0378-1844/02/04/186-05

Received: 11/22/2001. Modified: 01/24/2002. Accepted: 01/30/2002

INFLUENCE OF MICROCLIMATE AT DIFFERENT CANOPY HEIGHTS ON THE GERMINATION OF Ficus (Urostigma) SEEDS DISPERSED BY MEXICAN HOWLER MONKEYS (Alouatta palliata mexicana)

Juan Carlos Serio-Silva and Victor Rico-Gray

KEY WORDS / Ficus / Germination / Alouatta palliata mexicana / Disturbed Habitat / Preserved Habitat /

Juan Carlos Serio-Silva. Ph.D. in Ecology and Management of Natural Resources, Instituto de Ecología, AC, Xalapa, Veracruz, México. Address: División Académica de Ciencias Biológicas. Universidad Juárez Autónoma de Tabasco. Km. 0.5 Carretera Villahermosa-Cárdenas. Villahermosa, Tabasco 86039, México. e-mail: serioju@ecología.edu.mx

Victor Rico-Gray. Ph.D., Tulane University, USA. Senior Research Scientist, Plant Ecology Department, Instituto de Ecología, AC, Xalapa, Veracruz, México. e-mail: ricogray@ecologia. edu.mx

Summary

A variety of microclimatic factors influence the success of seed germination in the strangler figs Ficus perforata and F. lundelli consumed by howler monkeys (Alouatta palliata mexicana) in southern Veracruz, Mexico. Seed germination was compared at two canopy heights in two different study sites: disturbed (Playa Escondida; 40ha) and preserved (Carolino Anaya Reserve, Coatzacoalcos; 600ha). Germination varied depending on canopy height where the seeds were placed, and the quality (degree of conservation) of the habitat (preserved or disturbed). There was an evident between-habitat variation in humidity, light intensity, and temperature in the host trees for hemiepiphytic Ficus, which may affect the percent of germination response. The results show higher germination at the highest canopy location for seeds of both species. Germination was significantly higher in the preserved site for seeds from feaces vs. seeds from fruits source. The latter is probably the effect on seed germination of the higher relative humidity and low light and temperature levels in the preserved site.

Resumen

Diversos factores microclimáticos influyen en el éxito de la germinación de semillas de Ficus estranguladores (F. perforata y F. lundelli) consumidas por monos aulladores (Alouatta palliata mexicana) en el sureste de Veracruz, México. La germinación de semillas de estas especies fue comparada entre dos estratos arbóreos en dos diferentes sitios de estudio: perturbado (Playa Escondida; 40ha) y conservado (Reserva Carolino Anaya, Coat-zacoalcos; 600ha). Los resultados muestran que la germinación varió con el estrato arbóreo donde fueron depositadas las semillas y con la calidad (grado de conservación) del hábitat (conservado o perturbado). Bajo estas diferentes condiciones de hábitat, fueron evidentes las variaciones en humedad, intensidad de luz y temperatura de los árboles hospederos para los Ficus hemiepífitos, que podrían estar afectando el porcentaje de germinación. Se registró mayor germinación de ambas especies en los estratos superiores. La germinación fue significativamente mayor en el sitio conservado para las semillas que provenían de las heces contra aquellas no dispersadas de esta manera. Esto último es, probablemente, resultante de una mayor humedad relativa y bajos niveles de luz y temperatura que influyen positivamente en la germinación en el sitio conservado.

Resumo

Diversos fatores microclimáticos influem no êxito da germinação de sementes de Ficus estranguladores (F. perforata y F. lundelli) consumidas por macacos uivadores (Alouatta palliata mexicana) no sudeste de Veracruz, México. A germinação de sementes destas espécies foi comparada entre dois extratos arbóreos nos dois diferentes lugares de estudo: perturbado (Playa Escondida; 40ha) e conservado (Reserva Carolino Anaya, Coatzacoalcos; 600ha). Os resultados mostram que a germinação variou com o extrato arbóreo onde foram depositadas as sementes e com a qualidade (grau de conservação) do habitat (conservado ou perturbado). Sob estas diferentes condições de habitat, foram evidentes as variações em umidade, intensidade de luz e temperatura das árvores hospedeiras para os Ficus hemiepífitos, que poderiam estar afetando a percentagem de germinação. Registrou-se maior germinação de ambas espécies nos extratos superiores. A germinação foi significativamente maior no lugar conservado para as sementes que provinham das fezes em vez daquelas não dispersadas desta maneira. Este último é, provavelmente, resultante de uma maior umidade relativa e baixos níveis de luz e temperatura que influem positivamente na germinação no lugar conservado.

