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- POPULATION DENSITY OF “Varecia Variegata”
- Patricia C. Wright, Vololontiana R. Razafindratsita, Sharon T. PochroN, Jukka Jernvall The Key to Madagascar Frugivores Abstract. In the Malagasy ecosystem one particular animal group, lemurs, have the greatest biomass and species richness of frugivores. The peak fruit production in the Malagasy rain forests is about three months shorter compared to peak fruit production in the Amazon and the African rain forests. This suggests that the environment in Madagascar has more well-defined constraints than other continental areas with primates. In Ranomafana National Park, both the overall number of trees, and the number of tree species producing fruit drops during winter months. Particularly in large-bodied lemurs such as sifakas, drop in fruit availability corresponds to an increase in leaf eating. In addition to dietary shifts, all lemur species appear to be able to deal with the season of scarce fruit availability by conserving energy. Extreme responses to winter season are seen in small-bodied lemurs which go into hibernation up to six months every year. Unlike many primate communities in other continents, lemurs do not have synchronous birth peaks across species. In Ranomafana sympatric lemurs show that while individuals within a species have synchronized births, across species lemurs have synchronized weaning. The weaning synchrony coincides with maximum fruit availability and production of small fruits peaks when small juvenile lemurs begin to forage independently. These patterns suggest that lemurs do not appear to rely on fruits to carry them over the period of food scarcity as would be expected from classical descriptions of keystone resources. Rather, we propose that lemurs as a guild rely on fruits as a keystone resource during the warm, wet months in order for lactation and weaning to succeed. Many of the fruit tree species used by lemurs are also hardwood species favored by selective loggers. While loss of these key fruit trees may not drive lemurs into extinction immediately, it may adversely affect reproductive success years after logging. Key Words: Frugivory, weaning synchrony, color vision, Ranomafana National Park, Madagascar. INTRODUCTION Madagascar, the fourth largest island in the world, rifted from Africa more than 150 million years ago, and has been isolated in its present position for over 88 million years (Krause, 1997). Over 1500 km long, Madagascar supports as rich and varied a flora as can be found anywhere in the tropics (Schatz et al., 2002), including rain forest, dry subtropical forest and spiny desert. Botanists surveying 3 one ha plots in the Ranomafana National Park (RNP) rain forests have found 37 families and 105 species of trees (Schatz and Malcomber in Wright, 1997a). These RNP plots were not as diverse as one ha plots in Colombia (with 44 families and 197 species), but were still more diverse than an African lowland forest in Gabon (29 families and 99 species) (Gentry, 1993; Reitsma, 1988). Many animal taxa are absent from Madagascar because of biogeographical history and ungulates, monkeys, many birds, and many bats simply never reached the island. What effect does this absence have on the ecology of the rain forest? In most rain forests the primary pollinators and seed dispersers are insects, birds and bats (Bawa et al., 1990; Fleming et al., 1987,). Terborgh (1986) estimated that as much as 80% of Amazonia’s mammalian biomass depends on fruit resources. As pointed out by Fleming et al. (1987), in contrast, in Madagascar 68% of the birds are insectivores and only 8% are frugivores. The only avian seed dispersers in the rain forest are the velvet asity (Philepitta castanea) in the understory and the Madagascar bulbul (Hypsipetes madagascariensis) in the canopy (Langrand, 1990; Razafindratsita, 1995). Four bird species are nectivores and pollinators. Two species of parrots and several species of pigeons are seed predators. Bats are also relatively depauperate in diversity with 28 species, and almost all are insectivorous (Peterson et al., 1995). Lemurs may be the primary pollinators and seed dispersers in the rain forests of Madagascar (Balko, 1998; Kress et al., 1992; Nilsson et al., 1993; Overdorff, 1992; Ratsimbazafy, 2002; Wright & Martin, 1995). Black and white ruffed