Effects of bird ingestion on seed germination of four woody species of thetemperate rainforest of Chiloé island, Chile

Javier A. Figueroa* and Sergio A. CastroDepartamento de Ecología, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile; *Authorfor correspondence (e-mail: jfiguero@genes.bio.puc.clfax: 56-2-6862621)

Received 9 November 1999; accepted in revised form 1 November 2000

Key words: Endozoochory, Frugivorous birds, Seed dispersal, Seed germination, Seed ingestion, Temperate rain-forest

Abstract

We study the effect of ingestion by birds on seed germination and the consequences of absence of dispersal, withthe persistency of the seeds inside the fruit. We collected seeds of four woody species of the temperate rainforestof Chiloé: Gaultheria mucronata, Luma apiculata, Myrteola nummularia, and Myrceugenia planipes. The seedstested had the following origins: 1) Ingested seeds: seeds collected from the feces of birds, 2) Extracted seeds:seeds obtained directly from the fruits, and 3) Intact fruits: fruits collected directly from the plants. Germinationof Myrceugenia planipes under greenhouse conditions, Luma apiculata, and Myrteola nummularia under labo-ratory conditions, and Gaultheria mucronata under both conditions was analyzed. We found that the seeds reachtheir maximum germination between 15–20 days after sowing, with the exception of those of G. mucronata sownin the greenhouse, which showed a low germination rate. In the greenhouse assay, seeds of G. mucronata in-gested by birds, seeds extracted manually from the fruits, and seeds inside the fruits did not show significantdifferences in their germination percentages. In the laboratory assays, the seeds of G. mucronata and M. num-mularia ingested by birds and the seeds extracted manually from the fruits also did not show any significantdifference in germination. Under laboratory conditions, the seeds of L. apiculata ingested by birds presented astatistically greater percentage of germination than the seeds extracted manually. Under greenhouse conditions,seeds of M. planipes ingested by birds did not present a statistically different germination percentage from thoseseeds extracted from the fruits. The seeds of M. planipes, and L. apiculata inside the intact fruits did not germi-nate. We conclude that birds do not affect the seed viability of any of the four species studied.

Introduction

The fate and ecology of seeds ingested by frugivo-rous animals continues to be the focus of many ex-perimental studies (Agami and Waisel 1986; Izhakiand Safriel 1990; Cipollini and Levey 1997; Willsonet al. 1996; Yagihashi et al. 1998). It has been shownthat the effects of seed ingestion by frugivorous ani-mals on germination can vary considerably (Barneaet al. 1990; Izhaki and Safriel 1990; Yagihashi et al.1998). After intact seeds are defecated by frugivorousanimals, their germination can increase (Noble 1975),diminish (Livingston 1972) or remain unresponsive(Salomonson 1978), as compared to seeds that do not

pass through the digestive tract. When seed ingestionincreases germination, it has been proposed that thefruit pulp that is consumed by the frugivore may con-tain a germination-inhibiting compound that is elimi-nated by the process of digestion (Mayer and Polja-koff-Mayber 1975; Cipollini and Levey 1997). It canalso be explained by some modification of the seedcover structure by digestive action (Agami and Waisel1986). When the ingestion of seeds does not affect thegermination rate, it has been proposed that the frugi-vores act only as dispersal agents (Barnea et al. 1990).If the passage through the digestive tract affects theviability of the seeds negatively, the frugivores wouldnot be legitimate dispersal agents. However, only

17Plant Ecology 160: 17–23, 2002.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.

scarce articles have evaluated the consequence of theendozoochory upon the plant population, for exam-ple, examining the germination of the non-dispersedseeds from the parent plant and of that remaining in-side the fruit (Izhaki and Safriel 1990; Yagihashi etal. 1998).

