Effects of Habitat Quality and Seasonality on Ranging ...

Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments Marco Campera, Valentina Serra, Michela Balestri, Marta Barresi, Murielle Ravaolahy, Faly Randriatafika & Giuseppe Donati International Journal of Primatology The Official Journal of the International Primatological Society ISSN 0164-0291 Int J Primatol DOI 10.1007/s10764-014-9780-6

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Author's personal copy Int J Primatol DOI 10.1007/s10764-014-9780-6

Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments Marco Campera & Valentina Serra & Michela Balestri & Marta Barresi & Murielle Ravaolahy & Faly Randriatafika & Giuseppe Donati

Received: 4 December 2013 / Accepted: 19 March 2014 # Springer Science+Business Media New York 2014

Abstract Degraded forest habitats typically show low fruit availability and scattered fruit tree distribution. This has been shown to force frugivorous primates either to move further in search of food, resulting in large home ranges, or to use energy saving strategies. Malagasy lemurs are known to face pronounced seasonality and resource unpredictability, which is amplified by the overall reduction in food availability due to the human-driven habitat disturbance on the island. To explore lemur flexibility to habitat disturbance, we examined the ranging behavior of collared brown lemurs (Eulemur collaris) in two differently degraded fragments of littoral forest of southeastern Madagascar. We collected data from February 2011 to January 2012 on two groups living in a degraded area and two groups living in a less disturbed forest. We calculated annual ranges, monthly ranges, and daily distance traveled. We then ran repeated measures ANOVAs using seasonality as dichotomous, intrasubject factor and site/group as intersubject nested factors. In the degraded forest, the lemurs had larger monthly ranges, and their annual ranges were either fragmented or characterized by M. Campera : M. Balestri Nocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K. M. Campera : V. Serra : M. Balestri : M. Barresi Department of Biology, University of Pisa, 56126 Pisa, Italy M. Ravaolahy Department of Animal Biology, University of Antananarivo, BP 906 Antananarivo, Madagascar F. Randriatafika QIT Madagascar Minerals, Rio Tinto, BP 225 Tolagnaro, Madagascar G. Donati (*) Nocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K. e-mail: [email protected]

Author's personal copy M. Campera et al.

multiple core areas. They were able to use a habitat mosaic that also included nonforested areas and swamps. In addition, they shortened their daily path length, possibly to preserve energy, and used different areas of their annual home ranges seasonally. Although a number of possible confounding factors may have been responsible for the observed differences between sites, our findings highlight the ranging flexibility of collared brown lemurs in littoral forest fragments. Keywords Collared brown lemur . Fragmentation . Habitat degradation . Home range . Kernel analysis . Madagascar

Introduction Ecological factors such as forest structure, fragmentation, and resource availability are critical in determining the spatial distribution of primates (Boyle et al. 2009; Barton et al. 1992; Chapman 1988; Clutton-Brock 1975; Irwin 2008). Because most habitats are heterogeneous and resources are often clumped, primates do not use their home range evenly (Haskell et al. 2002; Kelley 2013). Habitat disturbance is thus expected to play a role in shaping home range size and use owing to the consequent changes to resource distribution and availability (Bayart and Simmen 2005; Boyle et al. 2009; Donati et al. 2011a; Schwitzer et al. 2007). Recent studies investigating the influence of habitat degradation on primate ranging behavior found that higher food availability in less disturbed areas usually entails smaller home ranges (Curtis and Zaramody 1998; Donati et al. 2011a; Kelley 2013; Schwitzer et al. 2007), although this does not always seem clear-cut (Irwin 2008; Johnson 2002; Wallace 2006). Fragmentation has been also shown to influence ranging areas, with primates living in small forest patches usually having smaller home ranges than those in continuous forests (Colobus vellerosus: Wong and Sicotte 2007; Alouatta palliata: Cristóbal-Azkarate and Arroyo-Rodríguez 2007; Propithecus diadema: Irwin 2008; Chiropotes satanas: Boyle et al. 2009). Home range size can also vary according to species’ body mass, social system, activity cycle, season, and population density (Burt 1943; Clutton-Brock and Harvey 1979; Harestad and Bunnel 1979; Haskell et al. 2002). Several studies have shown that even distribution of food resources and high food availability allow animals to minimize their daily movements to fulfill energy needs, while in habitats where resources are more scattered and/or food availability is low, long traveling paths are necessary (Boyle et al. 2009; Curtis and Zaramody 1998; Kaplin 2001; Volampeno et al. 2011). However, also in this case exceptions seem to be as frequent as rules and other studies have found the opposite trend, with longer traveling paths in less degraded habitats and/or in areas with high food availability (Goodall 1977; Irwin 2008; Wallace 2006; Yamagiwa and Mwanza 1994). Two different strategies have been hypothesized to explain the relationship between animal ranging patterns and resource distribution/availability: resource-maximizing and area-minimizing (Mitchell and Powell 2004, 2012). According to these models, animals can either maximize resources within their home ranges via a random use of patches (resource-maximizing strategy), or they can gather resources to satisfy a minimum resource threshold (area-minimizing strategy). These strategies are modified from the energy-maximizing and the time-minimizing models of the classic optimal foraging theory (Hixon 1982; Schoener 1971).