 

Introduction

It has been shown that howler monkeys (Alouatta spp.) are particularly important seed dispersers of Ficus (Coates-Estrada and Estrada, 1986, Estrada and Coates-Estrada, 1991). This suggests that Ficus seeds consumed by these primates and deposited with their faeces, attain a higher germination success (De Figueiredo, 1993, Serio-Silva and Rico-Gray, unpublished). This process could be very important in the regeneration dynamics of tropical rain forests, especially with regard to Ficus species that belong to the subgenus Urostigma, which are hemiepiphytes and need a host or support tree in order to germinate. Howler monkeys use the canopy strata for their normal activities, and it is there where seeds are deposited with the faeces on host trees (e.g., branch forks, depressions, bark). On these sites, Ficus (Urostigma) seeds can find microclimatic factors appropriate to their germination and establishment success. However, these microclimatic factors are not uniform across a forested area (Laman, 1995a). Microclimatic conditions are highly variable when undisturbed and disturbed habitats inhabited by howler monkeys are compared. Laman (1995a), studying fruits seed germination using canopy planter boxes in a Bornean tropical rain forest, showed that given adequate water and nutrients, Ficus seedlings will grow faster in a higher light environment, and all these conditions are important for seed germination. In a previuos study (Serio-Silva, 2002), seeds of Ficus perforata and F. lundelli from faeces of Mexican howler monkeys (Alouatta palliata mexicana) collected at either disturbed or preserved habitats were found to germinate faster (9-11 days) and in higher numbers (60-80%) than seeds collected from fruits and kept under controlled laboratory conditions. In the present study, the effect on seed germination of different microclimatic factors (light, temperature, humidity) in the canopies of disturbed and preserved habitats is compared. The influence of canopy height (low, high) and habitat disturbance on in vivo germination success is analyzed, particularly how microclimatic factors influence the germination success of howler-ingested and -noningested seeds of two Ficus species. We also attempt to evaluate if the preserved habitat conditions and their microclimatic influence on canopies have a positive impact on Ficus (Urostigma) seed germination, as compared with a disturbed habitat.

Materials and Methods

Study sites

Field work and planter box experiments were carried out between January 1998 and June 1999 in two contrasting habitats, both of them inhabited by howler monkey troops, in southeastern Veracruz, México. Table I lists the general characteristics of the disturbed site (DIS), a relatively small isolated forest patch modified by human activities (extraction of species, artificial fires, agriculture, cattle raising, etc.) located in Playa Escondida, San Andrés Tuxtla, and those of the preserved site (PRE), a relatively undisturbed large area protected from human activities by a local company, but connected to other forested areas, which represent one of the most representative tropical rain forests in southern Veracruz. The latter is located in the Carolino Anaya Reserve, near Coatzacoalcos.

Study troops

In the disturbed site there are four howler monkey troops and in the preserved site there are eight troops (Table I). We studied two troops at each site. The two troops selected for study in the disturbed site had eight and nine individuals, and those in the preserved site had eight and ten individuals. To estimate the home range of howler monkey troops in each site, we conducted a preliminary survey following the suggestions by Zucker et al. (1996). Howlers exhibited larger home range size and lower density in the preserved (home range= 75ha, Density= 0.12/ha; 8 troops; 74 ind.) than in the disturbed habitat (home range= 10ha, Density= 1.05/ha; 4 troops; 42 ind.), based on estimations by Estrada and Coates-Estrada, (1984).

Seed collection

For controlled germination trials, mature syconia (at least 100g each time) of F. perforata and F. lundelli were collected from the forest floor, where they had fallen during monkey feeding bouts. Fruits were weighed, washed and dried, and then seeds were separated and randomly selected. Monkey faecal samples were collected from the forest floor, mostly under the trees where the monkeys defecated, particularly under those trees where they begin their locomotion patterns. Faeces were washed and dried to separate leaf fiber from seeds, which were then randomly selected for the germination trials. Seeds from both faeces and syconia were observed under the microscope to confirm the presence of an embryo and those with fig wasps (Agaonidae) were discarded.