The dominant seed-dispersal syndrome in the tem-perate rainforest of Chile is endozoochory, reportedfor approximately 70% of the woody species inChiloé (Armesto and Rozzi 1989; Willson 1991). Inthese forests, birds are the main consumers of thefleshy fruits and the 90% of them include fleshy fruitsin their diet (Correa et al. 1990; Sabag 1993; Rozzi etal. 1996). Mammals and reptiles play only a smallrole as fruit consumers and seed dispersal agents inthis region (Armesto and Rozzi 1989; Willson et al.1996). In spite of this evidence, there is scarce andfragmentary information on the effect of birds on thedistribution, structure, and composition of the forestecosystems in Chiloé (Villagrán et al. 1986; Armestoand Rozzi 1989; Hernández 1995; Willson et al.1996). While this evidence suggests that frugivorousbirds in the Chiloé rainforest could have importanteffects on both seed dispersal and germination, thereis no experimental evidence concerning the effect ofpassage through the bird’s guts on seed germinationof Chiloé species.

The object of this study was to determine the ef-fect of seed ingestion by frugivorous birds on thegermination of four plant species of the Chiloé tem-perate rainforest. Experiments in the laboratoryand/or in a greenhouse were carried out to evaluatethe effects of seed ingestion. Four main questionswere addressed in this study: (1) What is the mostprobable fate of seeds that remain inside the fruits,and that were not dispersed by the frugivorous birds?(2) Are the Chiloé birds legitimate dispersal agentswith regard to germination? (3) Do the seeds of themost common species of plants found in Chiloé re-spond in the same way to ingestion by birds? and (4)Do the seeds of Gaultheria mucronata respond in thesame way under laboratory and greenhouse condi-tions?

Materials and methods

Study area and species

This study was conducted at Estación BiológicaSenda Darwin (41°50� S; 73°45� W, approx.), located

10 km east of Ancud, on the Isla Grande of the Ar-chipiélago de Chiloé, Chile. The island is 180 kmlong and is approx. 2 km from the continent at itsnorthern end. At this site the mean annual precipita-tion and the mean annual temperature are approxi-mately 2200 mm and 9.5 °C, respectively. The cli-mate is temperate humid with intense maritime andMediterranean influence during the summer months(di Castri and Hayek 1975). The Senda Darwin arbo-real vegetation is dominated by species typical of theevergreen rainforest region of Valdivia (Gajardo1994), with representatives of the families Myrtaceae,Fagaceae, Proteaceae, and Winteraceae being com-mon. Shrubs (representatives of Baccharis, Gaulthe-ria, Berberis) are almost exclusively found in forestmargins, and in open fields. The forest understorey isdensely populated by woody vines (e.g. Luzuriagaspp), and tree seedlings. However, the Senda Darwinforests were severely disturbed by the previous own-ers during the last 30 years of use as pasture, culti-vated fields, and the production of firewood. Furtherdata on the climate, topography, soils, and history ofthe Chiloé vegetation are given by Veblen (1985);Holdgate (1961); Donoso (1985); Villagrán (1985).

To carry out our study, four species of plants werechosen: Gaultheria mucronata (L.f.) Gaud. ExSpreng (Ericáceae), Luma apiculata (DC.) Burret,Myrceugenia planipes (H. et A.) Berg, and Myrteolanummularia (Poiret) Berg (all Myrtáceas). Theseplants were chosen because during the study period(July to October of 1998) they offered the greatestnumbers of mature fruits and they were the most com-monly found seeds in bird feces (Sabag 1993;Hernández 1995). The most important biological,ecological and morphological characteristics of thespecies are indicated in Table 1.

The most common resident frugivorous birds inthe region during the study period were: Turdus fal-cklandii (Quoy and Gaimard), Pyrope pyrope (Kittl-itz), Phrygilus patagonicus (Lowe) (Rozzi et al. 1996;Sabag 1993). These birds are commonly observedfeeding on the fruits of the species chosen for thisstudy (pers. obs.). Later, the birds sit on fallen logs,isolated trees and fences and evacuate their feces con-taining seeds.

Seed collecting

In order to obtain seeds and fruits, propagules werecollected directly from the parent plants of Gaultheriamucronata, Luma apiculata, Myrceugenia planipes,

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and Myrteola nummularia. The defecated seeds wereobtained directly from fresh feces of those birds thatrested on logs, fences, the soil of open sites and un-der isolated trees. To obtain seeds of similar age, thefruits from the plants and seeds from the feces werecollected in the same period of the year (July of1998). Immediately after collection from the motherplant, seeds were extracted manually from the fruitsand air-dried for 2–3 days. In the other case, the seedswere removed manually from the feces.

