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Of Euphorbia Characias Seeds by Ants

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Of Euphorbia Characias Seeds by Ants Acta CEcologica, 1997, 18 (1), 39-46 Soil surface searching and transport of Euphorbia characias seeds by ants Xavier Espadaler (*) and Crisanto G6mez (**) (*) CREAF, Universitat A utdnoma de Barcelona, 08193 BeUaterra, Spain. (**) Departament de Ci~ncies Ambientals, Universitat de Girona, Plafa Hospital, 6, 17001 Girona, Spain. Received: 10.6.96 Accepted: 25.10.96 Abstract The intensity of exploring the soil surface by ants was studied for the four species involved in the dispersal and predation of seeds of the West-Mediterranean myrmecochorous plant Euphorbia characias. During the dehiscence period (June) the whole soil surface is scanned in 43 minutes. Not all ants that find a seed take it to the nest. For the four ant species studied (Pheidole pallidula, Aphaenogaster senilis, Tapinoma nigerrimum, Messor barbarus) the proportion of ants that finally take the seed is 67.6%. In spite of this, the high level of soil surface searching explains the rather short time that seeds remain on the soil before being removed. The presence of an elaiosome is a key element in the outcome of the ant-seed interaction: a seed with elaiosome has a seven-fold increase in probability of being taken to the nest if found by a non-granivorous ant. The predator-avoidance hypothesis for myrmecochory is supported. Keywords: Ants, seed dispersal, elaiosome, Euphorbia, myrmecochory, predation. R6sm~6 L'intensit6 avec laquelle les fourmis explorent la surface du sol a 6t6 6tudi6e pour les quatre esp~ces qui participent ~ la dispersion et 5 la pr6dation des graines d'Euphorbia characias, une plante myrm6cochore de l'ouest m6diterran6en. Au cours de la p6riode de d6hiscence (juin), la surface enti~re du sol est pass6e au crible en 43 minutes. Toutes les fourmis qui trouvent une graine ne l'apportent pas dans le nid. Pour les quatre esp~ces 6tudi6es (Pheidole pallidula, Aphaenogaster senilis, Tapinoma nigerrimum, Messor barbarus), la proportion de fourmis qui emportent finalement la graine est de 67,6%. Malgr6 cela, l'intense exploration de la surface du sol explique le peu de temps pass6 par les graines sur le sol avant d'etre emport6es. La pr6sence d'un 61a'fosome est un 616ment-cl6 darts l'issue de 1'interaction fourmi-graine : une graine pourvue d'un 61a'fosome a sept lois plus de chances d'6tre emport6e dans le nid, si elle est trouv6e par une fourmi non-granivore. L'hypoth~se scion laquetle la myrm6cochorie permet d'6viter la pr6dation est 6tay6e. Acta CEcologica 1146~509 X/97/0II$ 7.00/ Gauthier-Vitlars 40 X. Espadaler and C. G6mez INTRODUCTION Myrmecochorous plants produce seeds that attract ants. The seeds are transported to the ants' nests. Seeds are provided with an elaiosome rich in lipids (BREW et al., 1989; KUSMENOGLUet al., 1989), whose high molecular weight suggests scant diffusion rates. Non-granivorous ants feed on the elaiosome and discard the seed inside the nest or in the refuse pile. Granivorous ants, however, eat seeds regardless of the presence of an elaiosome. If a seed does not have any chemical attractant this finding is also a matter of chance: the ant must pass nearby the seed and touch it. Vision may help but there are no data concerning detection of immobile objects in ants (HOIIDOBLER & WILSON, 1990). Several hypotheses have been proposed as explaining the advantages of myrmecochory (BEATTIE, 1985) but only a single one, predator avoidance, has the characteristic of being influenced by the time a seed is left on the soil, before it is found and recovered by a myrmecochorous ant. The sooner the seed is found by a dispersing ant, the better the opportunity for escaping predation. Seeds removed slowly are more vulnerable to predators (TURNBULL & CULVER, 1983; BOND & BREYTENBACH, 1985). Predators fall in three groups: rodents (REICHMAN, 1979; INOUYE et al., 1980), birds (MARES & ROSENZWEIG, 1978; KELRICKet al., 1986) and granivorous ants (ASHTON, 1979; ANDERSEN, 1987). Here we offer some evidence that the probability of escape from predation is rather strong in the case of the Mediterranean myrmecochore Euphorbia characias L. (Euphorbia hereafter). Seeds of this species are scattered ballistically all during the day and are transported by ants (BAIGES et al., 1991; GOMEZ, 1994). A low level of interspecific seed-robbing between dispersing ants has been detected (ESPADALER et al., 1996) though its significance for Euphorbia seedling recruitment has still to be evaluated. Seeds are not attractive from a distance and have to wait until a particular ant species finds it. This waiting time is short (mean 52.3-t-6.7 [s.e.] minutes; ESPADALER 8Z; GOMEZ, 1996). The response of individual ants to different stimuli may depend on variables such as worker age, distance from the nest, prior experiences, resource availability, type of food or colony needs (Sul~D, 1987; TRANIELLO, 1987; TRANIELLO et al., 1992; FOURCASSII~ & TRANIELLO, 1994). So, even if a seed is found, there is no guarantee that the ant will take it to the nest. We address the following questions: 1. What proportion of ants finding a seed removes it to the nest ? 