Field experiments

Microclimate within a rain forest can be highly variable, even among trees of the same species (Laman, 1995b). To reduce inter-tree variation, within the most homogeneous portion of the studied forests, we selected one sampling tree of a typical Ficus host (e.g., Diospyros dygina, Ebenaceae), and increased the sampling units per tree (planter boxes). Thus, conditions (tree) were not replicated, hence; statistical inference is limited to the plots (planter boxes) included in this study (Wester, 1992). Planter boxes (constructed from polyvinyl chloride plastic roof gutter material) were designated as sampling units, and 10 of each were placed at two heights on the tree (low, 20m and high, 25-30m). Boxes were suspended from branches using ropes, and spaced ca. 5m apart. Each box (100x60x10cm) had 200 small isolated holes, which were stuffed with small pieces of Sabal mexicana bark and a small piece of humidified cotton (to provide for initial humidity). Holes were randomly assigned (50 holes/seed type/box) and contained one seed each from the following types: a) F. perforata seeds from fruits, b) F. perforata seeds from faeces, c) F. lundelli seeds from fruits, and d) F. lundelli seeds from faeces. A band of Tree Tanglefoot (The Tanglefoot Co., Jackson, MS, USA) was applied around each box to protect seeds from removal by ants. Boxes were also covered with cloth mesh to protect seeds from the direct impact of rain. At each germination box and canopy height a calibrated light-sensitive paper (Diazo) was placed for measuring integrated light (log10PAR; Bardon et al., 1995), and for each canopy height a hygro-thermometer clock (Extec Instruments, model 445702) was placed with a daily sampling of temperature (oC) and humidity (%). Germination (appearance of the radicle) was checked every two days for 40 days.

Statistical analyses

Log-linear models were fitted with the GLIM-4 statistical package (Francis et al., 1993) to test the hypothesis that differences in germination are related to the factors considered: species (F. perforata, F. lundelli), site (preserved, disturbed), canopy height (high, low), and seed source (fruits, faeces). As "proportions data" were used, a logit model was employed. As a result of data overdispersion, the goodness-of–fit was evaluated with an F-test, using a binomial error over the proportions. With binomial errors, the change in variance can be compared directly at F tables to assess its significance (Crawley, 1993).

One way ANOVA was used to compare microclimatic factors: light (log10PAR), temperature (oC), and humidity (%) per site and per canopy height, during the 40 days period. For each factor we used a Tukey test to evaluate all pairwise multiple comparison for significant differences (Zar, 1996).

Results

Significant differences (P<0.001) were obtained for integrated light (PAR) between sites and canopy heights, with higher PAR values in both high canopy heights of disturbed and preserved sites (Figure 1a). The results also show significant differences (P<0.001) in temperature, with higher temperature levels on both canopy heights of the disturbed site (Figure 1b). Finally, humidity was significantly higher (P<0.001) on both canopy heights in the preserved site (Figure 1c). In summary, the disturbed site was subject to higher light intensity and temperatures, and lower humidity levels than the preserved site.

For both sites and species, a higher germination percentage was obtained for seeds taken from faeces than for seeds taken directly from fruits, despite canopy height (Table II). The log-linear model showed a significant difference (P<0.0001) in germination between sites, species, seed sources and for the interaction of site x species. These accounted for 16.32%, 10.44%, 40.68% and 1.10%, respectively, of the total variation explained by the model (Table III).

Discussion

The results show that microclimatic factors (humidity, light, temperature) differed between preserved and disturbed tropical rainforest sites, and that these factors had a significant influence on seed germination. Seed source (from faeces rather than from fruits) was, however, the factor that explained the most in the resulting model. Even though certain authors have suggested that consumption of Ficus seeds by animals is not an obligatory condition for germination (Titus et al., 1990; Laman, 1995b), the present results assess that the number of seeds germinating after their passage through the digestive tract of howler monkeys is very important. Thus, despite site characteristics, the effect of howler monkeys is to facilitate germination success of Ficus seeds. Furthermore, we found differences in germination success between experiments in the field (planter boxes) and under controlled laboratory conditions (Serio-Silva, 2002), being lower in the former (Table II). All this suggests that in order to study the regeneration of tropical rain forests, the microclimatic conditions should be taken in consideration, rather than those found to be successful in laboratory environments.

