Revista Chilena de Historia Natural 69: 339-342, 1996 Seed dispersal by lizards in Chilean rainforest Dispersion de semillas por lagartijas en el bosque lluvioso de Chile 1 MARY F. WILLSON , CARLOS SABAG2, JAVIER FIGUEROA2, 2 JUAN J. ARMESTO2 and MARCELO CAVIEDES 1Foreslry Sciences Laboratory. 2770 Sherwood Lane. Juneau AK 99801, USA. E-mail: /s=M .WILLSON/OUI = RI OA@ MHS-FSW A.A TTMAIL.COM 2Dcpartamcnto de Biologia, Facultad de Ciencias. Universidad de Chile, Casilla 653, Santiago, Chile ABSTRACT Lizards (Liolaemus pictus) of the south-temperate rainforest of Chile eat fruits of Nerrcra granadensis Re!bunium hypo- carpium, and occasionally other species. Seeds may be retained in the digestive tracts for several days. Nertera granadensis seeds that passed through lizard digestive tracts germinated more rapidly than untreated seeds. Thus, these lizards are capable of dispersing viable seeds of N. granadensis. Key words: frugivory, Liolaemus pictus, seed dispersal, south-temperate rainforest, Nertera granadensis. RESUMEN La laga11ija (Lio!aemus pictus) de Ios bosques lluviosos del sur de Chile come frutos de Nertera granadensis, Relbunium hy- pocarpium y ocasionalmente de otras especies. Las semillas pueden ser retenidas en el tracto digestivo durante algunos dias. Las semillas de N. granadensis ingeridas por la lagartija germinan más rapido que las semillas control. Por tanto, esta lagartija puede ser un agente dispersor de semillas de N. granadensis. Palahras clave: frugivoria, Liolaemus pictus, dispersion de semillas. bosque lluvioso templado del sur, Nertera grana- deJlsis. INTRODUCTION both tropical and temperate (e.g., Symon 1979, Clifford & Hamley 1982, Iverson The fleshy fruits produced by many species 1985, Barquin et al. 1986, Whitaker 1987, of seed plants are an adaptation for seed Traveset 1990, Fleming & Lips 1991, Cortes dispersal by animals, especially vertebrates Figueria et al. 1994, Valido & Nogales (Ridley 1930, Van Der Pijl 1982). Birds and 1994). Frugivory by lizards of the Chilean mammals are by far the most commonly rainforest has been suspected for some time studied seed vectors among the vertebrates, (Armesto & Rozzi 1989, C. Villagnin, pers. although reptiles and fishes are also known comm.); we here document frugivory and to disperse seeds regularly (references in transport of intact, germinable seeds by Willson 1983). Indeed, reptiles were prob- Liolaemus pictus chiloeensis (Muller & ably the earliest terrestrial animals to inter- Hellmich) (Tropiduridae). act with seed plants in seed-dispersal mutualisms (Weigelt 1930, Chalchoner & Sheerin 1981, Tiffney 1984, Herrera 1989, METHODS Fleming & Lips 1991 ), although amphibians should not be discounted out of hand (Da Ten individuals of L. pictus were captured in Silva et al. 1989). Among reptiles, tortoises late November, 1992, and 62 individuals are perhaps the best-known -though little were captured in January 1994, near the edge studied- agents of seed dispersal, but of mature secondary forest near Huelden, evidence is slowly accumulating that lizards northeast Isla de Chiloe (approx. 42°S 74° may be important mutualists in many areas, W). They were housed individually, for one- (Received 20 July 1995: accepted 15 !\!arch !996: managed by Javier A. Simonctti and Fabian M. Jaksic). 340 WILLSON ET AL. two weeks, in cages made of perforated defecated intact Nertera seeds from fruits plastic soda bottles. Body size of the captives consumed before capture. Some of the ranged from 5-8 cm snout-vent length (ap- defecated seeds appeared as long as 5-7 days proximately). We inspected each cage peri- after capture. In 1994, 32 of the 62 lizards odically for seed-containing feces. At the (52%) passed seeds of N. granadensis, eight end of these observations, most lizards were individuals (13%) passed seeds of R. hypo- released near the site of capture; two were carpium, one individual (2%) passed seeds returned to Santiago for confirmation of of Gaultheria sp., and 21 individuals (34%) identification. passed no seeds during the captive period. Two species of seeds commonly found in Among the lizards that had eaten some fruit, the feces of captive lizards were used in the the estimated median number of N. grana- germination experiments. Nertera grana- densis fruits eaten per lizard was 2 (range 1- densis (Mutis ex L. f.) Druce (Rubiaceae) is 8) and of R. hypocarpium was 3 (range 1- a ground-hugging herbaceous species that 14). Of all the seeds (n = 285) passed by produces red-orange fruits, 2-3 mm in dia- captive lizards in 1994, 62% were N. grana- meter, both in exposed positions above the densis, 28% were R. hypocarpium, and 10% leaves and in concealed positions beneath the were Gaultheria. leaves Relbunium hypocarpium (L.) Hems!. Germination of R. hypocarpium was very (Rubiaceae) is an herbaceous species that low (maximum = 2 seeds/replicate) and no commonly twines among the branches of difference could be detected between treat- small shrubs. The orange fruits are about 2 ments. Nertera granadensis seeds generally mm in diameter. There are usually two seeds germinated faster after passage through per fruit in both species, and the pulp of both lizard digestive tracts. The median percent- kinds of fruits is very watery (ea. 96% water age of seeds germinating after passage was in N. granadensis). 