lemurs, red-bellied lemurs and brown lemurs, medium sized (2-4kg) diurnal, diurnal primates pass vine and tree seeds intact, and these sprout faster and with less mortality than seeds not passed through a primate gut (Dew & Wright, 1998). Indeed, in the Malagasy ecosystem it is actually possible to single out one particular animal group, lemurs, which have the greatest biomass of frugivores and may qualify as keystone mutualists (Gilbert, 1980). Almost all lemur taxa eat some fruit but despite this, some fruits such as figs are much rarer in Madagascar than in other tropical forests where they are described as keystone food sources for monkeys (Goodman & Ganzhorn, 1997; Terborgh, 1983). Although in other tropical rain forests, such as Kibale Forest (see Chapman et al., this volume), and BCI (see Milton et al., this volume), long-term phenology data show that fruit production varies greatly for individual trees, there are fruits available in those forests all year (Struhsaker, 1997). And in rain forests such as Manu Park in the Peruvian Amazon, keystone resources such as figs (large-crowned) or nectar (abundant patches) provide food for frugivores during extended periods of fruit scarcity, (Terborgh, 1983; Wright, 1989). Madagascar rain forests, unlike other forests with 12-14 species of sympatric primates, have a much longer period without fruits, up to six months a year (Wright, 1999). These long periods without fruits are reflected in the fact that few lemurs are obligate frugivores (Dew & Wright, 1998; Fleming et al., 1987; Goodman & Ganzhorn, 1997; Overdorff & Strait, 1998; Tattersall, 1982), but nonetheless, fruits, seeds and flowers compose 40-90% of the annual diet of Eulemur, Varecia, Eulemur ssp., Propithecus, Microcebus, Cheirogaleus and perhaps Mirza and Phaner (Atsalis, 1999; Balko, 1998; Ganzhorn & Kappeler, 1996; Ganzhorn et al., 1999; Hemingway, 1996, 1998; Overdorff, 1991, 1993; Overdorff and Strait, 1998; Powzyk, 1997; Wright & Martin, 1995). In this paper we examine fruiting patterns in the rain forest of Madagascar, paying particular attention to the degree of seasonality of fruit production in relation to lemur life history. To understand long term patterns in detail we examine feeding and reproduction in the largest species of lemur (6kg), the Milne Edwards sifaka, Propithecus diadema edwardsi. The feeding behavior of this species is compared with fruit availability in the forest using fruiting phenology of 98 plant species. Finally, we compare fruiting with key life history events among several sympatric lemurs. We propose that for lemurs fruits are keystone foods critical for lactation and reproductive success rather than for survival during harsh years. METHODS Study Site Ranomafana National Park, established in 1991, is 43,500 ha of continuous rain forest located in southeastern Madagascar at 21 16’S latitude and 47 20′E longitude (Wright, 1992, Wright and Andriamihaja, 2002). The park is 25 km from Fianarantsoa and 60 km from the Indian Ocean. Elevations range from 500-1500m within the park, and annual rainfall ranges from 1600-4017 mm (RNP records). Most of the rain falls during the months from December to March. Temperatures range from lows in June-September (4-12C) to highs in December-February from (30-32C). The study groups of sifakas were located in the 5km2 Talatakely study site (TTS) which was selectively logged by hand in 1986-1989. The park contains moist evergreen forest and the canopy height ranges from 18m-25m. Phenology data have also been taken at an unexploited site within the continuous forest of the park 3km south of Talatakely at Vatoharanana (Hemingway, 1996; Overdorff 1991) and a third unexploited site 3km further South at Valohoaka (Balko, 1998). Botanically, RNP is one of the most diverse rain forests in the world (Lowry et al., 1997). This area has had a non-hunting tradition, and impact of human predation on lemurs and viverrids has been minimal over at least the last 50 years (Wright, 1997a). The faunal diversity in Ranomafana National Park (RNP) is high for Madagascar (Wright, 1992, 1997a), with 114 species of birds including six species of raptors, six species of viverrid, and twelve species of primates (Table 1). (Wright 1998; Razafindratsita, 1995). Sifaka biomass estimates were 125kg/km2 (Wright, 1998). Total biomass of primates at this site was 