxa with respect to food items taken, the foraging biology of ants
can be broken down into four general categories: (1) taxa that are primarily
predators; (2) taxa that are herbivores and seed eaters; (3) taxa that are
scavengers; and (4) taxa that primarily harvest secretions (Wheeler, 1910;
Wilson, 1971 ; Carroll & Janzen, 1973). The specialized feeding biology within
the Formicidae implies that classifying all ant species as mutualists or predators
of butterfly larvae is too simplistic. Specializations in ant feeding biology suggests
that the two hypotheses for explaining the evolution of ant-organs must be tested
in different ways. By using simple pair-wise ant exclusion experiments one can
test directly whether a particular larval-ant association is mutualistic: either
there is a measurable benefit or there is not (e.g. Pierce & Mead, 1981; Pierce
et al., 1987). Appeasement of ants by larvae, however, must be tested by
measuring the outcome of the interactions between larvae and the different ant
species composing an ant community, a test for which there are no available
data.
The purpose of this paper is to illustrate that broad patterns of butterfly-ant
associations and the evolution of ant-organs may be better understood by
examining them from the point of view of the ants, rather than of the butterflies
(as has been traditionally done). This argument is developed in four stages. First,
the facultative association between the riodinid butterfly Thisbe irenea and its
attending ants is examined experimentally. Secondly, the interactions between
T. irenea larvae and a subset of a local ant fauna are used to develop the idea
that not all ants tend or kill larvae, and suggest that three outcomes may arise
from ant-larval encounters, which are determined by the feeding biology of the
ants. Thirdly, the general pattern of what types of ants tend T. irenea larvae is
shown to occur in other local but terfly-ant associations. Finally, from
observations and literature records it is argued that out of the total recognized
ant diversity, only those small number of any genera that harvest secretions have
selected for specialized ant-organs, and thereby promote the evolution of
butterfly-ant mutualisms.
Natural history of Thisbe irenea
The study organism, Thisbe irenea (Stoll, 1780), is a widespread Neotropical
riodinid butterfly that ranges from Mexico through Central America to
Colombia, Venezuela and Ecuador. The present study was conducted in
Panama on Barro Colorado Island, and surrounding mainland habitats (see
Croat, 1978; Leigh, Rand & Windsor, 1982 for description of the area) from
September 1985 to August 1986, and intermittently from October 1987 to
182
P. J. DEVRIES
August 1988. At the study site 1.irenea lavae are monophagous on sapling plants
of Croton billbergianus (Euphorbiaceae), a secondary forest tree that is common in
lightgaps and along forest trails (Robbins & Aiello, 1982; personal observations).
Each hostplant leaf bears a pair of extrafloral nectaries that produce secretions
attractive to ants and to 1.irenea larvae.
The primary ant species tending both larvae of T. irenea and C. billbergianus
nectaries was Ectatomma ruidum (Ponerinae),one of the most abundant ant species
at the study site (D. Feener & E. Schupp, unpublished). However, depending
on the local distributions of ant colonies, some larvae and plants were tended by
E. tuberculatum, or species in the genera Camponotus, Wasmannia, Pheidole or
Tapinoma. O n many occasions wasps, beetles, flies and other insects were
observed foraging on the leaves and/or extrafloral nectaries of C. billbergianus
(and other plant' species) and being repelled by ants (personal observations),
suggesting a facultative plant-ant mutualism similar to those found in many
other plants (see review in Beattie, 1985).
Of the five total larval instars of 1.irenea, only the third to fifth bear three
distinct sets of ant-organs-vibratory
papillae, tentacle nectary organs and
anterior tentacle organs-that are used to attract and maintain ant associations
(DeVries, 1988). Larvae remain in physical contact with a n individual hostplant
throughout their lives, and duration of larval stages ranges from two days as first
instars to as long as eight days in the fifth instar. All larval instars gain a
measurable growth benefit from drinking the extrafloral nectar produced by the
hostplant nectaries, in addition to consuming leaf tissue (DeVries & Baker,
1989). Since T. irenea larvae can be raised to adulthood without ants, their
association with ants is facultative.
From rearing numerous field-collected larvae, I established that the major
parasitoids attacking 1.irenea at Barro Colorado Island and adjacent areas were
three or more undetermined species of tachinid flies, all of which emerge from
fifth instar larvae. Observations showed repeatedly that several species of vespid
wasps commonly search C . billbergianus foliage and kill T. irenea larvae when they
are found.
