Xavier Espadaler, Crisanto Gomez, and David Suiter.
Seed-robbing between ant species intervenes in the myrmecochory of Euphorbia characias (Euphorbiaceae).
Psyche 102:19-25, 1995.

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SEED-ROBBING BETWEEN ANT SPECIES INTERVENES IN THE MYRMECOCHORY OF EUPHORBIA CHARAC1AS
(EUPHORBIACEAE)
A case of interference competition in which some ant species (Messor barbarus and Aphaenogaster senilis) rob seeds of Euphor- bia characias from other ants (especially Tapinoma nigerrin~um) is reported. Seed robbing is here regarded as a possible natural impediment to myrmecochory as it may interfere with the seedling recruitment process of the myrmecochorous plant. Interference competition is a rather frequent phenomenon in ant communities (Holldobler and Wilson, 1990) and may involve terri- torial guarding (Holldobler and Lumsden, 1980), the use of chemi- cal deterrents (Adams and Traniello, 1981), threat displays (Holldobler, 1981), physical fighting (Holldobler, 1979) and nest- plugging (Moglich and Alpert, 1979; Gordon, 1988). Interspecific prey robbing, as defined by Holldobler (1986), is a spectacular form of competition in which the robber ant takes the food from the grasp of a foraging ant of another species. Though the success rate of prey robbing may be as high as 25.5% (Holldobler, 1986), eventual positive or negative ecological and reproductive effects on both parties have not been evaluated. Intraspecific intercolonial prey robbing has been recently described (Breed, Abel, Bleuze, and Denton, 1990; Yamaguchi, 1995). Though not strictly similar, a case of indirect seed scavenging involving granivorous ants is reported by Levieux (1 979) in African dry savannas: Brachypon- era senaarensis takes seeds from external middens of Messor galla and Messor regalis. This case could be regarded as an evolutionary step towards the robbing of individual ants. 'c.R.E.A.F. Universitat Autbnoma de Barcelona 08193 Bellaterra, Spain. ^epartament de Cikncies Ambientals, Universitat de Girona Pla{a Hospital, 6. 17001 Girona, Spain.
Manuscript received 10 August 1994.




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20 Psyche [VOI. 102
In this paper we report a case of direct interference competition, in which ants rob another ant species of the seeds of a myrmeco- chorous plant (Euphorbia characias). Myrmecochorous plants have seeds with an oily aril called an elaiosome. Ants that are attracted to the elaiosome feed on it and discard the seeds inside their nests or in nearby middens, where they may germinate. This results in the seeds being dispersed to sites that may offer better conditions for germination and growth (Beattie, 1985). Nothing is known of the relative importance of Euphorbia seeds in the diet of granivorous ants. The elaiosome is rich in lipids (Bresinsky, 1963) and may be an important source of nutrition for the growing larvae of robber species. Further work is needed to understand variation in the response of ants to the elaiosomes. Seed robbing may also have consequences for E. characias.
Observations were made during a long-term study on the disper- sal ecology of west Mediterranean Euphorbia species, conducted in an herbaceous community of Inulo-Oryzopsietum miliaceae (Bolos, 1962) at the Collserola Park, an ecological preserve near Barcelona, NE Spain (2'6'E, 41å¡25'N elevation: 315 m) during the summers of 1993 (July) and 1994 (June). The site is on an east- facing slope; the climate is Mediterranean, with 620 mm of annual rainfall. Mean monthly temperatures are highest in August (aver- age 22.6OC) and lowest in January (7.1å¡C (data from 1914-1991). The site is a clearing bordered by a mixed wood of Pinus pinea, Pinus halepensis, and Quercus ilex with a developed underwood of Rhamnus alaternus, Rosa sp., Pistacia lentiscus, Hedera helix, Ruscus aculeatus, and Smilax aspera. All observations were made in a field that has been abandoned for 13 years, with a slope of 15' and an area of 1800 m2. The dehiscence period of Euphorbia characias at Collserola lasts for four weeks, and depending on the year, from mid May to the end of June. The plants scatter seeds singly throughout the day and the seeds do not release recruitment behavior by ants.
Seed retrieval was assessed from 8:30 a.m. to 19:30 p.m. as fol- lows. A single seed was put at each corner of a square of 7 cm and the time elapsed between deposition and retrieval of the seed by an ant was recorded. The ant species initially finding the seed was