Germination assays

In order to maintain greater control over the germi-nation conditions and over each seed sown, in theseassays we prefer sown seeds in the laboratory andgreenhouse. There are studies that show differencesin the germination percentages and rates of seedssown under laboratory conditions to those of seedssown under natural conditions. However, there is evi-dence that the qualitative effect of bird ingestion onseed germination is similar for both conditions (Yagi-hashi et al. 1998).

Laboratory assays in Facultad de Ciencias, Univer-sidad de Chile, Santiago, were initiated less than 8days after seed harvest in the field. The seeds weresown onto papers in Petri dishes, 9 cm diameter, in-side a germination chamber under controlled condi-tions. The seeds were moistened with distilled water.To determine the number of seeds that germinatedunder laboratory conditions, the Petri dishes weremonitored every three days. In the germination cham-ber, a thermal regime of 20/10 °C (day/night respec-tively) and a light regime of 12 hours light/darkness

were established. This temperature range is suitablefor seed germination in most temperate forest species(Bradbeer 1988), and close to that used by Figueroaet al. (1996) for the Chiloé species.

Greenhouse assays in the Estación BiológicaSenda Darwin were initiated less than 5 days afterseed harvest from plants. The seeds also were sownonto papers in Petri dishes, 9 cm diameter, but theenvironmental conditions were uncontrolled. How-ever, the windows were opened during periods ofhigher temperatures, although they were scarce be-cause the assays were in the winter. The seeds weremoistened with distilled water, and, to determine thegermination dynamics, were monitored every tendays.

The seeds, in the laboratory and greenhouse weresown onto papers because these are most homoge-neous to that of forest soil and to diminish the seeddepredation by fungi that inhabit soil. The germina-tion assays concluded one month after sowing in thelaboratory and two months after sowing in the green-house. The germination assays were concluded ac-cording to germination times obtained for these spe-cies by Figueroa et al. (1996).

Origin of the seeds assayed

The seeds of Myrceugenia planipes and Gaultheriamucronata were incubated in the greenhouse. Theseeds of Luma apiculata, Gaultheria mucronata andMyrteola nummularia were incubated in the labora-tory, because there was not enough laboratory mate-rial in the greenhouse for all of the species. Only inthe case of G. mucronata had we a sufficient number

Table 1. List of species studied in the Chiloé rainforest, their taxonomic assignment, life form, forest habitat, flowering period, fruitingperiod, and fruit and seed attributes.

Species

Characteristic Gaultheria mucronata Luma apiculata Myrceugenia planipes Myrteola nummularia

Family Ericaceae Myrtaceae Myrtaceae Myrtaceae

Life form Shrub Tree Tree Shrub

Forest habitat Edge Edge Interior Edge

Flowering period Summer Fall Summer Summer

Fruiting period All year Winter Spring Fall

Fruit type Berry Berry Berry Berry

Fruit color Red - Pink - White Black Violet Pink

Fruit mass (mg) 300 300 800 100

Seed mass (mg) 0.2 1 90 0.07

Seeds per fruit >30 4–7 4–7 >30

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of defecated seeds to be able to incubate them underboth laboratory and greenhouse conditions. The seedshad the following origins. 1) Ingested seeds: seedscollected from bird feces. 2) Extracted seeds: seedsobtained directly from fruits. 3) Intact fruits: fruitscollected directly from the plants. Due to the limitednumber of seeds found in bird feces, we had to re-duce the number of seeds sown under laboratory con-ditions for G. mucronata and M. nummularia. Theseeds sown and their replicate numbers are shown inTable 2.

Statistics

To compare the final percentage of germinated seedsbetween origins 1 and 2 (see above) in Gaultheriamucronata (under laboratory conditions), Luma api-culata, Myrceugenia planipes, and Myrteola nummu-laria, the Mann-Whitney non-parametric test was ap-plied. To compare the final percentage of germinatedseeds among origins 1, 2 and 3 (see above) in Gault-heria mucronata (under greenhouse conditions) theKruskal-Wallis non-parametric test was used. Lastly,to compare the germination dynamic of the seeds be-tween origins 1 and 2 for each species studied, re-peated measures ANOVAs was used.