MATERIALS AND METHODS
To test whether the presence of ants influence larval abundance on hostplants,
102 C. billbergianus saplings (all approximately 1.5-2.0 m in height) were marked
in three separate populations. All larvae (eggs could not be found reliably) and
ants were removed from each plant, and the stem of each lant was then ringed
12 cm from the base with a viscous barrier of TanglefootTR to exclude crawling
arthropods (i.e. ants, beetles, spiders, Hemiptera). From the ground upwards all
surrounding vegetation that might serve as a bridge to insects was cut back at
least 12 cm from each plant. Half of each population received a wooden stick
bridge attached to the main stem above the Tanglefoot barrier and reaching to
the ground, allowing ants to move on and off the plants. Experimental plants did
not receive the bridge and therefore ants were denied access to these plants.
Larvae subsequently found on plants were assumed to originate from eggs
deposited by T, irenea females. All plants were censused once per week and the
numbers of first through fourth instar larvae found on each plant were recorded.
During each census the Tanglefoot barrier was inspected and all potential
THISBE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS
183
vegetation bridges were pruned back. In each population the abundance of
larval instars on plants with and without ants, treatment effects and the attrition
of larval instars were compared using replicated goodness-of-fit tests (Sokal &
Rohlf, 1981). Congruence of the three populations was compared with a 3-way
contingency test (Bishop, Fienberg & Holland, 1975).
To test if ant association reduced parasitoid attacks in T. irenea, all late fourth
instar larvae were removed from plants in the three experimental populations
over the course of 26, 31 and 42 weeks, depending on the population. These
larvae were placed in individual petri dishes in an ambient temperature
laboratory, and reared to adulthood or until parasitoids emerged. The
differences in parasitoid and adult emergence between larvae originating from
experimental and control plants were compared using a contingency test (Sokal
& Rohlf, 1981).
To test if the presence of ants reduced attacks on T. irenea larvae by predatory
wasps the following experiments were performed. Two potted C. billbergianus
saplings of approximately the same size, condition and number of leaves were
ringed 12 cm from their bases with Tanglefoot, and placed in an area patrolled
heavily by foraging vespine wasps ( = the Clearing Site). One plant received a
stick bridge attached above the Tanglefoot barrier and leading to the ground
near an E. ruidum colony, allowing the ants access to the plant; the other plant
did not. Two additional pairs of potted plants (treated in the same manner) were
placed in two areas within 30 m of the Clearing site but that appeared to be less
patrolled heavily by wasps ( = the Edge Sites).
Paired larvae of the same instar were placed simultaneously on each of the
plants and then censused at various intervals. In some cases a stationary observer
recorded all interactions between larvae, ants and wasps. A total of 33 pairs of
larvae were tested at the Clearing site and 19 pairs were tested at the Edge sites.
In all potted plant experiments, those larvae not found after a careful inspection
of the plants between censuses were assumed to have been killed. In many
instances this was confirmed by direct observation of wasps killing larvae, or by
haemolymph stains on the plant (a characteristic effect of wasps killing larvae).
For the Clearing site and pooled Edge Sites, the differences in time larvae
remained on the plant pairs were compared against a binomial probability using
a sign test (Siegel, 1956). Site effect was examined by comparing the pooled
Edge sites to the Clearing site using a contingency test (Sokal & Rohlf, 1981).
In an attempt to assess the ability of larvae to appease ants, 26 a n t species (see
Table 4 for taxa) that occur commonly on Barro Colorado Island were allowed
to encounter T . irenea larvae passively and the outcomes noted. Single larvae
kept in containers without ants for at least 1 day (to avoid contamination by ant
odours) were placed on potted plants and carried to areas where different ant
species occurred. A bridge was then placed from the potted plant to where
worker ants of the test species would encounter it, include the plant into their
foraging territory, and eventually find the larva. Over 70 larvae were tested, and
those used for more than one trial were always kept isolated from ants at least
1 day before retesting. Tests were done intermittently between 900 and 1600
hours except Camponotus sp. 1 which was active nocturnally. The number of
colonies used varied with the species of ant: 1 colony Atta, Paraponera clavata,
Pheidole, Crematogaster, Labidus; 2 colonies Aphaenogaster, Ccmponotus, Eciton
hamatum; 3 colonies Wasmannia, Tapinoma; 4 colonies Monacis, Azteca, Zacryptocerus;
I84
P. J. DEVRIES
> 5 colonies Pseudomyrmex, Ectatomma tuberculatum; and > 12 colonies Ectatomma
ruidum. Each colony was tested with at least two larvae. Variation in colony
responses to larvae was not investigated.