Author's personal copy Ranging Behavior of Eulemur collaris

Malagasy environments are notoriously suffering high levels of habitat degradation and fragmentation (Du Puy and Most 1996; Green and Sussman 1990; Schwitzer et al. 2014; Wright 1999). Moreover, pronounced seasonality, climatic unpredictability, and natural fluctuations in food availability represent a serious challenge to lemurs (Dewar and Richard 2007; Jolly 1984; Wright 1999). The littoral forest of southeastern Madagascar, for example, is naturally characterized by low productivity due to the sandy soil and it has been reduced today to an archipelago of fragments smaller than a few hundred hectares (Bollen and Donati 2005, 2006). Thus, this area may represent today a harsh environment for frugivores and a model to test predictions concerning lemurs’ behavioral and ecological response to habitat disturbance. The collared brown lemur (Eulemur collaris) is the largest lemur living in the littoral forest habitat, where it maintains a mainly frugivorous habit, supplementing its diet mostly with flowers, young leaves, and invertebrates (Donati et al. 2007a). In littoral forest fragments this species has been shown to have a high degree of social and ecological flexibility (Donati et al. 2007b, 2011a,b). However, these lemurs do not shift to a more folivorous diet when they have to face periods of fruit scarcity (Donati et al. 2011a), contrary to what has been observed in other brown lemur populations (Rasmussen 1999; Sussman 1974). In fact, one of their strategies to counteract potential food scarcity is an increase in ranging areas rather than a shift to fallback species (Donati et al. 2011a). This is in line with other findings on frugivorous lemurs in disturbed habitats (Eulemur macaco: Bayart and Simmen 2005; Eulemur flavifrons: Schwitzer et al. 2007). However, this raises the question as to how a highly frugivorous lemur with large home range requirements is able to cope in small islands of forest at low productivity. We studied variability in the ranging patterns of collared brown lemurs living in the highly disturbed fragments of Mandena and those inhabiting a less disturbed fragment of Ste. Luce, in the littoral forest of southeastern Madagascar. We increased the resolution of previous analyses (Donati et al. 2011a) by providing a more extensive, comparative dataset and by focusing on different facets of the ranging patterns. We compared our results with previous data, since patterns of small and isolated populations may change considerably over a short period of time (Wieczkowski 2005). We hypothesize that lemurs in the more disturbed area: 1. Will use larger annual and monthly ranging areas to fulfill their nutritional requirements. 2. Will have discontinuous and fragmented core areas owing to the expected patchy distribution of resources. 3. Will have to travel more daily as resources are more scattered and smaller trees are more quickly depleted. 4. Will require larger monthly ranges and longer travel distances during the lean period than during the period of fruit abundance.

