Info

1999; Powzyk and Mowry, 2003). Varecia stands out as the only lemur that eats fruits for about 90% of its diet (Balko, 1998; Vasey, 2004, 2005; Balko and Underwood, 2005). The evolution of three species of bamboo specialists (Tan,

1999) and many nocturnal leaf specialists (Ganzhorn, 1993; Warren and Crompton, 1997; Thalmann, 2001) may be a direct result of the adaptations of lemurs to these long periods of fruit scarcity (Wright, 1999). And this in turn may influence other traits such as unusually low metabolic rates of these primates (Ganzhorn, 1993; Schmid, 1998b; Pereira et al., 1999; Schmid and Speakman,

Propithecus edwardsi Eulemur fulvus rufus Eulemur rubriventer Varecia variegata Hapalemur griseus Hapalemur simus Hapalemur aureus Cheirogaleus major Microcebus rufus

12 1 23456789 101112 1 23 Month

Figure 2. In Ranomafana National Park, the percentage of plant species fruiting, lemur species gestating, and lemur species lactating over a 2-year period. Note how lactation and fruiting peaks coincide. (Adapted from Wright et al., 2005a.)

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 (Sussman and Rakotozafy, 1994; Abraham et al., 1996; Lowry et al., 1997), the fruiting patterns in Madagascar contrast with many rainforests (Ganzhorn et al., 1999; Wright, 1999; Wright et al., 2005a). Madagascar phenology plots in the eastern humid forest show a prolonged season of 4-6 months with few trees in fruit (Sauther, 1991; Overdorff, 1993; Hemingway, 1995; Powzyk, 1997). In addition, in Malagasy rainforest many canopy species produce flowers and fruit on irregular, asynchronous, or alternate year cycles (Morland, 1993a; Overdorff, 1993; Hemingway, 1995; Powzyk, 1997). A phenology study of 98 rainforest tree species showed that the number of species that carried fruit varied between 10 and 50 (Wright et al., 2005a). In fact, during the austral winter June-September of 1997 and 1998, the number of fruiting species remained below 25 and 20, respectively (Wright et al., 2005a). In contrast, the times of abundant fruiting of individual trees are typically during austral summer (Figure 1). 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.

In this study of rainforest tree phenology less than half of the 98 sampled plant species carried fruit in any single month, and the overall turnover of fruiting species calculated by cumulative fruiting curves showed 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 (Wright et al., 2005a). These numbers suggest a relatively high turnover rate of fruiting species which suggests that the flexible fruit feeding of most lemurs may be a good strategy in a Malagasy forest where species richness and composition of fruiting plants changes through time.

The seasonal cycling of Malagasy rainforest fruit diversity is strongly reflected in the diet of Propithecus edwardsi. During an annual cycle, these sifakas ate fruits

12 1 23456789 101112 1 23 Month

Figure 2. In Ranomafana National Park, the percentage of plant species fruiting, lemur species gestating, and lemur species lactating over a 2-year period. Note how lactation and fruiting peaks coincide. (Adapted from Wright et al., 2005a.)

of 31 out of the 98 species studied (Wright et al., 2005a). Fruiting of the 31 species resembled closely the overall seasonal patterns. 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. In Figure 3 the percentage of fruit feeding minutes is plotted for one annual cycle. Sifakas spend about half of their feeding time on fruits during the summer while the proportion of fruit feeding drops to zero in July (Figure 3). The majority of sifakas' feeding time is spent eating leaves.

In contrast, in this same rainforest habitat, Varecia variegata specialized on a few species of fruits each month, and ranged widely to find these fruiting trees (Balko and Underwood, 2005). In fact, over an annual cycle the majority of feeding minutes was on four tree species at one site and two tree species at another (Balko and Underwood, 2005). Balko also found that the fruiting phenology was tied to patterns and distribution of rainfall with the peak of fruiting occurring after a 4-month period of consistent rainfall including consecutive cyclones in the months prior to the peak. The behavioural response to the lack of fruits during the winter months, is reduction of activity and energy expenditure (Morland, 1993a,b; Balko, 1998; Vasey, 2005).

In the dry western forests, there is a dramatic contrast in rainfall compared with the eastern rainforests. The dry season extends 6-8 months (Sorg and Rohner, 1996; Scholz and Kappeler, 2004). At Kirindy Forest there are 8 months with no rain, with a total annual rainfall of 800 mm (Scholz and Kappeler, 2004). The Beza Mahafaly Reserve and Berenty Reserve have less than 500 mm annual

Month

Figure 3. Fruit productivity and lemur lactation and gestation of 12 species over a 2-year period in Ranomafana National Park. (Adapted from Wright et al., 2005a,b.)