T o illustrate a pattern that is apparent on a local scale, the ant taxa found
associating with T. irenea larvae were compared with ant taxa found associating
with other species of butterfly larvae, Homoptera and plant EFNs. This pattern
was then developed further by compiling literature records from other
geographic areas in which ant taxa that visit butterfly larvae and secretion
producing organisms were reported.
RESULTS
Larval abundance
Table 1 presents the summed totals of weekly larval censuses. Because weekly
censuses are summed, a single larva could have been recorded on subsequent
occasions, but never twice as the same instar (the longest duration of any instar
censused ranged 5-6 days). Lack of larval movement and census interval
ensured that each larva was counted only once during each instar. In all three
populations most plants accrued larvae, some individual plants (both
experimental and controls) accrued higher cumulative larval densities than
others, while some individuals were never occupied by larvae during the censuses
(10% population 1, 30% population 2, and 12% population 3). However, the
most parsimonious 3-way contingency model (larval instar, treatment,
population: G = 18.82, d.f. = 14, 0.1 < P < 0.5) showed a significant
relationship between larvae and treatment (G = 30.53, d.f. = 3, P < 0.001), that
is independent of population. Significantly more larvae of all instars were found
on ant occupied plants than on plants with ants excluded, and all populations
showed a decline in proportions of later instars on plants without ants (Table 1).
Four events might account for the higher numbers of larvae on plants with
ants and the declining number of larvae on those plants without ants: (1) female
1.irenea may oviposit more frequently in the presence of ants, generating a
pattern of more larvae on ant-tended plants; (2) larvae may crawl or drop off
plants without ants; (3) attack by tachinid parasitoids may cause larvae to drop
or crawl off the plant; (4) flying predators may remove larvae from plants
without ant associates, especially larger larvae.
Ant-mediated oviposition
Ant-mediated oviposition as shown for some lycaenid species (Atsatt, 1981b;
Pierce & Elgar, 1985) is unlikely for 1.irenea. Within the experimental
populations, individual females of T. irenea laid single eggs quickly and
indiscriminately on leaves, stems, and dead branches of C. billbergianus plants,
often alternating between plants with and those without ants. Females also laid
on detritus accumulated on plants, or on non-host plants near individual
C. billbergianus (personal observations). Therefore, the disparity of larvae
between plants with and without ants is most likely caused by egg and/or larval
loss rates, and not adult choice of oviposition sites. However, the number of
plants in all three experimental populations ( 10-3070) that did not accrue
larvae suggests a potential effect of female oviposition undetected by this study.
THISBE IRENEA AND T H E EVOLUTION OF BUTTERFLY-ANT MUTUALISMS
185
TABLE
I . Attrition of older instars and larval
abundance on plants with and without ants. All
plants were censused once per week. Population
1 was censused for 31 weeks, population 2 for
26 weeks and population 3 for 42 weeks
Instar
With ants
((yo)
Without ants (T,)
Population I (N=30)
I st
2nd
3rd
4th
Total
54
80
41
22
197
(27)
(41)
(21)
(11)
27
29
15
1
72
(29)
(34)
(23)
(14)
25 (25)
12 (12)
6 (14)
1 (2)
44
(24)
(40)
(26)
(10)
36
36
15
4
91
(38)
(40)
(21)
(1)
Population 2 ( N = 30)
1st
2nd
3rd
4th
Total
56
65
43
27
191
Population 3 ( N = 42)
1st
2nd
3rd
4th
Total
58
99
64
24
245
Larval attrition
Larval abundance
d.f.
c
P
3
15
18
170.72452
42.94902
213.67354
<0.001
<0.001
<0.001
Total
Population
d.f.
G
P
1 Ants
I No ants
3
3
3
3
3
3
37.07103
38.30632
18.144I3
3 1.06788
49.39645
39.68773
213.67354
<0.001
'rest
Pooled
Hetero.