Methods Study Site and Species We conducted this comparative study in the littoral forest fragments of Mandena and Ste. Luce in southeastern Madagascar. The Conservation Zone of Mandena (24°57′S, 47°0′E), 11 km northwest of Fort Dauphin, is located on sandy soils at an altitude 0–20


m above sea level. Our study was conducted in M15 and M16 fragments consisting of a total of 148 ha of fairly degraded littoral forest (Ganzhorn et al. 2007). The two fragments are separated by a swamp (ca. 82 ha) that collared brown lemurs use frequently; therefore we considered the complex as a single area of ca. 230 ha. The mean canopy height in Mandena is 8.9 ± SD 4.4 m (Rabenantoandro et al. 2007). Furthermore, some groups of collared brown lemurs use a fragment outside the Conservation Zone (M20), which includes ca. 6 ha of heavily degraded forest, and is located northeast of the other two fragments (Ganzhorn et al. 2007). The collared brown lemurs intensively use the swamp that links M20 with the other fragments, called Analamafotra from the vernacular name of the tree (mafotra) that characterizes this swamp. In addition to Eulemur collaris, four nocturnal (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major, Avahi meridionalis), and one cathemeral (Hapalemur meridionalis) lemur species are found in this area. The second study site, the protected littoral forest of Ste. Luce (24°46′S, 47°10′E), ca. 30 km northeast of Fort Dauphin, is among the most intact littoral ecosystems in Madagascar and possesses a very high diversity of vegetation (Bollen and Donati 2006). Our study fragment was S9, ca. 252 ha of well preserved (Ganzhorn et al. 2007) littoral forest and swamp, 190 of which are included in the Conservation Zone. The mean canopy height in S9 is 14.7 ± SD 4.3 m (Rabenantoandro et al. 2007). In addition to Eulemur collaris, four nocturnal lemur species (Microcebus sp., Cheirogaleus medius, Cheirogaleus major, Avahi meridionalis) are present in S9. Floristically Mandena and Ste. Luce littoral forests are very similar and structural differences indicate that Mandena represents degraded forms of the vegetation type in Ste. Luce (Rabenantoandro et al. 2007). This inference is also suggested by the disappearance of some tree families known to be logged in Mandena but not in Ste. Luce (Rabenantoandro et al. 2007). The collared brown lemur is a medium-size strepsirrhine with a mean body mass of 2.15 ± SD 0.25 kg and a mean body length of 46.1 ± SD 2.6 cm (Donati et al. 2011a). The population density in Mandena is ca. 12 individuals/km2, while the density in Ste. Luce is ca. 38 individuals/km2 (Donati et al. 2007b). Previous studies indicate that Mandena is a lower quality habitat for Eulemur collaris when compared to Ste. Luce in terms of food nutritional values and size of feeding trees (Donati et al. 2011a). Collared brown lemurs now living in Mandena were relocated to M15 and M16 in 2000 and 2001 from nearby forest fragments chopped down by charcoal makers (Donati et al. 2007b). The species was not present in M15 and M16 before the relocation because the resident population was hunted out while the area was unprotected. It is well known that relocated animals may range over large areas as a consequence of their initial explorative behavior (Ostro et al. 1999; Richard-Hansen et al. 2000). Since their relocation, however, the population in Mandena has been monitored regularly and the lemurs have shown stable ranging areas during the last few years (Donati et al. 2007b, 2011a). Thus, we are confident that the ranging patterns recorded in our study have not been severely influenced by the relocation. Data Collection We examined food abundance via five plots (20 m × 50 m) within the home range of each focal group. In each plot we measured the circumference of all trees >5 cm