The degree of site preservation should not only affect germination success but seedling establishment as well. Although we did not study seedling establishment, the results show that similar conditions to those suggested by Laman (1995a) were present in the higher canopy of the preserved site, where germination success was higher. The hemiepiphytic habit is considered an adaptation to exploit the high-light canopy environment (Laman, 1994, 1995b; Dobzhansky and Murca-Pires, 1954; Ramírez, 1977; Putz and Holbrook, 1986; Daniels and Lawton, 1991). Nevertheless, the present results suggest that the relative humidity and temperature of the germination site and its surroundings, as well as host density (Athreya, 1999) should also be considered. Sites in the canopy with this combination of conditions for Ficus seed germination appear to be very scarce (Galil and Meiri, 1981), particularly in disturbed sites. Under such circumstances, areas of preserved forest that maintain optimal (undisturbed) conditions, coupled with the presence of substrates with good moisture retention, should highly influence seed germination success (Putz and Holbrook, 1989).

Howler monkeys in natural habitats (perturbed or preserved) perform an important role in depositing seeds in optimal sites for germination (Estrada and Coates-Estrada, 1986; de Figueiredo, 1993; Martínez-Mota, 2001) and establishment. However, host microclimatic conditions should also be considered to attain successful establishment. Although Ficus have commonly been regarded as keystone species for conservation in many tropical rain forests (Leighton and Leighton 1983; Terborgh, 1986; Mc Key, 1989), the present results suggest that the consequences of habitat fragmentation could be to contribute to decreased howler monkey-Ficus interactions and, thus, the possibility of seed dispersal, the first step in the process of seed germination and eventual establishment and development of tropical forests.

In the future it will be important to carry out studies that help to understand if other factors are also important in this dispersal process, for example: a) the role of howlers on successful deposition of seeds in host trees, b) the value of feaces for seeds while they can be germinated and established on the trees, c) the effect of digestion by howlers on the germination of seeds, depending on ingestion time (Liberman et al., 1979; Murray et al., 1994), and d) the influence of some secondary compounds from fruits and their relation with ingestion by howlers and the possibility to be dispersed. In summary, the biology of forest regeneration is very complex and can easily be altered by forest transformations (Howe and Miriti, 2000; Zuidema et al., 1996). It is clear that the range of herbivore behavior and their interactions with plants should be studied in more detail, especially under the environmental conditions associated with habitat fragmentation.

Acknowledgments

The authors thanks to Albright and Wilson Troy for permission to work in the Carolino Anaya Reserve, Tim Laman, V. J. Sosa-Fernández, V. Parra-Tabla, R. Manson and two annonymous reviewers for their comments and suggestions on earlier drafts of this manuscript, and J. Bello-Gutiérrez for his help with the statistical analyses. The research was supported by Instituto de Ecología A.C. (902-16) and a CONACyT scholarship to JCSS. We thank field equipment donation by Idea Wild.

Figure 1. Mean (+sd) of light (a), temperature (b) and humidity (c) for each canopy height for disturbed and preserved sites. HCP: high canopy preserved. LCP: low canopy preserved. HCD: high canopy disturbed. LCD: low canopy disturbed.

 

References

Athreya VR (1999) Light or presence of host trees: which is more important for the strangler fig? J. Trop. Ecol. 15: 589-603.

Bardon RE, Countryman DW, Hall RB (1995) A reassessment of using light-sensitive Diazo paper for measuring integrated light in the field. Ecology 76: 1013-1016.

Coates-Estrada R, Estrada A (1986) Fruiting and frugivores at a strangler fig in the tropical rain forest of Los Tuxtlas, México. J. Trop. Ecol. 2: 349-357.

Crawley M (1993) GLIM for ecologists. Blackwell Scientific. Oxford. 379 pp.

Daniels JD, Lawton RO (1991) Habitat and host preferences of Ficus crassiuscula, a neotropical strangling fig of the lower-montane rain forest. J. Ecol. 79: 129-141.

De Figueiredo RA (1993) Ingestion of Ficus enormis seeds by howler monkeys (Alouatta fusca) in Brazil: effects on seed germination. J. Trop. Ecol. 9: 541-543.