Total
2 Ants
2 No ants
3 Ants
3 No ants
Total
(40)
(40)
(16)
(4)
18
<0.001
<0.001
<0.001
<0.001
<0.001
d.f.
G
P
Pooled
1
2
3
226.41322
6.40771
232.82093
<o.oo 1
Hetero.
d.f.
G
P
1
I
2
3
Total
1
1
60.38065
99.15112
73.28916
232.82093
<0.001
<0.001
<0.001
Test
Population
3
<0.05
<0.001
Larvae dropping of plants
The larvae of at least one lycaenid species are known to drop off plants when
they are not tended by ants. Although tarpaulins were not placed under plants
(cf. Pierce & Easteal, 1986), it is unlikely that larvae dropping off the plants
accounted for the disparity in abundance between experimental and control
plants. Even when not tended by ants, T. irenea larvae do not drop off their
hostplant when attacked by predators in the field or laboratory, nor can they be
induced to drop off the plant by prodding them (they grip the substrate tighter).
P.J. DEVRIES
I86
TABLE2. Comparison of the number of butterflies and
tachinid parasitoids arising from larvae reared on
experimental plants with ants and without ants over the
course of the study
With ants
Butterflies
Tac hinids
Total
50
23
73
Origin of larvae
Without ants
5
1
6
Total
55
24
79
d.E= I , G=0.641, P=0.423.
Furthermore, larvae grown on potted plants in a laboratory never crawled off
plants ringed with Tanglefoot ( N > 400, personal observations).
Parasihm
Fourth instars reared from the experimental populations of C. billbergianus
showed that E. ruidum did not protect T. irenea larvae against the attack of
tachinid flies. Although larvae (both parasitized and unparasitized) were more
abundant on plants with ants, there was no significant difference between rates
of parasitoid attack on larvae from plants with or without ants (Table 2). Some
tachinids that oviposited directly on T. irenea larvae were ignored by ants, and
one species of tachinid circumvented ants by depositing minute eggs on leaf
surfaces that were then apparently ingested by larvae (personal observations).
This suggests that parasitoid attack did not account for differences in larval
abundance between treatments in the experimental populations. However,
removing fifth instars may have biased the results if some tachinids only attack
this stage.
Predators
Potted C. billbergianus plants at experimental sites were patrolled by
individuals of at least seven species of vespid wasps (Polistes canadensis, Polybia
rejecta, Polybia aff. similliana, Stelopolybia areata, Parachartergus fraternus and
Brachygastru sp.), all which were observed investigating the stems and leaves
carefully, and killing and removing 7.irenea larvae whenever possible. When a
wasp encountered a larva without attending ants it immediately stung the larva,
eviscerated it, cut the carcass into pieces, and carried it off, leaving the gut
contents behind. Small wasp species (e.g. Polybia rejecta) would make several
return trips to completely remove the larval carcass, whereas a large species (e.g.
Polistes canadensis) could, after manipulation, carry away the entire carcass. No
other flying insect predators were observed killing T.irenea larvae. Therefore, it
seems most likely that the differences in abundance between experimental and
control plant populations was due to the effects of predatory wasps.
Protection of larvae by ants
In both Clearing and Edges sites, larvae tended by ants stayed on plants
significantly longer than did larvae without attending ants (Table 3). All direct
THISEE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS
187
TABLE
3. Ant protection from wasp predation on paired larvae on potted plants at two separate
sites. ‘The occupancy times of larvae attended by ants were longer than larvae where ants were
excluded
Larval occupancy longer
Clearing sites ( N = 33 pairs)
Edge sites ( N = 19 pairs)
SitK KffKCt
With ants
Without ants
Equal
P (I-tailed)
25
I1
0
1
8
7
<0.001
<0.005
d.f.=2, x2=2.96, P = 0 . 2 3
observations of wasp-larval encounters indicated that once a foraging wasp
found a larva unprotected by ants, the larva had no chance of survival. In
contrast, wasps of all body sizes encountering larvae with even a single ant in
attendance were consistently repelled by the attending ants.