2. Is the elaiosome a key element in seed transport ? 3. How intense is the searching of the soil surface by ants that retrieve Euphorbia seeds ? METHODS Observations were made in a herbaceous community at the Collserola Park, an ecological preserve near Barcelona, NE Spain (41~ 2~ The site is an old field on former agricultural arable land, abandoned for 14 years. The site is located on an east-facing slope. The climate is Mediterranean, with 620 mm of annual rainfall. Mean monthly temperatures are highest in August with an average 22.6~ and a low of 7.1~ in January (data from 1914-1991). The site is a clearing bordered by a mixed wood. Vegetation in the clearing is mainly a herbaceous community of Inulo-Oryzopsietum miliaceae (BoLos, 1962). Though there are 17 ant species, only four remove Euphorbia seeds: Messor barbarus (granivorous), Pheidole pallidula (omnivorous), Aphaenogaster senilis (omnivorous) and Tapinoma nigerrimum (mainly nectarivorous). The total density of nests for the four species is 0.2 per m 2. During Acta O~cologica Soil surface searching by ants 41 the dehiscence period, in June, the soil surface is denuded, thus, ants can easily walk and retrieve items; there are no difficult areas to search such as steep or wet patches. Data recording The proportion of seeds found and taken by ants was evaluated by offering intact single seeds (n = 590) to ants and noting if the seed was recovered after being found. The influence of the elaiosome was evaluated by offering single seeds (n = 361) with the elaiosome artificially removed. We recorded the behaviour of individual ants upon finding a seed as a) taking it to the nest or b) ignoring the seed. The intensity of surface soil searching by ants was evaluated by drawing the trajectory made by individual ants during a sampling period of 5 minutes on an acetate sheet with a square of 10 x 10 cm, on top of a wire frame at 5 cm from the soil. A single ant could be followed and traced even if more than one was present. If the ant we were tracing left the 10 x 10 area before the 5 minutes were over, the first new incoming ant was followed and so on. This constitutes a sample. A new sampling point was designated by randomly changing among six compass directions with a random distance from 1 to 6 meters from the previous point. Trajectories for each ant species were color coded. Data for Pheidole pallidula have been underestimated due to its small size and to its temporary disappearance from sight amid grasses or herbs. A total of 129 5-minutes samples was taken, beginning at 8 h in the morning and ending at 20 h in the evening. Data were obtained on different days (July 1991, June 1993, June and July 1994, May 1995), in the middle of the dehiscence period of Euphorbia. Trajectories were recorded only for those ant species involved in seed transport. Data analysis The mean expected time (Te) a seed remains on soil surface after being released by the mature plant depends on a) the time needed for a complete searching of the surface (Tr) and, thus, for a seed to be found and b) the probability (/9) of a seed that has been found is transported to the nest. Not all seeds found are actually taken; a fraction of ballistically dispersed seeds will remain on soil and, in turn, will wait a new Tr and the process will iterate "a" times, as expressed in (1) (t) ~=~ aTrrp(1-p)~-1 1 Tr was obtained by relating the surface to be scanned and the surface actually scanned by ants per time unit (Vr). The surface to be scanned is the sample of 10 x 10cm (S). The surface occupied by the seed was not considered since it is extremely small (7.43 x 10 -4 cm 2, based on the estimated seed density of 2.29 seeds/m2/day and seed size of 3.65 mm length x 2.10 mm width; ESPADALER& GOMEZ, 1996). Vr, the surface searched per time unit, depends on the surface searched by each species. When foraging, ants walk with the funiculi directed somewhat outside. Since species differ in size, the antennal gap (= distance between tip of antennae) was measured on photographs of foraging ants for each species. Size of antennal gap of each species was used to construct a grid of small squares; thus, each species has a particular "searching grain". Each specific grid was superimposed on actual trajectories and the number of squares traversed by or touched by the trajectories were counted.
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