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International Journal of Primatology

, Volume 39, Issue 3, pp 377–396 | Cite as

Predictions of Seed Shadows Generated by Common Brown Lemurs (Eulemur fulvus) and Their Relationship to Seasonal Behavioral Strategies

  • Hiroki SatoEmail author
Article

Abstract

Frugivorous primates in the family Lemuridae, the largest seed dispersers in Madagascar, often modify their behavior dramatically to cope with seasonal fluctuations in food availability and climate. Such behavioral strategies influence seed dispersal distances and seed shadows, which determine seed fate, gene flow, and the geographical range expansion of plant populations. To examine seasonal variation in seed shadows generated by the common brown lemur (Eulemur fulvus), I combined data on movements of a wild group of lemurs in northwestern Madagascar from full-day observations made twice weekly for 1 year and full-night observations made once a fortnight during the dry season, with gut passage times for three captive individuals in a Malagasy zoo. During the rainy season, brown lemurs increased traveling effort (mean daily path lengths: 1172 ± SE 59 m), adopting a high-cost/high-yield foraging strategy to maximize harvest under periods of fruit abundance; this resulted in long seed dispersal distances (median: 170 ± MAD 77 m). During the dry season, daily path lengths (mean: 469 ± SE 30 m) were shorter owing to midday resting and consumption of water-rich succulent leaves, probably to avoid overheating and dehydration. These behaviors led to short-distance seed dispersal (median: 75 ± MAD 47 m). Although brown lemurs moved nocturnally during the dry season (mean nightly path lengths: 304 ± SE 58 m), nocturnal seed dispersal distances were short (median: 34 ± MAD 21 m). This seasonal variation in seed shadows might cause different population dynamics for rainy- and dry-season-fruiting species of large-seeded plants that depend on brown lemurs for seed dispersal. Additionally, lemur-facilitated seed dispersal distances were shorter than those of large frugivores elsewhere in the world. Therefore, lemur-mediated seed dispersal systems are likely to be vulnerable to forest fragmentation, which can isolate new recruits and prevent gene flow among plant metapopulations.

Keywords

Large frugivores Madagascar Movement patterns Seasonality Seed dispersal distance 

Introduction

Seed dispersal at a local scale can improve seed survival rates via transport away from dangerous zones of high density-dependent mortality near the mother plant (Comita et al. 2014; Connell 1971; Howe and Smallwood 1982; Janzen 1970). On large spatial scales, new recruitment via long-distance dispersal can facilitate the colonization of new habitats and the spread of a plant population, although the fate of seeds will largely depend on the context of the environments in which they are deposited (Cain et al. 2000; Nathan 2006). Therefore, a seed shadow—the frequency distribution of seed dispersal distances— logically determines the gene flow, spread rate, and colonization ability of plant populations (Higgins and Richardson 1999; Loiselle et al. 1995), and influences the species diversity and structure of plant communities and ecosystems (Levin et al. 2003; Nathan and Muller-Landau 2000). The analysis of animal-mediated seed shadows is important in evaluating seed disperser effectiveness in zoochorous systems (Schupp et al. 2010; Spiegel and Nathan 2007).

The shapes and scales of seed shadows vary widely among seed dispersers owing to the distinctive movement patterns, home range sizes, and gut passage times of different animal species (e.g., Fuzessy et al. 2017). Even in a specific animal species, seed shadow patterns vary with sex-specific behavior (Koike et al. 2011; Nakashima and Sukor 2010), time of day (Russo et al. 2006; Westcott et al. 2005), and years (Koike et al. 2011; Tsuji and Morimoto 2016). Several previous studies have explained the seasonal dynamics of animal-generated seed shadows based on foraging strategies developed around seasonal changes in the availability and distribution of resources. For example, tamarins (Saguinus spp.: Culot et al. 2010) and woolly monkeys (Lagothrix lagotricha: Stevenson 2000) disperse seeds further during periods of fruit abundance or high fruit diversity than they do during periods of fruit scarcity. This mechanism can be explained by a high-cost/high-yield strategy, in which animals increase their traveling efforts to maximize the harvest of patchily distributed food during periods of abundance (Agetsuma and Nakagawa 1998; Harrison 1985). In other cases, when animals visit a few widely scattered important resources, their seed shadows extend the tails of the probability distributions representing long-distance dispersal events. For example, long-range travel by Asian elephants (Elephas maximus) to scattered water holes increases long-distance dispersal events during the dry season (Campos-Arceiz et al. 2008). As many plant species bear fruits seasonally, the study of seasonal dynamics in animal-mediated seed shadows contributes to our understanding of the distance-dependent seed dispersal effectiveness (i.e., the product of the distance-dependent number of seeds dispersed and the distance-dependent probability of survival: see Schupp et al. 2010; Spiegel and Nathan 2007) of specific seed dispersers in each plant species.