diameter at breast height (DBH) and we identified the species. The plot locations were selected randomly within the area occupied by each group. In Mandena, we also collected data on fruit availability during the study period. The presence of ripe fruits, unripe fruits, flowers, buds, and young leaves was reported twice a month on a sample of 107 species (with 3 individuals per species) included in a phenological trail. We then filtered from the sample the 46 species included in diet of Eulemur collaris. These species consisted of both forest (35) and swamp (9) species and covered 90.2 % of the tree species eaten by Eulemur collaris in Mandena during our study period. The sample encompassed all the priority feeding species, i.e., used for >1 % of feeding records. We present only ripe fruits availability, as this represents the main food used by Eulemur collaris (Donati et al. 2011a). We collected data on four groups (Table I) of collared brown lemurs: two groups in Mandena (MAN-AB and MAN-C), and two groups in Ste. Luce (STL-A and STL-B). To ensure systematic observations, four individuals (one for each group) were captured and equipped with radio-collars (TW-3, Biotrack, 29 g). Each group was followed 4 d/mo. Overall, we collected 962 observation hours in Mandena and 1118 hours in Ste. Luce. We followed the groups from 06:00 to 18:00 h during each observation day. We chose a focal individual among the adult individuals at the beginning of each observation, balancing the time spent observing males and females. We followed the focal individual as long as possible, and substituted with the first visible individual of the same sex if lost. To examine lemurs’ diet and feeding trees used, we collected behavioral data using instantaneous sampling (Altmann 1974), with recordings taken every 5 min. We recorded intergroup encounters with any visible group of Eulemur collaris via all occurrences sampling (Altmann 1974). We also recorded the lemur location every 30 min via a handheld GPS (Garmin 60CSx). In total, we used 2310 GPS points to obtain home range estimates for the Ste. Luce groups (1229 for group STL-A, 1081 for group STL-B) and 1731 GPS points for the Mandena groups (1090 for group MANAB, 641 for group MAN-C). The total duration of the data collection in Mandena was shorter owing to the unfeasibility of observing the animals during wet periods, when the water level of the marsh exceeds breast height. This delayed the captures and consequently the observation period (group MAN-AB was followed from March 2011 to January 2012; group MAN-C was followed from June 2011 to January 2012).

Table I Composition of the four study groups of Eulemur collaris from February 2011 to January 2012 at Ste. Luce and Mandena Ste. Luce

Adult males

Mandena

Group STL-A

Group STL-B

Group MAN-AB

Group MAN-C

4

3–4

2–3

2–3

Adult females

3

3–4

1

1–2

Juveniles

1

2

0

1

Infants

5

3

1

1

Total

8–13

8–11

3–4

5–6


Ethical Note The four adult individuals equipped with radio-collars were captured via cages, using banana slices as bait, and were rapidly anesthetized with Zoletil 100 (5 mg/kg of tiletamine hydrochloride). All subjects recovered from anesthesia within 1.5 h and were not moved from the capture area. The lemurs were followed until regaining full mobility in trees and there were no injuries as a consequence of the captures. The collars were below the 5 % threshold of the subjects’ weight recommended for arboreal animals. Because no adverse effect of the collars was detectable during the study we did not remove them at the end of the research. This was decided to facilitate the ongoing program of systematic observations at both sites, as collar batteries work for longer than our study period. We conducted this study with the authorization of the Commission Tripartite of the Direction des Eaux et Forêts de Madagascar (Autorisation de Recherche n.29/11/MEF/ SG/DGF/DCB.SAP/SCB du 20/01/11). This study was ethically approved by the University of Pisa (Animal Care and Use Board). Data Analysis To estimate food abundance within vegetation plots, we selected all the priority feeding trees. We calculated the Index of Dispersion (ID; Pielou 1969) within the home range of each group for each priority tree species via the formula: ID = σ2 / μ, where σ2 was the variance and μ was the mean number of trees in each plot. The overall ID in each home range was obtained as the mean of the IDs for each priority tree species. We classified distribution patterns as random (ID = 1), uniform (ID < 1), and clumped (ID > 1). We then performed χ2 tests to compare the given distributions to the Poisson distribution. We distinguished between a lean period (from May to October) and a period of abundance (from November to April) to evaluate the effects of food availability. We made this distinction on the basis of both previous multiannual phenological studies in Ste. Luce (Bollen and Donati 2005) and the phenological data collected in Mandena during our study period (Fig. 1). In Mandena and Ste. Luce, we defined lean periods all the months that were below the median percentage of trees with ripe fruits. Fruit availability in Mandena (Fig. 1) shows an season of abundance in February 2011–April 2011 and in November 2011– January 2012, and a lean season in May 2011–October 2011. The lowest fruit availability was found in June (2.2 % of priority tree species had ripe fruits), whereas the highest values were recorded in February (19.6 % of priority tree species had ripe fruits). We analyzed ranging patterns via Ranges 7 (Anatrack Ltd.). For compatibility with previous studies we estimated the monthly and the annual home ranges via minimum convex polygons (MCPs) using all the location points. However, MCPs have been shown to bias the results because of the inclusion of never visited areas (Powell 2000). MCP estimates might also affect small-scale comparisons, i.e., within species or populations, although when large differences occur most of the variation is due to real differences (Nilsen et al. 2008). Therefore, we also used 95 % and 50 % fixed kernel (FK) analyses with the smoothing selected by least-squares cross-validation (LSCVh) (Seaman et al. 1999). Choosing the appropriate smoothing parameter (h) is the most important factor when using the kernel method for home range analysis (Worton 1995). LSCVh generally performs better than the optimal h for a standard multivariate normal distribution (Seaman