330kg/km2, comparable to terra firme forests in Central Amazon and Lope Reserve in Gabon, but roughly half the primate biomass of the alluvial flood plain forest of Manu, Peru or Kirindy dry forest in western Madagascar (Ganzhorn & Kappeler, 1996; Oates et al., 1990; Peres, 1993; Terborgh, 1983; Wright, 1998). Table 1. Lemur species in the rainforest site of Ranomafana. Lemurs with an annual diet of at least 30% fruits are marked with asterisk. Only one diurnal species, Varecia variegata eats fruits for over 85% of its diet (Balko, 1998; Ratsimbazafy, 2002). Species Body Mass (g) Biomass (kg/km2) Avahi laniger, woolly lemur 900 18 Propithecus edwardsi, Milne Edward’s sifaka* 5800 125 Cheirogaleus major, fat-tailed dwarf lemur* 350 18 Microcebus rufus, rufous mouse lemur* 42 4 Daubentonia madagascarienis, aye-aye* 3500 7 Lepilemur microdon, sportive lemur 970 1.6 Hapalemur griseus, grey gentle lemur 935 20 Hapalemur aureus, golden bamboo lemur 1550 9.6 Hapalemur simus, greater bamboo lemur 2450 12 Eulemur fulvus rufus, brown lemur* 2200 66 Eulemur rubriventer, red bellied lemur* 2000 48 Varecia variegata variegata, ruffed lemur* 3650 9 Fruit Collection and Morphology During the 27 month time period April 1997-June 1999, fruits were collected in the forest by TR, Paul Rasabo, ICTE botanists, and other research assistants. All fleshy fruits from canopy trees, understory trees, bushes and vines were chosen regardless of the animal consumer in order to obtain a quantitative measure of fruit availability. The parent plant was measured as to height, dbh, crown diameter, crown depth and located on a map. In the lab 10 fruits of each plant were weighed on a digital scale, measured with calipers. Color was noted. Then the fleshy aril was removed and seeds were counted, weighed and measured. For analysis the fruits were grouped according to weight. The small fruit category consisted of fruits that weighed 1g. In addition, fruits were grouped into four color categories. “Dark” were black, purple and brown, while the category “red” were red and orange and “light” were white and yellow. The fourth category was “green,” which were green colored ripe fruits, thus excluding green but unripe fruits. Monitoring Fruit Phenology One to three individuals of 98 species (a total of 233 trees) of fruiting trees were chosen. Morphological information including height, dbh, crown diameter, crown depth were taken on each selected tree, bush or vine. The location of each study tree was mapped on the Talatakely trail map. Twice each month from March 1997-February 1999 a botanist and several assistants observed each tree using binoculars to determine if a tree had fruits (ripe and unripe), flowers, or new leaves. A score of 1-5 was given on abundance of each category with five being high abundance. Sifaka Fruit Feeding Patterns Within the same trail system as the phenology trees we have been conducting studies on the behavior and ecology of four adjacent groups of Milne Edward’s sifakas, Propithecus diadema edwardsi since 1986 (Pochron et al., 2004; Pochron & Wright, 2002; Wright, 1995, 1998, 1999). Individuals from these groups were captured with anesthetic darts, weighed, measured and given colored nylon collars for field recognition (Glander et al., 1992; Wright, 1995). The demography and changes in group composition are described in detail by Pochron & Wright (2004) and Wright (1995). For this paper, we examined the proportion of feeding time spent feeding on fruits. One individual sifaka per day was observed from awakening until asleep in the sleep tree for 2 days each month from January 1998-December 1998. During this time all foods eaten were identified, and the number of five-minute samples during which each individual fed was recorded. RESULTS AND DISCUSSION Seasonality in Fruiting and Fruit Feeding Despite the similarity of Madagascar in number of species and number of stems found in tropical forests of other geographic areas (Abraham et al., 1996; Lowry et al., 1997; Sussman & Rakotozafy, 1994) the fruiting patterns in Madagascar contrast with many rain forests (Ganzhorn et al. 1999, Wright, 1999). Madagascar phenology plots, including the data shown in this paper, show a prolonged season of 4-6 months with few trees in fruit (Hemingway, 1995; Overdorff, 1993; Powzyk, 1997; Sauther, 1991). In addition, in Malagasy rain forest many canopy