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noted and followed when possible to the nest. Each sampling point was designated by changing randomly among six compass direc- tions and with a random distance from one to six meters from the previous point. During seed retrieval some robbing by other ant species took place. Seed robbing can also occur during the manipu- lation time (MT) that occurs after an ant has found a seed for the first time and before it carries the seed away.We hypothesized that longer MT would result in more robbing. During separate trials and for each species, 40 manipulation times on individually offered seeds were measured with a stop watch. A total of 285 seeds were offered individually. Four ant species retrieved seeds. Tapinoma nigerrimum (worker size: 2.5-5.1 mm; polymorphic) and Pheidole pallidula (size: 2.2-4.5 mm; dimorphic) were the two most abundant, retrieving 26.3% and 30.5% respec- tively. The nests of both species appear to act as safe-sites for E. characias seeds because seedlings appear there. Aphaenogaster senilis (size: 6.4-7.7 mm; monomorphic) took 23.8% of the seeds and deposits them outside of the nest in an external midden after elaiosome removal. Messor barbarus (size: 3- 12 mm; polymorphic) took 19.3% of the seeds. This ant is granivorous and thus seeds are lost for plant recruitment. An analysis of M. barbarus middens from 9 nests yield 2 intact seeds and 185 empty seeds, proving that this ant consumes the seed as well as the elaiosome. The percentage of seeds robbed did not differ between the two years of the study (Wilcoxon matched pairs signed ranks test, z=1.6; p=0.1). Tapinoma nigerrimum and Pheidole pallidula are the most frequent victims of seed robbing (Table 1). Messor ants are never robbed because they carry seeds high above the soil. Likewise, A. senilis holds the seeds in a similar position, above the level of the antennae of Pheidole or Tapinoma. In contrast, seeds transported by Pheidole or Tapinoma are readily detectable by Messor or A. senilis. Seed transport by P. pallidula is variable: sometimes it drags the seed, sometimes it carries the seed as in Messor or A. senilis. It is robbed both by Messor or A. senilis but defends the seed by leaving it and attacking the raider, which may allow other workers in the vicinity to rob the unprotected seed. A. senilis may even try to rob seeds when a Pheidole forager is near



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Psyche [vo~. 102
Table 1. Seed robbing in ants retrieving myrmecochorous seeds of Euphorbia characias at Collserola, NE Spain. Indi- cated is the species initially getting the seed and the species finally taking the seed to the next. A. July 1993. B. June 1994. M: Messor barbarus; A: Aphaenogaster senilis. P: Pheidole pallidula. T: Tapinoma nigerrimum.
A Final
Initial M A P T Total % robbing
B Final
Initial M A P T Total % robbing
its nest entrance: the first try is usually fruitless, but in the second opportunity the movements of the robber ant are very precise, agile, and sometimes successful. If Pheidole continues its attack, A. senilis sets the seed aside, frees itself from the small Pheidole, and picks up the seed again.
Tapinoma always drags the seed. It has a small mandibular gap and usually has much difficulty carrying seeds. It often loses the seed but may find it again. It is frequently robbed by all of the other species. When a robbery is attempted, Tapinoma workers leave the seed and try to attack the intruder but its attack is frantic, making rapid, rather undirected turns. Encounters between individ- uals of different species seem to be haphazard and robbed species do nothing to avoid encounters with the robber species. Seed rob- bing consists entirely of encounters between two ants, the robber and the victim. Cooperative behavior, such as recruitment, does not occur in either of the participating ant species. Robbing may occur both during the manipulation process or during the transport



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and either early in the morning or in the afternoon. This bimodal distribution of time of robbing reflects the daily bimodal activity rhythm of Messor, Aphaenogaster, Pheidole, and Tapinoma. Manipulation time
The length of manipulation times differs between species (one- way ANOVA on log transformed data: F(3,156)=3.9; p=0.009) but the only statistically significant difference is between Tapinoma and Pheidole (post-hoc Scheffe test, ~~0.03). All other combina- tion pairs are not distinct. Manipulation time is not related to body size or to the frequency of being robbed. Many factors can affect the number and rates of robbing events. In 1994 the level of robbing (7.6%) was lower than in 1993 (19.1%). Combining data for both years reveals that 33.3% of seeds collected by Tapinoma nigerrimum are robbed. Of these robbed seeds, 25/29 were taken by Aphaenogaster or Messor, ants that substantially reduce the probability of seed survival. Because the attraction response to seeds is a generalized one released by key substances (Brew, O'Dowd, and Rae, 1989), it is difficult to imagine any strategy whereby the plant could target seed attrac- tiveness towards ant species that promote seed survival by deposit- ing seeds within the nest.
Robbing ants are an integral part of a guild of species very com- mon in west Mediterranean open biotopes. The group of Pheidole, Messor, Tapinoma, and Aphaenogaster (s.str.) has been found else- where by Baroni Urbani, 1968 (Malta); Rodriguez and Ferniindez, 1983 (So Spain); Cagniant, 1973 (Algeria), 1988 (Morocco); Case- vitz-Weulersse, 1989 (Corsica). Zorrilla, Serrano, Casado, Acosta and Pineda, (1986) report this group of ants from therophytic pas- tures in central Spain with different degrees of disturbance. Seed robbing is very probably a widespread phenomenon. Davidson and Morton (1981) suggest some Australian ant species may be parasites of the interaction between ants and chenopods. A more extreme case of disruption of myrmecochory involving the invasive Argentine ant and Proteaceae in Cape Fynbos



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24 Psyche [vo~. 102
is reported by Bond and Slingsby (1984). At our site the level of disruption is apparently not so important as in the systems men- tioned above. Moreover, since there is no reason to suspect that the relationship between disperser ants and robber ants is recent, plant populations are unlikely to be threatened by the toll imposed by robber ants. Myrmecochorous Euphorbia characias faces both beneficial and detrimental ants and it is a matter of chance which particular species finds its seeds. This case of seed robbing may be regarded as a possible natural impediment to myrmecochory. We thank Josep Morera and the Sangrh family for permission to work on their properties. Gabriel Genovk and Xavier Roig assisted in field experiments. Two anonymous referees provided very wise and useful suggestions on the work and kindly revised the lan- guage. The project is supported by a grant from DGICYT (PB91- 0482) to XE.
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