Why older instars declined on plants through time is unknown, but it is likely
that larger larvae are more readily found by visually hunting wasps. Two
parallel observations argue that predation rates increase with larval instar: larval
ant-organs which are important to ant association become functional at third
instar, and late fourth and all fifth instar T. irenea feed almost entirely at night
(DeVries, 1988). The discovery rates of different instar T. irenea by wasps is
currently under investigation.
Ant responses to larvae
Table 4 shows the rsponses of 26 ant taxa tested. Although the responses of
some ants were equivocal (e.g. Camponotus sp.-2, Monacis bispinosa), three general
outcomes were apparent from encounters between different ant species and
T. irenea larvae:
( 1 ) An ant species may ignore larvae (actively or passively), being neither
mutualist not predator. Fourteen of the 26 ant taxa showed this response.
(2) An ant species may attack larvae, injuring or killing them, thereby being a
predator. Four ant taxa responded in this manner.
(3) An ant species may investigate larvae and accept rewards from the antorgans. If the ant species continues to accept these rewards and attends the
larvae, it thereby becomes a mutualist potentially capable of defending its
resources against intruders. Six ant taxa responded in this way.
Ants that ignored larvae were either specialist predators (i.e. Eciton) or general
scavengers from all subfamilies, those that killed larvae were carnivores in the
Ponerinae or secretion foragers in the Dolichoderinae, and those ants that tended
larvae were all secretion foragers from the ponerine, formicine, myrmicine and
dolichoderine subfamilies.
A pattern became evident when 31 common Barro Colorado Island ant taxa
were considered with respect to whether or not they were observed tending any
species of riodinid or lycaenid butterfly larvae, extrafloral nectaries (EFNs) or
homopterans under natural conditions. Ants that tended butterfly larvae were
the same taxa that tended EFNs and homopterans (Table 4), and not
surprisingly, all are well known to forage on secretions (D. Feener and
E. Schupp, personal communication; personal observations). In contrast, it
P. J. DEVRIES
188
TABLE
4. Thirty-one common Barro Colorado Island ant species and their reactions to 1.ireneu
(=Ti) larvae, and their observed responses to other species of riodinid and lycaenid larvae,
+
extrafloral nectaries or homopterans. Symbols:
= positive response; - =negative response;
=response variable; + - =infrequently tended; ?=unknown; * =ant taxa tested with 1.ireneu
larvae
Ant taxon
Ponerinae
Ectatomma ruidum*
E. tuberculatum*
Pachycondyla harpax
P . uilosa*
P. sp.
Paraponera clauata*
Odontomachus bauri*
Forrnicinae
Camponotus sericeiuentris*
c . sp. - I *
c . sp. -2*
Parathrechina sp.*
Myrrnicinae
Pheidole sp. - I *
Monomorium sp.
Solenopsis sp.
Crematogaster sp. - I *
c. sp. -2*
Wasmannia auropunctata*
Cephalotes atratus*
Zacryptocerus sp. - 1*
.5. sp. -2'
Aphaenogaster araneoides*
Atta cephalotes.
Tend Ti
Kill Ti
Ignore Ti
-
?
+
?
-
+
+-
Other
larvae
EFNs and
Hornoptera
+
+-
-+
+
+
+
+-
-
+
f
?
?
+
++
+
+
+
+
+
+
+
+
+
+++- -
Dolichoderinae
Monacis bispinosa*
Azteca sp. - 1 *
A . SP. -2*
Tapinoma sp.*
-
-
+
+
+
Pseudornyrrnecinae
Pseudomymex sp. - I *
P . sp. -2*
+
+
-
+
-
-
-
Ecitoninae
Eciton hamalum*
E . birchelli
Labidus praedator:
f
?
t
-
would have been surprising indeed to find leaf-cutting ants (Atta) or army ants
(Labidus, Eciton) tending any secretion producing organisms.
Although not accounting for possible variation ant colonies, or potentially
specific larval-ant associations (see below), two conclusions are suggested by
these preliminary observations. One is that on Barro Colorado Island there are
several possible outcomes in the encounters between ants and 7.irenea larvae
(ant taxa ignore larvae, kill larvae or tend larvae). Secondly, of the ants that
exhibited tending behaviour toward butterfly larvae, both riodinids and
lycaenids, all were species that typically harvest the secretions of both insects and
plants.