Fig. 1 Monthly fruit availability of tree species used by Eulemur collaris in Mandena from February 2011 to January 2012 (46 species). Period of food abundance is in the gray background, lean period in the white background.

and Powell 1996; Seaman et al. 1999) but has very poor performances at small sample size (Horne and Garton 2006; Seaman et al. 1999). Thus, we considered the differences on monthly ranges reliable only when statistically confirmed both using 100 % MCP and 95 % FK analyses. Owing to the different number of GPS points per group, we performed an incremental area analysis (IAA) to determine whether annual ranges estimated via 100 % MCP and 95 % FK provide evidence of stability. To control for the possibility that unbalanced sample sizes were driving the differences, we also provided the values of the group home ranges for the June 2011–January 2012 period. This additional analysis allowed a direct comparison during the time window when all four groups were followed simultaneously. We calculated the daily distance traveled (km) for each day as a proxy of energy expenditure. In addition, we determined the Defensibility Index (D; Mitani and Rodman 1979) for each group using data from all months to assess the feasibility of territorial defense. This was calculated using the formula: D = d * (4A/μ)0.5, where d was the mean daily distance traveled and A was the annual home range obtained via 95 % FK analyses. D ≥ 1 indicates that territoriality is efficient, D < 1 indicates that territoriality is not efficient. We also calculated a daily intergroup encounter rate for each of the four focal groups to determine the potential resource contest competition in the two areas. To test for structural differences between the vegetation in the groups’ ranges, we used the nested ANOVA with mean DBH and density of priority feeding trees as dependent variables and Site and Group as intersubject nested factors. Differences in encounter rates were also tested via the nested ANOVA with Site and Group as intersubject nested factors. Repeated measures (RM) ANOVA was conducted to evaluate differences in ranging patterns between sites, groups, and seasons, with seasonality (abundance/lean) as intrasubject factor and Site and Group as intersubject nested factors. We used Tukey’s HSD as post hoc analyses. Before running the ANOVAs, we tested for normality (Kolmogorov–Smirnov test), sphericity (Mauchly’s test) and equality of variances (Levene’s test) as underlying assumptions, and we logtransformed the data when the assumptions were not met. In the case of a significant Kolmogorov–Smirnov test and a nonsignificant Levene test we used a Duncan’s post hoc analyses. We performed all tests with STATISTICA 8.0 and considered P < 0.05 as the significant level.