Forest ecosystems in Madagascar lack large-bodied frugivores because of geographical isolation, which precludes immigration of animals from other continents (Bollen et al. 2004; Federman et al. 2016; Fleming et al. 1987) and the recent extinction of megafauna including large-bodied primates due to human activities (Crowley et al. 2011; Godfrey et al. 2008). Within the strikingly depauperate frugivorous guilds, members of Lemuridae, as the sole large-bodied frugivores >1500 g in body mass, play a vital role in seed dispersal, particularly for large-seeded plants (Bollen et al. 2004; Ganzhorn et al. 1999; Razafindratsima 2014; Sato 2012a, 2013; Wright et al. 2011). Therefore, an analysis of seed dispersal distances and seed shadows generated by Lemuridae will enhance our understanding of the spatial patterns and regeneration systems of large-seeded Malagasy plants (Moses and Semple 2011; Razafindratsima et al. 2014).

The climate of Madagascar—especially in the western region, which is characterized by dry and rainy seasons influenced by tropical monsoons (Jury 2003)— causes seasonal dynamics in the behavioral strategies of frugivorous lemurs in terms of activity patterns (e.g., Donati et al. 2009; Vasey 2005) and dietary modifications (e.g., Sato et al. 2016; Vasey 2000; Yamashita 2008). The common brown lemur (Eulemur fulvus, Lemuridae), the largest seed disperser in western Madagascar (Sato 2012a, 2013), changes its activity (Sato 2012b) and feeding patterns (Sato et al. 2014) seasonally in Ankarafantsika National Park, northwestern Madagascar. Brown lemurs rest at midday during the dry season, whereas they are active throughout the daytime during the rainy season (Sato 2012b). This midday rest correlates with high diurnal temperature and low water availability, which has been interpreted as a possible behavioral reaction to avoid overheating and minimize water loss via excessive evaporative respiration under heat stress and water scarcity (Sato 2012b). Brown lemurs mainly consume diverse fruits during the rainy season (Sato 2013; Sato et al. 2014). During the dry season, brown lemurs drastically increase folivory on a succulent herbal species, Lissochilus rutenbergianus, probably for rehydration under drought conditions (Sato 2013; Sato et al. 2014). In addition, brown lemurs living in dry deciduous forests in western Madagascar tend to become cathemeral (active during both the day and night) during the dry season, while being diurnally active during the rainy season (Rasmussen 1999). However, nightly path lengths are shorter than daily path lengths (Rasmussen 1999).

Following previous findings on seasonal dynamics in ranging patterns and seed shadows generated by animals (Campos-Arceiz et al. 2008; Culot et al. 2010; Stevenson 2000), I hypothesized that the behavioral strategies of brown lemurs cause seasonal variation in the daily path lengths and the corresponding seed dispersal distances and seed shadows. I modeled the seed shadows produced by brown lemurs based on gut passage time and movement pattern data, and I compared those patterns between the rainy and dry seasons to test the following predictions. I predicted that daily resting time during the dry season will negatively affect daily path lengths seasonally. Moreover, since Lissochilus rutenbergianus is commonly distributed on the forest floor throughout the year (Sato et al. 2014), brown lemurs will decrease their traveling efforts with increased consumption of this herb during the dry season. In contrast, during the rainy season, highly frugivorous diets are linked to long-distance travel to acquire fruit resources that are scattered spatiotemporally (i.e., high-cost/high-yield strategy). As a consequence of those seasonal ranging patterns, I predicted that brown lemurs would generate seed shadows with a higher probability of long-distance seed dispersal during the rainy season than the dry season.

I also hypothesized that the cathemeral activities of brown lemurs will characterize the pattern of seed shadows created at night during the dry season. I modeled the seed shadows generated at night by brown lemurs and compared it with the seed shadows in daytime during the dry season. I predicted that seed dispersal distances would be shorter at night than during the daytime, even if brown lemurs would frequently disperse seeds outside the crown areas of mother trees (>20 m in seed dispersal distances).

Methods

Study Site and Subjects

The study site was in Ankarafantsika National Park, northwestern Madagascar. I conducted surveys in the Jardin Botanique A, the rectangular trail system, at Ampijoroa Forest Station (16°31′S, 46°82′E) in a primary dry deciduous forest. During the study period (December 2006–November 2007) the hourly mean temperature was 26.1 ± SD 4.8 °C, and most rainfall occurred during the rainy season (November–April: 1653.0 mm). It rarely rained during the dry season (May–October: 6.8 mm).