THISBE IRENEA AND THE EVOLUTION O F BUTTERFLY-ANT MUTUALISMS
189
TABLE
5. Out of 266 ant genera recognized by Brown (1973), only
these 24 are reported consistently to tend facultatively extrafloral
nectaries, Homoptera and butterfly larvae, or combinations
thereof. See text for orgins of the records. =Interactions
+
Taxon
Ponerinae
Ectatomma
M yrmicinae
Myrmica
Pheidole
Tetramorium
Monomorium
Solenopsis
Cremalogaster
Wasmannia
Dolichoderinae
Dolichoderus
Monacis
Iridomyrmex
Azteca
Tapinoma
Formicinae
Oecophylla
Brachymyrmex
Anoplolepis
Acantholepis
Prenolepis
Paratrechina
Lasius
Myrmecocystus
Formica
Camponolus
Polyrhachis
Number of interactions
EFNs
Hornoptera
Larvae
+
+
+
+
+
+
+
+
?
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
?
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
?
+
+
+
22
23
23
+
+
+
+
+
+
+
+
?
Ecological traits of tending ants
A robust relationship emerges when records of ants tending EFNs, Homoptera
and butterfly larvae from temperate and tropical sites throughout the world are
summarized and compared. Of the 266 ant genera recognized by Brown (1973),
only 24 are consistently reported as foraging on secretions of both insects and
plants (these are listed in Table 5). Virtually all ant genera reported to associate
regularly with lycaenid and riodinid larvae (see records and references in
Lamborn, 1915; Farquarson, 1922; Jackson, 1937; Hinton, 1951; Clark &
Dickson, 1971; Atsatt, 1981a; Cottrell, 1984; Pierce & Elgar, 1985; Maschwitz
et al., 1985; Callaghan, 1977, 1986; Fiedler & Maschwitz, 1988, 1989; Horvitz
et al., 1987; DeVries, 1987, 1988), also regularly tend homopterans (see records
and references in Wheeler, 1910; Lamborn, 1915; Farquarson, 1922; Way, 1963;
Malicky, 1969, 1970; Bristow, 1984; personal observations) and EFNs (see
records and references in Bentley, 1977; Beckman & Stucky, 1981; Schemske,
1982; Buckley, 1983; Koptur, 1979, 1984; Koptur & Lawton, 1987; Horvitz &
Schemske, 1984; Longino, 1984; Smiley, 1985; Beattie, 1985; Whalen &
MacKay, 1988; Oliviera & Brandao, 1991; D. Feener & G . Schupp,
unpublished data; personal observations).
I90
P. J. DEVRIES
Although it is not known how specific the foraging biology of all species in the
largest ant genera may be (e.g. Camtonotus, Crematogaster, Pheidole, Aeteca,
Zridomyrmex), or how complete these literature records are, the overall pattern
presented in Table 5 indicates that only a fraction of the world’s generic
diversity of ants (in this case less than 10%) tend secretion producing organisms.
Thus insects and plants that typically produce secretions are unlikely to have
strong interactions with the majority of ant species.
DISCUSSION
Ecological variation
The facultative association between T. irenea and attending ants is mutualistic,
and may be an important factor in determining larval population densities on
hostplants. When a predatory wasp attempts to attack a larva tended by even a
single E. ruidum it is likely that the ant will repel the wasp. In contrast, larvae
without attending ants are virtually certain to be killed during a wasp attack.
The larvae of T. irenea ‘pay’ for this production against predators by producing a
concentrated amino acid secretion that is constantly solicited and imbibed by
attending ants (DeVries, 1988; DeVries & Baker, 1989). The protection
provided by ants explains part of the higher larval abundance on plants
patrolled by ants shown in Table 1. Several factors not examined by this study
may also affect larval abundance.
Adult vespid wasps hunt for arthropods to supply their growing larvae with
food (Spradbury, 1973; Evans & Eberhard, 1970; J. Carpenter, personal
communication). If colony size and reproductive state influences wasp foraging
behaviour, predator pressure on butterfly larvae is likely to vary in space and
time. Thus, the local species composition and reproductive state of individual
wasp colonies are factors likely to affect larval population densities of T. irenea.