Results Food Abundance and Availability Mean DBH of priority feeding trees (Table II) was larger in Ste. Luce (mean: 13.08 ± SD 2.48 cm; N = 10 plots) when compared to Mandena (mean: 9.59 ± SD 0.91 cm; N = 10) (nested ANOVA, Site effect: F1,16 = 19.50, P < 0.001), while it was not different between groups (Group effect: F2,16 = 0.42, P = 0.666). Priority feeding tree density was not different between Ste. Luce (mean: 783 ± SD 256 n°trees/ha; N = 10) and Mandena (mean: 640 ± SD 193 n°trees/ha; N = 10) (Site effect: F1,16 = 2.10, P = 0.167) as well as between group home ranges (Group effect: F2,16 = 1.48, P = 0.257) (Table II). The ID indicated a clumped distribution of priority feeding trees within the home ranges of the four groups (Table II). Home Ranges The largest annual home range was recorded for group MAN-C, followed by group STL-A, group MAN-AB, and group STL-B (Table III). IAA showed that annual ranges stabilized for Ste. Luce groups, while annual ranges in Mandena groups continued rising, without reaching an asymptote (Table III). The analysis of the home ranges calculated from June 2011 to January 2012 (when all four groups were observed simultaneously) indicated that group MAN-C still had the largest range (MCP: 112.54 ha; FK: 83.25 ha), followed by group MAN-AB (MCP: 66.06 ha; FK: 37.52 ha), group STL-A (MCP: 20.74 ha; FK: 17.10 ha), and group STL-B (MCP: 17.74 ha; FK: 14.70 ha). Monthly ranges were larger in Mandena groups than in Ste. Luce groups (RM ANOVA, site effect: F1,16 = 26.85, P < 0.001), with a mean of 23.70 ± SD 15.03 ha (N = 19 mo) in Mandena and a mean of 12.01 ± SD 5.04 ha (N = 24) in Ste. Luce, using the MCP analyses (Fig. 2a). Monthly ranges calculated via MCP analyses differed also between groups (Group effect: F2,16 = 3.73, P = 0.047). In particular, group MAN-C had larger monthly ranges than group STL-A (Duncan: P < 0.001), group STL-B (P < Table II Diameter at breast height (DBH), density, and Index of Dispersion (ID; χ2 test results in parentheses) of priority feeding trees used by Eulemur collaris in Ste. Luce and Mandena DBH (cm) (N = 5)

Density (n°trees/ha) (N = 5)

ID (N = 14–24)

Group STL-A

13.0 (±2.6)

790 (±278)

4.53 (χ2 = 4.19, N = 24, P < 0.001)

Group STL-B

13.2 (±2.6)

776 (±265)

6.38 (χ2 = 3.07, N = 21, P = 0.006)

Group MAN-AB

10.1 (±0.6)

760 (±208)

4.78 (χ2 = 4.59, N = 18, P < 0.001)

Group MAN-C

9.0 (±0.9)

520 (±67)

2.59 (χ2 = 6.71, N = 14, P < 0.001 )

Ste. Luce

Mandena

DBH and density values are means and standard deviations (in parentheses). The sample size for DBH and density is the number of plots. The sample size for ID is the number of priority tree species. Study period: February 2011–January 2012.


0.001), and group MAN-AB (P = 0.012), and group MAN-AB had larger monthly ranges than group STL-B (P = 0.022). Monthly ranges in Mandena groups (mean: 23.07 ± SD 16.56 ha; N = 19) were also larger than in Ste. Luce groups (mean: 16.65 ± SD 7.59 ha; N = 24) using the FK analyses (Site effect: F1,16 = 6.01, P = 0.026) (Fig. 2b). Monthly ranges calculated via FK analyses differed between groups (Group effect: F2,16 = 6.53, P = 0.008), with group MAN-C having larger monthly ranges than group STL-B (Tukey HSD: P = 0.005). Monthly ranges were not different between seasons using the MCP analyses (Period effect: F1,16 = 0.09, P = 0.767), but they were larger during the period of abundance (mean: 23.26 ± SD 14.84 ha; N = 23) than during the lean period (mean: 15.66 ± SD 5.83 ha; N = 20) using the FK analyses (Period effect: F1,16 = 6.48, P = 0.022). Core Area Use FK analyses showed a less fragmented use of space in Ste. Luce groups, with a single core area (in the cases of group STL-A and group STL-B) and a single annual ranging area (in the case of group STL-B) (Fig. 3). The annual range of group STL-A was fragmented because this group moved to the southern part of S9 between March and April. In Mandena, group MAN-AB had a single core area in the M16 fragment, but the annual ranging area was fragmented between M15 and M16. Group MAN-C had four different core areas (one in M20, one in M16, one in Analamafotra, and one in M15) and a single annual range (Fig. 3). On a monthly basis, group STL-A had fragmented ranges and multiple core areas in February and in December, while group STL-B had a fragmented range in September and multiple core areas in June. In Mandena, group MAN-AB had fragmented ranges from September to December and multiple core areas in December and January, while group MAN-C had fragmented ranges from June to October and in January and multiple core areas from July to September, in December, and in January. The annual core area of group MAN-C was about four times that of the other three groups (Table III). Considering only the period from June 2011 to January 2012, the core area size of group MAN-C remained the largest (22.27 ha), followed by group MAN-AB (9.14 ha), group STL-B (5.35 ha), and group STL-A (4.64 ha). The size of Table III Home range comparison between the four focal groups of Eulemur collaris in the two study sites Annual home range size (ha) No. of months