species produce flowers and fruit on prolonged, irregular, asynchronous or alternate year cycles (Hemingway, 1995; Morland, 1991, 1993a,b; Overdorff, 1993; Powzyk, 1997). Figure 1A shows that of the 98 species studied, the number of species that carry fruit cycles between 10 and 50. During the austral winter June-September of 1997 and 1998, the number of fruiting species remained below 25 and 20, respectively. In contrast, the times of abundant fruiting of individual trees (scores 3 to 5) are typically during austral summer (Fig. 1A). Thus Malagasy winters are not only characterized by a drop in the number of trees producing fruit but also a lack of species producing fruits. Figure 1. Phenology of fruit availability in 98 species (A) and a subset of 31 species eaten by sifakas (B) in the rain forest of Ranomafana National Park during April, 1997 to June, 1999. Note how changes in number of fruit species eaten by sifakas track the overall richness of fruiting taxa. Fruit score one represents even one fruit observed in a tree, fruit score two represents up to a quarter of the branches having fruit and score five describes branches having abundant ripe fruits. Months in parenthesis lack data. Compared to Madagascar, where fruit availability is highly seasonal, fruiting occurs throughout the year in other tropical forests such as Kibale Forest, Uganda (Chapman et al., this volume; Struhsaker, 1997), Ketambe, Sumatra (van Schaik, 1986), Manu, Peru (Gentry & Terborgh, 1990; Terborgh, 1983) Gabon (Gautier-Hion et al., 1985), Barro Colorado Island, Panama (Foster, 1982; Milton et al., this volume), Colombia (Stevenson, this volume), Manaus, Brazil (Lovejoy & Bierregaard, 1990), and Maraca, Brazil (Nunes, 1998) with a tendency for slightly lower fruit production in the driest months, usually for a two or three month period. The seasonal cycling of Malagasy fruit diversity (Fig. 1A) is strongly reflected in the diet of Propithecus diadema edwardsi. During 1998, these sifakas ate fruits of 31 species out of the studied 98. Fruiting of the 31 species resembled closely the overall seasonal patterns (Fig. 1B). However, sifakas appear to increase the relative diversity of fruit species consumed during the summer season compared to winter. Roughly 20% of concurrently fruiting species were eaten during the winter while up to 30% were eaten during the summer. This suggests that sifakas are opportunistic frugivores that track the overall fruit richness in the forest. This is further evident when the amount of fruit feeding is examined. In Figure 2 the percentage of fruit feeding minutes is plotted for 1998. Sifakas spend about half of their feeding time on fruits during the summer while the proportion of fruit feeding drops all the way to zero in July (Fig. 2). There is a high turnover of top ranking fruits in the diet among months (from the families Clusiaceae, Myrtaceae, and Lauraceae) implicating again the opportunistic nature of fruit eating in sifakas. The majority of sifakas’ feeding time is spent eating leaves. Figure 2. Distribution of fruit feeding (% of total feeding time) of sifakas during January, 1998 to December, 1998 and phenology of fruit availability Because less than half of the 98 sampled plant species carried fruit in any single month (Fig. 1A), we also examined the overall turnover of fruiting species by calculating cumulative fruiting curves (Fig. 3). Beginning from a fruiting peak when roughly 42% of species carry fruit, in 12 months over 70% of the species have fruited, and in 24 months up to 85% of species have fruited (Fig. 3). These numbers suggest a relatively high turnover rate of fruiting species which suggests that the flexible fruit feeding of sifakas may be a good strategy in a Malagasy forest where species richness and composition of fruiting plants changes through time. Figure 3. Cumulative fruiting curves calculated starting from 1997 and 1998 fruiting peaks. Over 70% of species fruit within a year. Fruit Color and Size Compared to rain forests in Asia, Africa and South America, frugivorous birds and bats are restricted to a few species in Madagascar, and fruit eating mammals are predominantly primate species (Fleming, 1987). With a lower diversity of seed dispersers than other geographic regions, one could expect plants to produce fruits of relatively uniform size and color. For example, extant