The focal group consisted of 12 individuals (6 adult males, 3 adult females, 1 subadult male, and 2 young females). I captured an adult male at the beginning of November 2006 using a blowpipe and injection darts containing 30 mg of ketamine hydrochloride, and placed a radio collar (M1920, 35 g weight; Advanced Telemetry Systems, Inc., Isanti, MN, USA) on this individual for tracking and observation. After 1 mo of habituation to the presence of an observer, I followed the group from December 2006 through November 2007. I have previously reported resting and feeding patterns for the same study group (Sato 2012b, 2013; Sato et al. 2014). I conducted full-day observations (06:00–18:00 h) twice weekly for 1 year (101 observation days, 1212 h). I recorded the activity engaged in by the majority of visible members at 1-min intervals and classified it into four behavioral categories: resting, feeding, traveling, and other (Sato 2012b). During the scans of group feeding activity, I recorded the food items eaten in seven categories: fruits, flowers, mature leaves, new leaves, succulent leaves of Lissochilus rutenbergianus, other, and unknown (Sato et al. 2014).

Because brown lemurs at Ankarafantsika are active during both day and night during the dry season (Rasmussen 1999), I conducted full-night observations (18:00 − 06:00 h) once a fortnight during the dry season (13 observation nights, 156 h). During nocturnal observation, I observed lemurs with the aid of a headlamp and a hand-held flashlight covered with red cellophane to avoid disturbing the nocturnal primates (Charles-Dominique and Bearder 1979). I characterized the group’s nocturnal activities into four behavioral categories (resting, feeding, traveling, and other) using auditory group sampling methods (Andrews and Birkinshaw 1998) because of the difficulty involved in detailed visual observation of the activities. During auditory sampling, I judged feeding activity to be occurring if food fragments fell to the ground, or if I heard chewing noises (Andrews and Birkinshaw 1998; Sato et al. 2014).

Measurement of Path Length

I measured the location of the group using a Global Positioning System (GPS) device (eTrex Vista; Garmin International, Olathe, KS, USA) at 5-min intervals (accuracy: 5–20 m). When the group stayed at the same location for >10 min (over two measurement points), I used the first GPS data for analysis to minimize the effects of measurement errors in GPS data at the same locations. I collected 3929 first GPS points corresponding to 14,354 location points at 5-min intervals among a potential 14,645 points during the 101 full-day observations. I was unable to measure the remaining 291 points (1.99%) when I could not locate the focal group until 06:00 h or continue to observe them until 18:00 h, or when I lost the lemurs during the observation period. I calculated the daily and nightly path lengths using the QGIS 2.8.1 distance-matrix tool with 5-min interval GPS data during each observation.

Modeling of Seed Shadows

To model the seed shadows generated by brown lemurs, I used data on gut passage time reported by Sato (2009) following the methods of Lambert (2002). I measured the gut passage time of three captive brown lemurs (one male and two females) at the Tsimbazaza Botanical and Zoological Park in Antananarivo, Madagascar (Sato 2009). In an experimental session, I provided 150 g of three fruit species (Opuntia vulgaris, Passiflora edulis, and Vitis sp.), including 240–535 small seeds (seed length < 7 mm; seed width < 5 mm), to individual lemurs and measured the elapsed time from consumption to defecation for each seed. I conducted two sessions for each individual, and then took an arithmetic mean of the results of six sessions (Fig. 1). The lemurs started to eliminate the ingested seeds 72 min after the feeding and continued until 7 h later (Sato 2009). Although my modeling of seed shadows did not consider the potential effects of seed size and dietary fiber content on gut passage time, this influence should be considered when interpreting the results. Previous studies have noted that high fiber content hastens gut passage time (Schmidt et al. 2005), but no effects of particle size have been observed for Eulemur (Campbell et al. 2004; Sato 2009).
Fig. 1

Gut passage time of seeds swallowed by brown lemurs (Eulemur fulvus) captive in Tsimbazaza Botanical and Zoological Park in Antananarivo, Madagascar in February and March 2006. This figure is modified from Fig. 1b in Sato (2009).

Given that brown lemurs generally eliminated the ingested seeds by 7 h after feeding, I followed the dispersal of seeds ingested from 06:00 to 11:00 h during the full-day observations or from 18:00 to 23:00 h during the full-night observations. Thus, I set the starting points for estimating seed shadows as the locations where feeding bouts on fruits occurred during the above time periods. I defined a feeding bout as a period in which the group fed on a fruit item at a feeding patch.

I predicted the seed shadows from these feed patch starting points by combining data for brown lemur movement and gut passage time following the methods of Holbrook and Smith (2000). Using the QGIS 2.8.1 distance-matrix tool, I measured the direct distances from the location of each feeding bout to subsequent GPS points at 5-min intervals until 7 h later (84 distances for each starting point). Then, I calculated the means of six distances for every 30-min interval until 7 h later. I summed the probability of seed deposition (P) within each distance category (d) in 20-m intervals over all time intervals to yield the seed shadow:
$$ {P}_d={\sum}_t\ \left({A}_{dt}\times {B}_t\right) $$
where A is the probability of a lemur being a particular distance category (d) from the starting point at t min later, t varies in 30-min intervals between 30 and 420 min, and B is the probability of a lemur depositing a seed at t min later from the feeding bout.