Dobzhansky T, Murca-Pires J (1954) Strangler trees. Scientific American 194: 78-80.

Estrada A, Coates-Estrada R (1984) Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas, Mexico. Int. J. Primatol. 5: 105-131.

Estrada A, Coates-Estrada R (1986) Frugivory in howling monkeys (Alouatta palliata) at Los Tuxtlas: seed dispersal and fate of seeds. In Estrada A, Fleming TH (Eds) Frugivores and seed dispersal Dr W. Junk Publishers. The Hague. pp. 93-104.        [ Links ]

Estrada A, Coates-Estrada R (1991) Howling monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal; ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. J. Trop. Ecol. 7: 459-474.

Francis B, Green M, Payne C (Eds.) (1993) The GLIM system: release 4 manual. Claredon Press. Oxford. pp. 821.

Galil J, Meiri L (1981) Druplet germination in Ficus religiosa L. Isr. J. Bot. 30: 41-47.

Howe HF, Miriti MN (2000) No question: seed dispersal matters. Trends Ecol. Evol. 15: 434-436.

Laman TG (1994) The ecology of strangler figs (hemiepiphytic Ficus spp.) in the rain forest canopy of Borneo. Ph.D. Dissertation. Harvard University. 173 pp.

Laman TG (1995a) Ficus stupenda germination and seedling establishment in a Bornean rain forest canopy. Ecology 76: 2617-2626.

Laman TG (1995b) The ecology of strangler fig seedling establishment. Selbyana 16: 223-229.

Leighton M, Leighton DR (1983) Vertebrate responses to fruiting seasonality within a Bornean rain forest. In Sutton SL, Whitemore TC, Chadwick AC (Eds.) Tropical rain forest: ecology and management. Blackwell. London. pp. 181-196.        [ Links ]

Liberman D, Hall JB, Swaine MD, Liberman M. (1979). Seed dispersal by baboons in the Shai Hills, Ghana. Ecology 60: 65-75.

Martínez-Mota R (2001) Papel de las hormigas en la remoción de semillas de Ficus perforata excretadas por Alouatta palliata mexicana en un fragmento de selva (Playa Escondida) en Los Tuxtlas, Veracruz. B.Sc. Thesis, Universidad Veracruzana-Xalapa. México. 37 pp.

McKey DB (1989) Population biology of figs: applications for conservation. Experientia 45: 661-673.

Murray KG, Russell S, Picone CM, Winnet-Murray K, Sherwood W, Kuhlmann ML (1994) Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75: 989-994

Putz FE, Holbrook NM (1986) Notes on the natural history of hemiepiphytes. Selbyana 9: 61-69.

Putz FE, Holbrook NM (1989) Strangler fig rooting habits and nutrient relations in the Llanos of Venezuela. Am. J. Bot. 76: 781-788.

Ramírez WB (1977) Evolution of the strangling habit in Ficus subgenus Urostigma (Moraceae). Brenesia 12/13: 11-19.

Serio-Silva JC (2002) El papel de Alouatta palliata mexicana como agente dispersor del género Ficus; especies clave de los bosques tropicales. Ph.D. Dissertation, Instituto de Ecología, A.C. Xalapa, Veracruz, México. 52 pp.

Terborgh J (1986) Keystone plant resources in the tropical rain forest. In Soulé M (Ed.) Conservation biology. Sinauer. Sunderland. MA. pp. 330-344.        [ Links ]

Titus JH, Holbrook NM, Putz FE (1990) Seed germination and seedling distribution of Ficus pertusa and F. tuerckheimii: are strangler Figs autotoxic? Biotropica 22: 425-428.

Wester DB (1992) Viewpoint: replication, randomization, and statistics in range research. J. Range Manag. 45: 285-290.

Zar J (1996) Biostatistical analysis. Prentice Hall. Englewood Cliffs, NJ. USA. 662 pp.

Zucker EL, Clarke MR, Glander KE, Scott Jr. NJ (1996) Sizes of home ranges and howling monkey groups at hacienda La Pacífica, Costa Rica: 1972-1991. Brenesia 45-46: 153-156.

Zuidema PA, Sayer JA, Dijkman W (1996) Forest fragmentation and biodiversity: the case for intermediate-sized conservation areas. Environ. Cons. 23: 290-297.