seed dispersing mammals, bats and birds in Madagascar’s rain forest are smaller in body size than those in African, Asian, and South American forests (Fleagle & Reed, 1995; Godfrey et al., 1997), and smaller fruit size would be expected. Indeed, only 5 out of the 98 species studied in this work had fruits larger than 50g. Color vision capabilities also vary greatly between continental areas. In Asia and Africa primates have excellent color vision (Dominy, 2001). in South America most monkeys have color vision, but are deficient in red wave lengths (Jacobs, 1993), and Madagascar’s lemurs have been shown to be largely devoid of the physiological equipment necessary for color vision (Jacobs, 1993). Indeed, in South America Janson found evidence that monkeys are attracted by the color and size of the fruit (Janson, 1983). Following this line of thinking, we might predict that fruits would be less colorful in Madagascar, where the color vision deficient lemurs are the predominant seed dispersers. Of 87 species with data on fruit morphology, 31 had red-orange, 24 had light (yellow or white), 21 had green, and 11 had dark coloration. This suggests that plants could have coevolutionary relationships with specific seed dispersers or, alternatively, that fruit colors could bear little adaptive significance in Madagascar. At least understory plants with dark fruits, such as Psychotria, may rely on birds as seed dispersers. This is indicated by the fact that the smaller size of dark fruits which have an average weight of 1.52 g compared to 4.2 – 6.7 g average weights of fruits in the other color groups. While all of the fruit color groups have synchronous fruiting through time (Fig. 4), sifakas appear to prefer red-orange fruits over other colors. Sifakas ate 14 (45%) of the red-orange, 8 (33%) of the light, and 8 (38%) of the green species. No dark species were eaten. Figure 4. Fruit color and phenology of fruit availability. Note how all fruit colors fluctuate synchronously in the number of species carrying fruit. This putative fruit color preference in sifakas, fitting the fact that Ranomafana forest has fruits of different colors, is corroborated by recent color discrimination tests showing that some lemurs can distinguish colors quite well (Gosset & Roeder, 2000; Jacobs & Deegan, 1993). One possible explanation is that even with only two classes of cone pigments (dichromatic), their behavioral performance can result from an ability to use signals from rods and cones jointly (Jacobs & Deegan, 1993). Sifakas showed also a slight preference towards larger fruits. Of the fruiting species that had fruits heavier than 1g, 16 (39%) species were eaten by sifakas while 14 (30%) of <1g species were eaten. Species with larger fruits showed earlier seasonal fruiting peaks (Fig. 5). Correlation between large and small fruited species is 0.70 (Spearman rank correlation, P = 0.002) when fruiting of large fruits is shifted one month later. Correlation without temporal correction is 0.44 (P = 0.027) suggesting that there is at least a one month delay in the fruiting peak of species with small fruits (Fig. 5). Figure 5. Fruit size and phenology of fruit availability. Note how species with large fruits peak before species with small fruits. Lemur Response to Scarce Food Periods The seasonal tracking of fruit feeding by sifakas (Figs 1B, 2), which reflects both the diversity and amount of available fruit, indicates that this lemur species is not dependent on fruits for individual survival during the lean season. In the case of sifakas, the drop in fruit feeding corresponds to an increase in leaf eating. In addition to dietary shifts, all lemur species appear to be able to deal with the season of scarce resources by conserving energy (Ganzhorn, 1993; Morland, 1993; Nash, 1998; Schmid, 1998; Schmid & Ganzhorn, 1996; Wright & Martin, 1995). Extreme responses to winter season are seen in small-bodied lemurs. Cheirogaleus spp. go into hibernation for 4-6 months every year (Muller, 1998; Wright & Martin, 1995) and Microcebus also enter torpor for several days at a time (Atsalis, 1999; Fietz, 1998; Schmid, 1998). Lepilemur ruficaudatus has the lowest basal metabolic rate recorded for any folivorous mammal (Schmid & Ganzhorn, 1996). Additional lemur traits that can promote energy conservation are thick insulating fur, increased resting