Data Analysis

Path length data consisted of continuous nonnegative values, and the datasets were mainly nonnormal (Shapiro–Wilk normality test: daily path length for the year, N = 101, W = 0.94, P < 0.001; daily path length during the dry season, N = 52, W = 0.94, P = 0.012; nightly path length during the dry season, N = 13, W = 0.75, P = 0.002; daily path length during the rainy season, N = 49, W = 0.98, P = 0.67). Therefore, I ran generalized linear models (GLMs) with a gamma distribution and log-link function (see also Tsuji and Morimoto 2016) to compare path lengths between the two seasons or between day and night. To examine the relationships between daily path lengths and the seasonal behavioral strategies of brown lemurs, I ran a GLM treating daily path length as a dependent variable and daily resting time (mean = 449.0 ± SD 88.5 scans, range = 169–630 scans, N = 101; Sato 2012b), proportions of fruit consumption (mean = 0.72 ± SD 0.27, range = 0.03–1.00, N = 101), and succulent leaf consumption (mean = 0.12 ± SD 0.24, range = 0.00–0.85, N = 101) during the daily feeding time (Sato 2013; Sato et al. 2014) as independent variables. Collinearity was not severe for any pair of independent variables; the maximum variance inflation factor (VIF = 2.25; between the proportions of fruit consumption and succulent leaf consumption) was smaller than the cutoff value (= 5) recommended by Kutner et al. (2004). In these GLM analyses, I treated the number of locational points as an offset term to eliminate bias due to missing time during observations.

I compared the direct distances after 3.5 h (the median time of seed dispersal) from the feeding sites between seasons in daytime and between day and night during the dry season using the Mann–Whitney U test because the data were not normally distributed (Shapiro-Wilk normality test: data for the day during the rainy season, N = 227, W = 0.82, P < 0.001; data for the day during the dry season, N = 162, W = 0.90, P < 0.001; data for the night during the dry season, N = 31, W = 0.70, P < 0.001). To compare the shapes of seed shadows between the rainy and dry seasons, or between day and night during the dry season, I used the two-sample Kolmogorov–Smirnov test (see Holbrook and Loiselle 2007). I conducted these statistical analyses using R 3.4.0 (R Foundation for Statistical Computing 2017).

Data Availability

The datasets during and/or analysed during the current study available from the corresponding author on reasonable request.

Ethical Note

The field research complied with the protocols and principles for the Ethical Treatment of Non-Human Primates was approved by the Primate Research Institute of Kyoto University (KUPRI), Japan, and adhered to the legal requirements of Madagascar’s Association Nationale pour la Gestation et Aires Protégées and the research permissions authorized by the Ministére de L’environnement, des Eaux et Forets de Madagascar (N°228 in 2006, N°103 and N°277 in 2007). At the end of this study, I safely removed the radio collar from the male and released the individual back to the focal group. The author declares no conflict of interest.

Results

Lemur Movement

The brown lemurs traveled 810.0 ± 47.8 m (mean ± SE, N = 101) from 06:00 to 18:00 h throughout the year. Their movement patterns varied seasonally (Fig. 2), and the daily path lengths were longer during the rainy season (1172.1 ± SE 59.3 m, N = 49) than during the dry season (468.8 ± SE 29.5 m, N = 52; GLM: t = 11.59, df = 99, P < 0.001). The lemurs traveled farther when the diet was more frugivorous (Table I). By contrast, the lemurs shortened their daily path lengths when they rested longer during the daytime and the proportion of succulent leaf consumption was higher (Table I). At night during the dry season, the nightly path lengths (303.5 ± SE 58.1 m, N = 13) were shorter than the daily path lengths during the dry season (GLM: t = −2.77, df = 63, P = 0.007).
Fig. 2

Monthly variation in the daily path lengths of brown lemurs (Eulemur fulvus) in Ankarafantsika National Park for 101 days from December 2006 to November 2007. N = the number of observation days in each month. Whiskers show the range, boxes the interquartile range, center lines the medians, dots the values that are outside 1.5 times the interquartile range.