Results

The seeds reached their maximum germination ratebetween 15 and 20 days after sowing with the excep-tion of those of Gaultheria mucronata that were sownin the greenhouse, which germinated at lesser ratesfor all of the origins (Figure 1). The higher tempera-ture of the germination camera probably increased thegermination percentage in G. mucromata seeds.

The delay of the germination was not affected dueto seed ingestion by birds. The germination in thelaboratory of G. mucronata, Luma apiculata, andMyrteola nummularia began after three days for bothingested and extracted seeds. The germination ofMyrceugenia planipes in the greenhouse was imme-diate, both for ingested and extracted seeds. Lastly,the germination of G. mucronata in the greenhousebegan after the one month from sowing (Figure 1).

In the laboratory, the germination dynamic of theG. mucronata seeds that had been ingested by birdsdid not differ significantly from the seeds that hadbeen extracted manually from fruits (repeated mea-sures ANOVA, P > 0.05). This same result was re-corded in M. planipes and M nummularia (repeatedmeasures ANOVA, P > 0.05) (Figure 1).

On the other hand, the percentage of final germi-nation differed significantly between ingested (32 ± 3S.E. %) and extracted (23 ± 2 S.E. %) seeds of Lumaapiculata (Mann-Whitney, U = 3.0, P = 0.047). How-ever, the germination dynamic between both originsin this same species were not significantly different(repeated measures ANOVA, P > 0.05) (Figure 1).

The seeds of L. apiculata, and M. planipes insidethe intact fruits did not germinate (Figure 1) and de-composed rapidly. However, in the greenhouse, theseeds of G. mucronata inside the intact fruits germi-nated (9 ± 2 S.E. %) without significant differencefrom ingested (23 ± 2 E.S. %) and extracted (17 ± 6S.E. %) seeds (Kruskal-Wallis, H = 3.3, P > 0.05).Finally, when we compared the percentage of finalgermination between ingested and extracted seeds ofG. mucronata in the laboratory (92 ± 5 S.E. % v/s 77± 12 S.E. %, respectively), M. planipes (42 ± 12 S.E.% v/s 37 ± 14 S.E. %, respectively), and M. nummu-laria (28 ± 5 S.E. % v/s 31 ± 3 S.E. %, respectively)the analyses did not show significant differences(Mann-Whitney, P > 0.05).

Table 2. Replicate and seed per replicate (n) number of each origin of the seeds sown in the greenhouse (Chiloé) and in the laboratory(Santiago) by four species of the Chiloé forest.

Species Germination conditions Origin of the seeds

Ingested Extracted Intact

replicates n replicates n replicates n

Gaultheria mucronata greenhouse 3 50 3 50 3 50

Gaultheria mucronata laboratory 3 25 3 25 - -

Luma apiculata laboratory 3 50 3 50 3 50

Myrceugenia planipes greenhouse 3 50 3 50 3 50

Myrteola nummularia laboratory 3 25 3 25 - -

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Figure 1. Germination dynamic for each origin of Gaultheria mucronata seeds under laboratory conditions, Gaultheria mucronata seedsunder greenhouse conditions, Luma apiculata seeds under laboratory conditions, Myrceugenia planipes seeds under greenhouse conditions,and Myrteola nummularia seeds under laboratory conditions. The bars indicate ± 1 S.E.

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Discussion

We do not know of any published information on seedgermination after ingestion by frugivorous birds inthe Chiloé forests. However, there is one previousobservation of germination in vitro of the seeds ofNertera granadensis and Relbunium hypocarpium ex-tracted from the feces of the lizard Liolaemus pictus(Willson et al. 1996). The results indicated that theseeds of N. granadensis that had been ingested bylizards germinated faster than the seeds that were notingested. On the contrary, the germination of R. hy-pocarpium was very low and no differences could bedetected between ingested and non-ingested seeds(Willson et al. 1996).