Month

Figure 3. Fruit productivity and lemur lactation and gestation of 12 species over a 2-year period in Ranomafana National Park. (Adapted from Wright et al., 2005a,b.)

rainfall, and potentially throughout the south, droughts occur about once every 10 years (Gould et al., 1999; Jolly and Pride, 1999; Richard et al., 2002).

Lemur Response to Scarce Food Periods

Many lemurs respond to scarce fruits by eating more leaves. For example, Propithecus edwardsi, Eulemur fulvus rufus, and Eulemur rubriventer replace fruit feeding by increasing leaf eating (Overdorff, 1993). 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. Propithecus edwardsi lose up to 20% of their weight during winter season (Pochron and Wright, 2002; Wright et al., 2005a) 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 (Overdorff, 1991; Balko, 1998; Balko and Underwood, 2005). Varecia, a highly arboreal lemur weighing 3 to 4 kg, can be regarded as the only diurnal 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 and Underwood, 2005). This specialized frugivory is reflected in Varecia having large territories and extreme seasonal shifts in territory use (Balko and Underwood, 2005). 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.

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, 1993b; Wright and Martin, 1995; Schmid and Ganzhorn, 1996; Warren and Crompton, 1997; Nash, 1998; Schmid, 1998a,b; Thalmann, 2001). Extreme responses to winter season are seen in small-bodied lemurs. Cheirogaleus spp. go into hibernation for 4-6 months every year (Wright and Martin, 1995; Schmid, 1998a; Fietz and Ganzhorn, 1999; Dausmann et al., 2004) and Microcebus also enter torpor for several days at a time (Fietz, 1998; Schmid, 1998b; Atsalis, 1999). Lepilemur ruficaudatus has the lowest basal metabolic rate recorded for any folivorous mammal (Schmid and 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).

Fruits as Keystone Resources for Reproductive Output

Individual lemur species have strict breeding synchrony with a mating season typically lasting less than 2 weeks (Rasmussen, 1985; Sauther, 1991, 1998). This breeding synchrony is triggered by changes in photoperiodicity which makes lemurs among primates uniquely coupled with seasonal changes (van Horn, 1975; Pereira, 1993). Furthermore, in contrast to most primate communities in the Neotropics, Africa, or Asia (Terborgh, 1983; Gautier-Hion et al., 1985; Struhsaker, 1997; Chapman et al., 1999), 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 the year (Wright, 1999; Wright et al., 2005a). However, while mating and birth seasons are not synchronized across lemur species, weaning appears to happen in all species during March-April (Wright, 1999; Wright et al., 2005a) in the rainforest.

One effect of the weaning synchrony is that all lemur species lactate during the period of increasing fruit availability (Figure 3). The smallest lemurs are able to fit their whole breeding cycle into the peak fruiting season, whereas sifakas, the largest of the living lemurs, lactate for the first 2 months without fruits. It is noteworthy that while lactation is the most energy-demanding stage of reproduction (Lee, 1997; Tilden and Oftedal, 1997), lemur newborns are small relative to their mothers. A newborn sifaka weighs around 100 g which is less than 2% of the mother's weight. Therefore, the initial cost of lactation is far less than during the peak fruiting season when the infant is 15-22% of the mother's weight (Wright, 1999). This will allow the infants to find abundant fruits, when the inexperienced forager needs to gain weight by eating large quantities of this abundant resource. The peak lactation synchrony among sympatric lemurs suggests that even sifakas, while relatively opportunistic fruit eaters, may rely on fruits as key resources for reproductive success. A close relationship between tree phenology and lemur reproductive success has also been found in the dry forest areas (Sauther, 1991, 1998; Gould et al., 2003).

Was this article helpful?

0 0
How To Bolster Your Immune System

How To Bolster Your Immune System

All Natural Immune Boosters Proven To Fight Infection, Disease And More. Discover A Natural, Safe Effective Way To Boost Your Immune System Using Ingredients From Your Kitchen Cupboard. The only common sense, no holds barred guide to hit the market today no gimmicks, no pills, just old fashioned common sense remedies to cure colds, influenza, viral infections and more.

Get My Free Audio Book


Post a comment