Table I

Results of generalized linear model for the effects of resting time and the proportion of fruits and succulent leaves consumed on the daily path lengths of brown lemurs (Eulemur fulvus) in Ankarafantsika National Park for 101 days from December 2006 to November 2007

Explanatory variable

Coefficient ± SE

P value

Resting time

–0.47E-02 ± 0.36E-03

< 0.001

Proportion of frugivory

0.38 ± 0.17

0.027

Proportion of feeding on succulent leaves

−0.96 ± 0.19

< 0.001

Residual deviance = 8.74; df = 97; AIC = 1363.82

Null model: Null deviance = 40.41; df = 100; AIC = 1517.76

Predicted Seed Shadows

From 06:00 to 11:00 h on the observation days, I observed 398 feeding bouts on fruits, i.e., 236 bouts in the rainy season and 162 bouts in the dry season. The lemurs left their starting points immediately during the rainy season (Fig. 3a), but stayed within 100 m even after 5 h and 40 min (Fig. 3b). After 3 h and 30 min from the feeding bouts (the median time of seed dispersal), the lemurs traveled farther from their starting points during the rainy season (185.8 ± SE 9.4 m, N = 227) than during the dry season (83.4 ± SE 5.4 m, N = 162; Mann–Whitney U test: U = 8529, P < 0.001). From 18:00 to 23:00 h on observation nights, I recorded 31 feeding bouts on fruits during the dry season. The lemurs stayed within 50 m (49.2 ± SE 12.1 m) of the starting points until 3 h and 15 min later, and traveled 100.8 ± SE 18.3 m after 6 h and 55 min from the feeding bouts (Fig. 3c). The distances from the starting points after 3 h and 30 min were shorter at night (50.4 ± SE 12.4 m, N = 31) than at daytime during the dry season (Mann–Whitney U test: U = 3425, P = 0.001).
Fig. 3

Mean direct distance from the location where brown lemurs (Eulemur fulvus) fed on fruit to their subsequent locations over 7 h in Ankarafantsika National Park. I set the starting points as the locations where feeding bouts on fruits occurred (a) from 06:00 to 11:00 h during the rainy season for 49 days from December 2006 to April 2007 and in November 2007 (N = 236); (b) from 06:00 to 11:00 h during the dry season for 52 days from May to October 2007 (N = 162); and (c) from 18:00 to 23:00 h during the dry season for 13 nights from May to October 2007 (N = 31).

Based on the seed shadow of the entire year (Fig. 4a), I estimated the median seed dispersal distance to be 124.0 ± median absolute deviation (MAD) 70.0 m (range: 0–1076.6 m; Table II). The patterns of seed shadows differed between the rainy and dry seasons (Kolmogorov–Smirnov: D = 0.41, df = 2, P < 0.001). Based on the seed shadow during the rainy season (Fig. 4b), the median seed dispersal distance was 169.7 ± MAD 77.4 m (range: 0–1076.6 m; Table II), and the lemurs potentially deposited only 3.4% of ingested seeds within 20 m of the mother plants; they dispersed 70.3% of ingested seeds over 100 m away (Table II). The estimated percentage of seeds dispersed over distances of ≥200 m was 38.9%. Based on the seed shadow during the dry season (Fig. 4c), the median seed dispersal distance was 74.5 ± MAD 47.2 m (range: 0–387.6 m; Table II). The lemurs deposited 15.4% of ingested seeds within 20 m of the mother plants, and they dispersed 35.2% of ingested seeds over 100 m away (Table II). Dispersal over distances of 200 m was rare (5.9%). Dispersal over distances of 500 m occurred only in the rainy season (3.2%), and was never recorded during the dry season (0.0%). The differences in seed shadows between day and night during the dry season were significant (Kolmogorov–Smirnov: D = 0.34, df = 2, P = 0.006). I estimated the median seed dispersal distance to be 34.0 ± MAD 20.6 m during night observations in the dry season (range: 0–327.3 m; Fig. 4d). The proportion of seeds dispersed over 100 m (15.7%) was lower than in daytime (35.2%; Table II).
Fig. 4

Predicted seed shadows of seeds ingested at the locations where brown lemurs (Eulemur fulvus) fed on fruit in Ankarafantsika National Park (a) from 06:00 to 11:00 h during the entire year for 101 days from December 2006 to November 2007 (N = 398); (b) from 06:00 to 11:00 h during the rainy season for 49 days from December 2006 to April 2007 and in November 2007 (N = 236); (c) from 06:00 to 11:00 h during the dry season for 52 days from May to October 2007 (N = 162); and (d) from 18:00 to 23:00 h during the dry season for 13 nights from May to October 2007 (N = 31).

Table II

Seed dispersal distance by brown lemurs (Eulemur fulvus) and the proportion of seeds deposited for each category of seed dispersal distance in Ankarafantsika National Park

Season

1 Year

Rainy

Dry

Dry

Time period

Day

Day

Day

Night

Date

Dec 2006–

Dec 2006–

May–Oct

May–Oct

Nov 2007

Apr, Nov 2007

2007

2007

Feeding bouts (N)

398

236

162

31

Seed dispersal distance (m)

 Mean

147.9

191.8

84.5

54.5

 Median

124.0

169.7

74.5

34.0

 Min

0.0

0.0

0.0

0.0

 Max

1076.6

1076.6

387.6

327.3

Probability of deposition (%)