Insect parasitoids are considered strong selective agents for the maintenance of
ant association in one North American lycaenid butterfly (Pierce & Mead, 1981;
Pierce & Easteal, 1986). Finding that E. ruidum ants provided T. irenea larvae no
protection against attack by tachinid flies (Table 2) is consistent with the
observations of Malicky (1969, 1970), who observed that ants attending
European lycaenids were too slow to protect larvae against parasitoids, and
Pierce et al. (1987) who showed that ants were ineffective against a braconid
wasp affecting an Australian lycaenid species. Together, these observations
indicate that the strength of selection due to parasitoids may, in general, vary by
site, the species of butterfly, and the species of parasitoids involved.
The quality of protection conferred to myrmecophilous insects by ants can
vary with ant species (Bristow, 1984). For T. irenea, smaller ants may be better at
protecting larvae against parasitoids than the medium-sized E. ruidum, which is
effective against wasp predators. Since the local distribution of ant colonies
influences what ant species associate with T. irenea and other riodinid species
(personal observations), rates of parasitism and predation may vary with the
identity of the ant species tending larvae.
Mutualism
The present study supports the idea that mutualisms were important in the
evolution of myrmecophily in butterflies: larvae gain survival benefits from
THISBE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS
191
associating with ants. However, had this study occurred under conditions of
negligible vespid predator attack (as tachinid parasitoid attacks were not ant
dependent), or had a different ant fauna been tending the plants and larvae, this
study might have lent support to the idea that appeasement is a driving force in
the evolution of butterfly myrmecophily.
The specialized ant-organs of riodinid and lycaenid larvae provide secretions
and stimuli critical for obtaining the benefits of ant attendance (Pierce et al.,
1987; DeVries, 1988, 1990; Fiedler & Maschwitz, 1988, 1989; DeVries &
Baker, 1989). The pattern presented here (Tables 4, 5) suggests that butterfly
larvae are attended only by ant taxa that frequently harvest the secretions
produced by plants and insects. Thus, specialized larval ant-organs and
butterfly-ant associations appear to have been selected for and maintained
through facultative mutualisms with a restricted subset of the total ant
species-secretion-foraging ants.
If only secretion-foraging ants enter into mutualisms with larvae, it is likely
that ant taxa with other feeding behaviours (predators, or taxa that ignore
larvae) may have played a minor role in the evolution of ant-organs and
associated characters. This study suggests that wherever myrmecophilous larvae
occur they will be found associating only with ant species that typically use
secretions as a major portion of their diet, and that the ant taxa found
associating with butterfly larvae will also tend local Homoptera and EFNs. If the
patterns found with T. irenea are general, many of the ant taxa in any
community, especially tropical ones, should not be larval predators (cf. Malicky,
1970), but should ignore butterfly larvae, homopterans and EFNs.
Facultative associations in which several different ant taxa may tend a species
of butterfly larva appear to be common among riodinids and lycaenids in the
neotropics (personal observations), and among lycaenids elsewhere in the world
(Pierce, 1987;J. Thomas, personal communication). Ant taxa that kill ‘I.irenea
(i.e. Azteca, M Q ~ Ubut
C ~tend
S ) other species of butterfly larvae (Table 4)indicate
that secretion harvesting alone does not necessarily mean that an ant species will
tend a butterfly larva-specialized associations do occur. Among neotropical
riodinids there seems to be two broad categories of larval-ant association:
facultative generalists that may associate with ants from the subfamilies
Ponerinae, Formicinae and Myrmicinae, and specialists that apparently
associate only with ants in the Dolichoderinae (DeVries, 1987, unpublished
data). Although obligate or highly specific ant associations (involving a single
ant species or genus) are uncommon in lycaenids (Pierce, 1987; Thomas el al.,
1989) and riodinids (personal observations), it is reassuring to note that even
these specialized associations all involve taxa of secretion harvesting ants.
Appeasement
The influence of appeasement on butterfly-ant interactions has been discussed
with respect to how larvae may avoid ant aggression. Thus, ant-organs are
thought to ‘detoxify’ ants by secreting adoption substances, appeasement
substances or food rewards (e.g. Malicky, 1970; Henning, 1983; Pierce, 1987;
Fiedler & Maschwitz, 1989). However, although it has been given thoughtful
discussion, the role appeasement plays in the evolution of butterfly ant-organs
needs to be broadly assessed experimentally in the future. I suggest that
experimental assessment of the ability of larvae to appease ants can be done
192
P.J. DEVRIES
through elaboration of the preliminary tests done with I: irenea described above.