50%, compared to 5% in the control in Ex- Preliminary germination trials with seeds periment 2 (Mann-Whitney U = 1, n = 8,8; of N. granadensis in growth chambers at the P < 0.001). There was no significant dif- Facultad de Ciencias showed that exposure ference in Experiment 1, although some to light enhanced the germination rate (75% seeds germinated in the treatment replicates of seeds) compared to germination in dark but none did in the controls. The total pro- conditions (1 0% ). Subsequent experiments portion of seeds germinating was greater were therefore conducted with 12 hours of after gut-passage than in controls in both exposure to light each day. Seeds were placed experiments (Experiment 1: 29% vs. 0%, n in Petri dishes, 10 seeds/dish, and the dishes = 70, 50; x2 = 15.2, P < 0.0001; Experiment 2 were placed in a growth chamber at 20° C. 2: 51% VS. 6%, n = 80,80; x = 39.5, p < Experiment 1 began on 9 August and ended 0.0001). Almost all germination of N. grana- on 7 October 1994; the seeds were checked densis occurred in a pulse, 2.5-3.0 weeks five times during this period. Experiment 2 after initiation of the experiment. began on 28 October and ended on 2 Decem- ber 1994; the seeds were checked seven times during this period. Germination data were DISCUSSION analyzed by Mann-Whitney U tests compar- ing the number of seeds germinated in each These observations document frugivory and replicate in treatment and control and, transport of intact seeds by L. pictus in the secondarily, by x2 tests on the total number rainforest of southern Chile. Although Do- of germinated seeds in treatment and control. noso-Barros (1966) described this species as fundamentally arboreal, on Chiloe they RESULTS are commonly found on the ground and have ready access to fruits of plants such as Ner- Most lizards produced 2-5 feces during the tera. Seed retention times were much longer observation period, each deposit composed (several days) than is usual in small chiefly of insect remains (especially Coleop- passerine birds (usually < 3 hr), although the tera). Seven of the ten lizards in 1992 residence time of seeds in the digestive tract SEED DISPERSAL RAINFOREST BY LIZARDS 341 might be somewhat less in free-ranging, Anna Traveset and two anonymous review- actively foraging lizards than in our captive ers for helpful comments on the manuscript. animals, which ate very little. This is contribution N° 2 from Estaci6n That N. granadensis seeds germinate Biol6gica Senda Darwin, Ancud, Chiloe, a faster after exposure to light may be associat- field station established by the Institute of ed with our observations that this species Ecological Research Chiloe. commonly grows in forest light-gaps and at forest edges, rather than in forest interior. In addition, lizards commonly bask in the light, LITERATURE CITED raising their body temperatures and meta- ARMESTO JJ & RR ROZZI (1989) Seed dispersal bolic rates. Higher metabolic rates might in- syndromes in the rain forest of Chiloe: evidence for the importance of biotic dispersal in a temperate rain crease rates of gut passage and the probabi- forest. Journal of Biogeography 16: 219-226. lity that seeds would be defecated in well-lit BARQUIN, E, M NOGALES & W WILDPRET (1986) In- sites. If so, then components of lizard be- tervenci6n de vertebrados en la diseminaci6n de plantas vasculares en Inagua. Gran Canaria (lslas Ca- havior would enhance their ecological role as narias). Vieraea (Spain) 16: 263-272. agents of seed dispersal. The low germina- CHALCONER WG & A SHEERIN (I 98 I) The evolution of tion rate observed for R. hypocarpium need reproductive strategies in early land plants. In: GGE SCUDDER & JL REVEAL (eds.), Evolution Today: not mean that lizards are poor dispersal Proceedings of the Second International Congress of agents for this species. We must know more Systematic and Evolutionary Biology: 93-100. about the germination requirements of this CLIFFORD HT & T HAMLEY (1982) Seed dispersal by species before we can assess adequately the water dragons. Queensland Naturalist 23: 49. CORTES FIGUEIRA JE, J VASCONCELLOS-NETO, MA possible role of lizards in dispersal. GARCIA & AL TEIXEIRA DE SOUZA (1994) Chile and New Zealand offer unusual Saurochory in Melocactus violaceus (Cactaceae). opportunities to examine seed dispersal by Biotropica 26: 295-30 I. DA SILVA HR. MC DE BRITTO-PEREIRA and U lizards in temperate forests: Both regions CARAMASCHI (1989) Frugivory and seed dispersal have relatively depauperate faunas of avian by Hyla truncata, a neotropical tree-frog. Copeia and mammalian seed dispersers, local I 989: 78 I -783.