 0 ~ 20 m

8.3

3.4

15.4

26.7

 ~ 100 m

33.3

22.2

49.4

57.6

 ~ 200 m

32.3

34.4

29.3

9.7

 ~ 500 m

23.6

35.7

5.9

5.9

 ~ 1000 m

1.8

3.0

0.0

0.0

 1000 ~ m

0.1

0.2

0.0

0.0

 Unknown

0.6

1.0

0.0

0.0

Discussion

Behavioral Strategies and Seed Shadows of Brown Lemurs

Brown lemurs in Ankarafantsika generated seed shadows with a higher probability of long-distance seed dispersal during the rainy season than during the dry season, as predicted. Brown lemurs traveled shorter distances when they engaged in longer midday rests and fed on succulent leaves than when they included a larger proportion of fruits in their diet. Such seasonal changes in diurnal activities and dietary modification caused seasonal variation in the seed shadows. Moreover, brown lemurs dispersed seeds at night during the dry season but at shorter distances than they did in daytime, as predicted.

Previous studies of activity patterns of Eulemur have shown that reduced day length causes the seasonal midday rest (Curtis et al. 1999; Donati and Borgognini-Tarli 2006; Kappeler and Erkert 2003). However, this mechanism cannot fully explain the findings of this study, because brown lemurs in Ankarafantsika increase their midday rest as temperature increases (Sato 2012b) and decrease daily path lengths from the early to later dry season, even with the extension in day length (Fig. 2: the day was shortest at the end of June). As observed in white-faced capuchins (Cebus capucinus: Campos and Fedigan 2009), I hypothesize that brown lemurs under heat stress and water scarcity reduced their ranging activities as a method of behavioral thermoregulation, and consequently seed dispersal distances decreased during the dry season.

Although no studies have focused on seasonal variation in the seed shadows generated by Malagasy primates, their seasonal ranging patterns have been analyzed in terms of foraging strategies. Collared lemurs (Eulemur collaris) decrease the daily path length during fruit scarcity as an energy-conservation strategy (Campera et al. 2014), whereas blue-eyed black lemurs (E. flavifrons) travel farther to visit patchily distributed fruiting trees during lean periods (Volampeno et al. 2011). Eulemur changes their travel habits to deal with the fluctuating spatiotemporal distributions of fruit resources due to their frugivorous niche and low dietary flexibility (Sato et al. 2016). In contrast, sifakas (Propithecus spp.), generalists with high dietary flexibility (Sato et al. 2016), increase their daily path length while consuming patchily distributed high-quality food (e.g., fruits, seeds, and new leaves), and decrease their daily path length when they modify their diet to low-quality ubiquitous food such as mature leaves during scarcity of high-quality food (Irwin 2008; Meyers and Wright 1993; Norscia et al. 2006). In Ankarafantsika, brown lemurs modified their diet for rehydration (Sato et al. 2014). Although the causes of dietary changes are different, the mechanisms driving seasonal changes in ranging patterns linked to foraging strategies are similar to those of sifakas.

This study confirmed nocturnal seed movements by brown lemurs during the dry season, although the sample size of night observations was small. Insufficient energy intake during the day probably led to nocturnal activities for fruit acquisition (Sato et al. 2014). However, like Rasmussen (1999), I found that brown lemurs traveled shorter distances at night than during the day in the dry season. These nightly path lengths indicate that nocturnal seed dispersal distances were shorter than diurnal ones in the brown lemurs of Ankarafantsika.

At the local scale, brown lemurs tended to deposit ingested seeds near the parent plants during the dry season. This type of clustered seed dispersal is expected to result in high mortality rates and high-density distributions of seedlings (Comita et al. 2014; Julliot 1997; Russo and Augspurger 2004). At larger scales, seed shadows had long tails (>500 m) during the rainy season (3.2%), but not during the dry season (0%). Despite the low frequency of long-distance dispersal events, the benefits in terms of reduced density-dependent mortality from predation and competition, or a rare genotype advantage reducing pathogen infection, allow such events to have disproportionately large impacts on the dynamics of plant populations and communities (Cain et al. 2000; Nathan 2006; Nathan and Muller-Landau 2000). The large-seeded plants that depend on brown lemurs for seed dispersal mostly fruit seasonally (Sato 2013). Therefore, as a consequence of the seasonal variation in seed shadows formed by brown lemurs, I predict that population dynamics will differ between the rainy-season-fruiting and dry-season-fruiting species of large-seeded plants. This prediction assumes that seed shadows are not materially affected by postdispersal processes. However, in practice, the contributions of the primary dispersers are often dramatically modified through the extremely high mortality of dispersed seeds and seedlings through predation, competition, disease, and/or climatic stresses (Balcomb and Chapman 2003; Houle 1998; Rey and Alcantara 2000) and through secondary seed dispersal by insects or rodents (Andresen 1999; Forget and Milleron 1991; Vulinec 2002), including the Malagasy lemur-dispersed tree species, Strychnos madagascariensis (Dausmann et al. 2008), which depends on brown lemurs for primary seed dispersal in Ankarafantsika (Sato 2012a). The postdispersal fates of such large-seeded plants must be examined in future studies.