In our study, the passage through the bird’s gutsdid not have a significant effect on the germination ofthe seeds of Gaultheria mucronata (Figure 1). Thishas also been observed in other species of Mediterra-nean, tropical and temperate plants (Brunner et al.1976; Debussche 1985; Izhaki and Safriel 1990;Salomonson 1978; Stocker and Irvine 1983). Theseeds of G. mucronata germinated inside the pulp ofthe fruit in a smaller proportion than the seeds out-side the fruit, but this difference was not statisticallysignificant. In field observations, S. Castro, J.Figueroa and M. Willson have independently foundthat seed germination occurs on the parent plant ofG. mucronata (unpublished data). These results sug-gest that the frugivorous birds are only dispersing theseeds of G. mucronata away from the parent plant,but this would not change the biology of the germi-nation. Also, G. mucronata forms a dense cover at theedge of the secondary forests of Chiloé. Therefore,frugivoruos species could play an important role inmoderating the strong intraspecific competitionthrough the dissemination in space of the newly re-cruited individuals, because the feces has the seeds ofonly a few species, usually one plant (Correa et al.1990).

The seeds of Luma apiculata and Myrceugeniaplanipes that belong to a group of Myrtaceae withnaked embryos, showed similar responses to inges-tion by birds. In both species, the seeds inside thepulp of the fruit did not germinate, whereas those in-gested by birds or extracted manually germinated(Figure 1). These results suggest that the pulp of L.apiculata and M. planipes may inhibit seed germina-tion. The pulp of the fruit could exert a filtering ef-fect on incidental light that could inhibit germination,furthermore, a chemical inhibitor of germination may

be present in the pulp (Cipollini and Levey 1997;Yagihashi et al. 1998). Our recent germination assaysin L. apiculata suggest that the germination absencein seeds that remain inside the pulp could be due toan effect combined between the absence of light in-side the fruit and the presence of a chemical inhibitor(unpublished data).

The passage of the seeds through the bird’s gutsalso does not affect the germination of Myrteola num-mularia seeds, and frugivorous birds (Turdus falck-landii and Pyrope pyrope) are probably legitimatedispersal agents of their propagules. It is likely thatbirds increase the probability that seeds of M. num-mularia will find appropriate sites for germinationand seedling establishment.

In the Chiloé forest, frugivorous birds in the pri-mary and secondary succession increase the abun-dance of plants with fleshy fruits (Villagrán et al.1986), and increase the regeneration rate of the sec-ondary succession (Hernández 1995). Additionally,with the results of our study we suggest the possibil-ity that most of the plants with fleshy fruits (mainlyMyrtaceae) of the temperate forests of southern Chileare dependent for their reproduction to a large extenton seed ingestion by birds.

Conclusions

Frugivorous birds are the most important consumersof fruits in the temperate rainforest of Chiloé (Arm-esto and Rozzi 1989; Willson 1991) and are mostlikely the main legitimate dispersal agents of seeds inplants with fleshy fruits in the region. Although pre-vious studies suggest and show the importance ofbirds in the colonization, dynamics, and structuring ofthe Chiloé rainforests (Villagrán et al. 1986; Hernán-dez 1995), no previous experimental studies in theliterature had shown the effects of frugivorous birdson seed germination. Our results show that seed in-gestion does not affect the viability of seeds in any ofthe species studied; frugivorous birds are legitimatedispersal agents for all four species. In G. mucronataand M. nummularia, the birds only perform the roleof seed dispersal, enabling the propagules to reachsites far from the parent plant without affecting ger-mination. In L. apiculata and M. planipes the birdsalso help to eliminate the pulp in order to permit seedgermination, as well as dispersing the seeds. If theseeds of L. apiculata and M. planipes are not ex-

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tracted from the fruit and dispersed by birds, micro-organisms or rodents are likely to consume them.

Acknowledgements

We thank P.A. Marquet, J.F. Hernández, and twoanonymous reviewers for making useful commentson the manuscript, E. Figueroa for his assistance inthe translation of the paper, and in laboratory experi-ments, and J. Vidal for his help in the field. This re-search was supported by the project FONDECYT3980020. This is a contribution to the research pro-gram of ONG Entorno and of Estación BiológicaSenda Darwin, Ancud, Chiloé. J.A.F. is funded by aMellon Foundation Fellowship.

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