behavior, maintenance of small group size, birth of low-weight infants, and relatively small brain size (Wright, 1999). The seasonal shift in sifaka diet does not, however, indicate that these lemurs are completely able to replace fruits with leaves in terms of energy. Sifakas lose up to 20% of their weight during winter season (Pochron & Wright, 2002, PCS unpubl. data) suggesting that fruits play an important role even in this relatively folivorous lemur. At least 30% of sifaka feeding time is on fruits annually while species of the most frugivorous lemur genera, Eulemur rubriventer and Varecia variegata, spend 70% and 90% of their annual feeding time on fruits, respectively (Balko, 1998; Overdorff, 1991). Varecia, a highly arboreal lemur weighing three to four kg, can be regarded as the only living lemur that is an obligate frugivore. It is also relatively specialized because fruits from five species make up to two thirds of its annual diet (Balko, 1998). This specialized frugivory is reflected in Varecia having large territories and extreme seasonal shifts in territory use (Balko, 1998). However, even Varecia has been reported to survive on leaves after total loss of fruit productivity due to cyclone damage on trees, albeit with a substantial weight loss and lack of reproduction (Ratsimbazafy, 2002; Ratsimbazafy et al., in press). Fruits As Keystone Resources for Reproductive Output Individual lemur species have strict breeding synchrony with a mating season typically lasting less than two weeks (Rasmussen, 1985; Sauther, 1991). This breeding synchrony is triggered by changes in photoperiodicity which makes lemurs uniquely coupled with seasonal changes among primates (Pereira, 1993; van Horn, 1975). Furthermore, in contrast to most primate communities in the Neotropics, Africa, or in Asia (Chapman et al., 1999; Gautier-Hion et al., 1985; Struhsaker, 1997; Terborgh, 1983), lemurs do not have synchronous birth peaks across species. In Ranomafana sympatric lemurs show that while individuals within a species have synchronized births, different species gave birth at different times of year (Wright, 1999, Fig. 6). However, while mating and birth seasons are not synchronized across lemur species, weaning appears to happen in all species during March-April (Fig. 6). Figure 6. Reproductive schedules for 9 of 12 species of the sympatric lemur community at Ranomafana National Park. Note birth asynchrony and weaning synchrony in these rain forest species. Weaning occurs around the end of March. For information about individual species, see Table 1. One effect of the weaning synchrony is that all lemur species lactate during the period of increasing fruit availability (Fig. 7). The smallest lemurs are able to fit their whole breeding cycle into the peak fruiting season while sifakas, the largest of the living lemurs at up to 7kg, lactate for two first months without fruits (Figs 2, 6, 7). It is noteworthy that while lactation is the most energy demanding stage of reproduction (Lee, 1997; Tilden & Oftedal, 1997), sifaka newborns are small relative to their mothers. A newborn sifaka weights around 100g which is less than 2% of the mother’s weight and thus the initial cost of lactation is far less than during the peak fruiting season when the infant is over 15% of mother’s weight (Wright, 1999). The peak lactation synchrony among sympatric lemurs (Fig. 7) suggests that even sifakas, while relatively opportunistic fruit eaters (Figs 1, 2), may rely on fruits as key resources for reproductive success. Figure 7. Percentage of plant species fruiting, lemur species gestating, and lemur species lactating. Note how lactation and fruiting peaks coincide while largest number of lemurs gestate during austral winter months when the fruit availability is low. It is also interesting that bigger fruits peak in abundance prior to smaller fruits in the forest (Fig. 5). The delayed peak richness of small fruits coincides with the beginning of weaning period in lemurs. Weaning marks a nutritional transition, when the infant becomes a juvenile foraging independently and is more vulnerable to the risks of malnutrition, infection and predation (Janson & van Schaik, 1993). For plants this synchrony of weaning produces a population peak of small juvenile lemurs foraging in the forest for fruits, effectively resulting in a peak of seed dispersers. Even