Comparison of Seed Dispersal Distances by Large Frugivores across the World

Although the shapes of seed shadows created by brown lemurs (leptokurtic shapes with long tails of long-distance dispersal events) are similar to those generated by other large-bodied frugivores (Campos-Arceiz et al. 2008; Holbrook and Smith 2000; Koike et al. 2011; Westcott et al. 2005), the scale of brown lemur seed shadows is much smaller than those of other species. In Africa, Asia, Latin America, and Oceania, large frugivores can carry seeds over several hundred meters to some kilometers (Table III). In addition to the species listed in Table III, Brazilian tapirs (Tapirus terrestris) and Asiatic black bears (Ursus thibetanus) are reported to be long-distance dispersers (Fragoso et al. 2003; Koike et al. 2011). Moreover, despite the lack of measurements of seed dispersal distances, there is little doubt that Asian and African megafrugivores disperse seeds over large spatial scales, i.e., great apes (chimpanzees, Pan troglodytes; gorillas, Gorilla spp.; orangutans, Pongo spp.: McConkey 2018; Poulsen et al. 2001) or very large herbivores (rhinoceroses Rhinocerotidae, African elephants Loxodonta spp.: Campos-Arceiz and Blake 2011; Corlett 2009, 2017). Compared with the animals in these regions, Lemuridae, the largest frugivorous taxon in Madagascar, has much shorter seed dispersal distances (Table III; Moses and Semple 2011; Razafindratsima et al. 2014; this study).
Table III

Summary of seed dispersal distances in large-bodied frugivores in Africa, Asia, Latin America, Oceania, and Madagascar

Region

Species of seed disperser

Seed dispersal distance (m)

Body mass (kg)

Reference

Mean

Maximum

Africa

Black-casqued hornbill (Ceratogymna atrata)

1422–1620

6919

1.4

Holbrook and Smith (2000)

White-thighed hornbill (Ceratogymna cylindricus)

1127–1947

3558–5698

1.0

Holbrook and Smith (2000)

Bonobo (Pan paniscus)

1183a; 777–783b

2995a; 1031–1886b

33.2–45b

aBeaune et al. (2013); bTsuji et al. (2010)

Asia

Asian elephant (Elephas maximus)

1222–2105

3968–5772

2040–4270

Campos-Arceiz et al. (2008)

Malayan tapir (Tapirus indicus)

917–1287

3289

< 350

Campos-Arceiz et al. (2012)

Gibbon (Hylobates muelleri × agilis)

339–431c

720–1300c

5–6.4d

cMcConkey and Chivers (2007); dMcConkey (2000)

Japanese macaque (Macaca fuscata)

270e; 420–486 (median)f

634e; 1261f

6.7–10.5f

eTerakawa et al. (2009); fTsuji and Morimoto (2016)

Common palm civet (Paradoxurus hermaphroditus)

216

> 800

1.7–2.8

Nakashima and Sukor (2010)

Rhesus macaque (Macaca mulatta)

117g

774g

6.8–9.2h

gSengupta et al. (2014); hClarke and O’Neil (1999)

Latin America

Many-banded aracari (Pteroglossus pluricinctus)

560i

< 0.7j

iHolbrook and Loiselle (2007); jHolbrook (2011)

Woolly monkey (Lagothrix lagothricha)

355k; 271–454l

1466k; 362–1106l

5.5–10.2m

kStevenson (2000); lYumoto et al. (1999); mPlavcan and Van Schaik (1997)

White-bellied spider monkey (Ateles bekzebuth)

443

1281

8.5

Link and Di Fiore (2006)

Red howler monkey (Aloutta seniculus)

255n; 218–440l

550n; 288–637l

5.2–9.0m

nJulliot (1996); lYumoto et al. (1999); mPlavcan and Van Schaik (1997)

Tufted capuchin (Cebus apella)

355o

1.8–4.5m

oWehncke and Domínquez (2007); mPlavcan and Van Schaik (1997)

White-throated toucan (Ramphastos tucanus), Channel-billed toucan (Ramphastos vitellinus)

338i

0.4p

iHolbrook and Loiselle (2007); pGaletti (2000)

Black spider monkey (Ateles paniscus)

245q

>1500q

7.0–9.5m

qRusso et al. (2006); mPlavcan and Van Schaik (1997)

Moustached tamarin (Saguinus mystax), Saddle-back tamarin (Saguinus fuscicollis)

239r

656r

0.4–0.6m

rHeymann et al. (2012); mPlavcan and Van Schaik (1997)

White-faced capuchin (Cebus capucinus)

216s

844s

3.0t

sWehncke et al. (2003); tMilton (1984)

Black howler monkey (Alouatta pigra)