Future tests should also include a comparison of ant responses to lycaenoid
larvae with ant responses to larvae from other groups of Lepidoptera that do not
bear ant-organs (e.g. Papilionidae, Pieridae, Nymphalidae, Noctuidae, etc.) .
By offering many species of larvae to many species of generally predaceous
ants, and scoring what proportion of ant species kill or ignore larvae, one could
estimate the importance of appeasement in ecological time. If larval ant-organs
have evolved to appease predaceous ants, we would expect to see significant
numbers of larvae with ant-organs surviving encounters with ants. If, however,
all larvae are killed by ants, this would suggest that larval ant-organs can only
‘appease’ potentially mutualist ant taxa. The contribution of ‘appeased’ ant
species to mutualistic associations with larvae can then be evaluated by
performing ant exclusion experiments. Using the three outcomes of interactions
between T. irenea larvae and ants as a model (ignore, kill, tend), ‘appeasement’,
then, is the evolution of ant response from predation to ignoring larvae, and
mutualism is the evolution from predation or ignoring larvae to tending them.
Appeasement and mutualism
There may be sufficient variation in diet among some predaceous ant taxa for
appeasement to function in some cases. The subfamily Ponerinae is composed of
predaceous ant species, all with well-developed stings used to immobilize
arthropod prey (Wheeler, 1910; Brown, 1973, 1976, 1978; Carroll & Janzen,
1973). The genus Ectatomma is unusual among ponerines in that all species spend
large fractions of their life harvesting secretions from EFNs (Bentley, 1977;
Wheeler, 1986; personal observations), Homoptera (Wood, 1983; personal
observations), and myrmecophilous butterfly larvae (personal observations).
This suggests that within at least one ant subfamily there has been evolution
from a predominantly predaceous diet to one where secretions are important.
Although they are not known to tend larvae, the occasional utilization of some
secretions in other ponerine genera (e.g. Odontomachus, Brown, 1976; Paraponera,
Carrol & Janzen, 1983) may eventually permit larval secretory organs to
function in appeasement, eventually leading to mutualism (e.g. as in Ectatomma).
Most of the major groups of ants were present by the Oligocene, and the
morphology of fossil ants suggests that many life-history patterns, including
secretion foraging, were present at this time (Wilson, 1971; Brown, 1973).
Assuming that the patterns of ant-larval associations described here reflect
evolutionary history, it is plausible that, regardless of which associations evolved
first-EFNs, homopterans or myrmecophilous butterfly larvae-once ants began
foraging on and protecting secretion producing resources, other groups of plants
or animals with secretory capabilities were effectively preadapted to form
mutualisms with the same ant taxa.
Although providing predaceous ants with appeasement rewards may have
been an initial step in the evolution of larval ant-organs for butterflies, once
larvae developed the capability to secrete substances, it is likely that the
evolutionary refinement of ant-organs and their spread through the lycaenid and
riodinid butterfly lineages was utlimately dependent upon mutualisms formed
with ants that use secretions. Although this historical scenario cannot be tested,
simple experimental manipulations with larvae and ant species can test whether
the results of evolution on ant-organs contribute to mutualisms, to what extent
THISBE IRENEA AND T H E EVOLUTION O F BUTTERFLY-ANT MUTUALISMS
193
ant-organs function in appeasement, and which ant taxa are likely candidates for
exerting selection on ant-organs and other secretion producing organisms.
ACLNOWLEDGEMENTS
This paper benefited from comments and discussion provided by M. Aide,
B. Bolton, L. Gilbert, N. Greig, D. Feener, D. Grimaldi, J. Longino, D. Nash,
N. Pierce, S. Rand, C. Thomas, W. Watt, R. I. Vane-Wright and three
anonymous reviewers. I thank B. Bock, J. Clark, C. DuFrane, T. Gutierrez,
N. Greig and J. May for field assistance, and D. Feener and G. Schupp for
unpublished data and ant identifications. For statistical consultation I thank
D. Feener, S. Adolph and R. Miller. This study was supported by a
Smithsonian predoctoral fellowship, and is part of a Ph.D. dissertation,
University of Texas at Austin. The study is dedicated to the mutualistic work of
J. Coltrane, S. La Faro, L. Morgan, W. Montgomery and M. Roach.
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