bamboo-eating lemurs (genus Hapalemur) follow the weaning synchrony and include small amounts of fruit to their diet during the summer fruiting season (Tan, 1999; Grassi, 2001). The peak fruit production in the Malagasy rain forest is three months shorter on average compared to peak fruit production in the Amazon forest (Stevenson, this volume; Terborgh, 1983; Wright, 1997b), and the African forest (Chapman, this volume; Gautier -Hion et al., 1985; Struhsaker, 1997). This suggests that the environment in Madagascar has more well-defined constraints than other continental areas where primates have evolved. In this respect it is informative that lemurs do not appear to rely on fruits to carry them over the period of fruit scarcity as would be expected from classical descriptions of keystone resources (Terborgh, 1983). Soil fertility overall in Madagascar is low, often lower than in other primate habitats on other continents (Ganzhorn et al., 1999). Smith and Ganzhorn (1996) compared lemurs and Australian marsupials, suggesting that both radiations were strongly influenced by these restricting environmental factors that contrast with many tropical habitats in South America, Africa and mainland Asia. Thus, even if lemur taxa had evolved to use classical keystone resources to survive winter seasons, the harsher environmental constraints of Madagascar may have weeded them out. In conclusion, the data presented in this paper suggest that lemurs as a guild rely on fruits as a keystone resource during the warm, wet months in order for lactation and weaning to succeed. It is important to note that many of the fleshy-fruited plant species used by lemurs are also hardwood species favored by selective loggers. While loss of key fruit trees may not drive lemurs into extinction immediately, it may adversely affect reproductive success years after logging (Pochron et al., 2004). This kind of "extinction debt" might remain unnoticed if "keystone resource" is considered in forest management and reserve planning only in the narrow sense. Thus keystone resources are probably not just the ones that help ecologically important animal guilds survive a bad season. ACKNOWLEDGEMENTS In Madagascar we would like to thank the National Association for the Management of protected Areas (ANGAP), Department of Water and Forests, and the Minister of the Environment. We also thank Benjamin Andriamihaja and the MICET and ICTE staff who expedite the research process and have made our long-term work in Madagascar possible. We acknowledge the David and Lucile Packard Foundation, Douroucouli Foundation, the Wenner-Gren Foundation, the John D. and Catherine T. MacArthur Foundation, National Geographic Society, National Science Foundation USA, Earthwatch Institute, and SUNY-Stony Brook. We would also like to acknowledge Paul Rasabo, the late George Rakotonirina, Remi Rakotovao, Raymond Ratsimbazafy, Pierre Talata, and Albert Telo for their expert assistance following animals and collecting phenological data. Our thanks to Ted Stiles who inspired this project and assisted with setting up the methods. References Abraham, J-P., Rakotonirina, B., Randrianasolo, M., Ganzhorn, J.U., Jeannoda, V., Leigh, E.G., Jr (1996). Tree diversity on small plots in Madagascar: a preliminary review. Rev. Ecol. 51:93-117. Atsalis, S. (1999). Diet of the brown mouse lemur (Microcebus rufuss) in Ranomafana National Park, Madagascar. Int. J. Primatol. 20: 193-229. Balko, E.A., (1998). 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Making a rain forest national park work in Madagascar: Ranomafana National Park and its long-term research commitment. In J. Terborgh, C .van Schaik. M. Rao and L. Davenport (eds): Making Parks Work: Strategies for Preserving Tropical Nature California: Island Press, pp. 112-136. Dept of Anthropology, SUNY, Stony Brook, Stony Brook, New York, USA; Institute for the Conservation of Tropical Environments, SUNY Stony Brook, Stony Brook, New York, USA; Centre VALBIO, Ranomafana National Park, Madagascar; Institute for the Conservation of Tropical Environments, Antananarivo 101, Madagascar and Centre VALBIO, Ranomafana National Park, Madagascar; Department of Anthropology, SUNY, Stony Brook, Stony Brook, New York, USA; Institute of Biotechnology, University of Helsinki, Helsinki, Finland
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