126u

439u

6.3–11.6m

uZarate et al. (2014); mPlavcan and Van Schaik (1997)

Mantled howler monkey (Alouatta palliata)

112v

811v

5.6–8.4m

vEstrada and Coates-Estrada (1984); mPlavcan and Van Schaik (1997)

Golden lion tamarin (Leontopithecus rosalia)

105w

858w

0.5m

wLapenta and Procópio-de-Oliveira (2008); mPlavcan and Van Schaik (1997)

Oceania

Southern cassowary (Casuarius casuarius)

336

1473

<76

Westcott et al. (2005)

Madagascar

Black-and-white ruffed lemur (Varecia variegata)

180×; 117y

506×; 630y

2.5–4.8y

xMoses and Semple (2011); yRazafindratsima et al. (2014)

Common brown lemur (Eulemur fulvus)

148; 124 (median)

1077

1.6–2.4z

This study; zSato (unpubl. data)

Red-bellied lemur (Eulemur rubriventer)

120

359

1.6–2.1

Razafindratsima et al. (2014)

Red-fronted brown lemur (Eulemur rufifrons)

96

417

2.2–2.3

Razafindratsima (2014)

Forest landscapes are being rapidly fragmented worldwide (Archard et al. 2002), including in Madagascar (Harper et al. 2007). Such forest fragmentation reduces the population densities of seed dispersers, and seed dispersal and regeneration consequently fail in zoochorous plants, particularly in the mutualistic systems involving large-seeded plants and large-bodied frugivores (Bueno et al. 2013; Cordeiro and Howe 2001; Estrada et al. 2017; Ganzhorn et al. 1999). In terms of seed dispersal distances and seed shadows, forest fragmentation potentially decreases seed-dispersal-mediated connectivity across forest patches, restricting new recruitment and gene flow among meta-populations (Bruna 1999; Cordeiro et al. 2009; Hamilton 1999), particularly for large-seeded plants (Cramer et al. 2007; McEuen and Curran 2004). The capacity to link otherwise isolated habitat patches in fragmented ecosystems differs among animal vectors (Jordano et al. 2007; Santos et al. 1999; Spiegel and Nathan 2007), and lemur-mediated seed dispersal systems have low connectivity (Table III). In a fragmented forest landscape in southern Madagascar, a simulation analysis predicted dramatically decreased connectivity by the ring-tailed lemurs (Lemur catta, Lemuridae) as their seed dispersal distances decreased from 1500 to 500 m (Bodin et al. 2006). Given the shorter empirical seed dispersal distances of brown lemurs in this study and other Lemuridae species (Table III), populations of lemur-dispersed plants must be easily isolated by forest fragmentation, following the predictions of Bodin et al. (2006). In such vulnerable ecological systems, the establishment of habitat corridors may be the best way to enhance seed dispersal by lemurs, helping to maintain gene flow and regenerate plant populations (Gilbert-Norton et al. 2010; Levey et al. 2005; McConkey et al. 2012; Trakhtenbrot et al. 2005).

In conclusion, this study provides two insights into Malagasy zoochorous systems, particularly for the large-seeded plants relying on lemurs. First, this study showed a temporal change in seed shadows of the common brown lemur with respect to behavioral strategies for coping with the remarkable seasonality in western Madagascar. Examining the effects of lemur behavioral strategies on the population dynamics of these plants via seed dispersal requires further analyses of the spatial distribution of individual plants (e.g., Razafindratsima and Dunham 2015; Russo and Augspurger 2004) and gene flow (e.g., Hardesty et al. 2006; Pacheco and Simonetti 2000). Second, I found that lemur seed dispersal distances are shorter than those of other large frugivores worldwide. Conservation management strategies should incorporate the distance-dependent seed dispersal effectiveness of lemurs for mitigating the vulnerable connectivity of zoochorous systems in Malagasy large-seeded plants ensuing from forest fragmentation (e.g., Bodin et al. 2006).

Notes

Acknowledgements

The author is grateful to A. Mori, H. F. Rakotomanana, F. Rakotondraparany, and all members of the Antananarivo-Kyoto University research team for their support in carrying out fieldwork; to G. Yamakoshi, A. Mori, and N. Nakagawa for their research guidance; and to all of the staff at Ankarafantsika National Park and Tsimbazaza Botanical and Zoological Park for giving permission to conduct this research. I thank O. Razafindratsima, Y. Tsuji, and L. Culot for co-organizing the special issue “Advances and Frontiers in Primate Seed Dispersal” in the International Journal of Primatology. I also thank J. M. Setchell, the editor-in-chief, and the three anonymous reviewers for their constructive comments and useful suggestions to improve my manuscript. This work was supported by the Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (Nos. 17405008 and 21-3399).

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Authors and Affiliations

  1. 1.Graduate School of Asian and African Area StudiesKyoto UniverityKyotoJapan

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