No. GPS locations

100 % MCP

95 % FK

50 % FK

Group STL-A

12

1229

98.86 (288)

50.23 (1066)

5.52

Group STL-B

12

1081

20.69 (737)

15.08 (712)

5.53

Group MAN-AB

11

1090

66.34 (>)

34.47 (>)

4.41

Group MAN-C

8

641

112.54 (>)

83.25 (>)

22.27

Ste. Luce

Mandena

Data were collected from February 2011 to January 2012. In parentheses: number of GPS locations needed to obtain a clear stability via the incremental area analysis. (>) indicates that no clear stability was reached.


Fig. 2 Variation in monthly ranges in the four study groups of Eulemur collaris in Mandena and Ste. Luce from February 2011 to January 2012. Data were obtained via 100 % MCP (a) and via 95 % FK analyses (b). Period of food abundance is in the gray background, lean period in the white background.

the monthly core areas was not different between Mandena (mean: 4.10 ± SD 3.80 ha; N = 19 mo) and Ste. Luce (mean: 3.08 ± SD 1.29 ha; N = 24) (RM ANOVA, Site effect: F1,16 = 1.89, P = 0.188) and between groups (Group effect: F2,16 = 1.06, P = 0.368) (Table III). Monthly core areas were not different also between the period of food abundance (mean: 4.29 ± SD 3.51 ha; N = 20) and the lean period (mean: 2.87 ± SD 1.57 ha; N = 23) (Period effect: F1,16 = 2.17, P = 0.160). Daily Distance Traveled The lemurs in Ste. Luce had longer monthly averages of daily distance traveled (mean: 1.04 ± SD 0.28 km; N = 24 mo) when compared to those in Mandena (mean: 0.82 ± SD


Fig. 3 Annual home ranges and core areas in the four focal groups of Eulemur collaris. Data were collected from February 2011 to January 2012. Depicted are the 95 % and 50 % FK analysis. Mandena forest (M15, M16, M20) is on the left while Ste. Luce forest (S9) is on the right. Darker areas indicate core areas.

0.16 km; N = 19) (RM ANOVA, site effect: F1,16 = 9.04, P = 0.008), while they did not differ between groups (Group effect: F2,16 = 1.70, P = 0.214). Post hoc test revealed that group STL-B traveled longer distances than group MAN-AB (Tukey HSD: P = 0.039) and group MAN-C (P = 0.048). Monthly averages of daily distance traveled (Fig. 4) varied between seasons (Period effect: F1,16 = 10.61, P = 0.005). Distances were longer during the period of abundance [mean: 1.19 ± SD 0.26 km (N = 12) in Ste. Luce, mean: 0.87 ± SD 0.16 km (N = 8) in Mandena] when compared to the lean period [mean: 0.89 ± SD 0.21 km (N = 12) in Ste. Luce, mean: 0.78 ± SD 0.14 km (N = 11) in Mandena]. In particular, lemurs traveled longer distances during the period of food abundance in Ste. Luce (Tukey HSD: P = 0.007), while we found no differences between the two periods in Mandena (P = 0.567). Territoriality Group STL-B had the highest Defensibility Index (D = 2.57), followed by group MAN-AB (D = 1.27), and group STL-A (D = 1.20). Group MAN-C was the only group in which territoriality was not economically convenient (D = 0.77). Encounter rates were significantly higher in Ste Luce (mean: 0.68 ± SE 0.06, N = 87 d) than in Mandena (mean: 0.03 ± SE 0.07, N = 72) (nested ANOVA, Site effect: F1,155 = 45.79, P < 0.001). Encounter rates were different between groups (Group effect: F2,155 = 6.33, P = 0.002). In particular, group STL-A had higher encounter rates than group STL-B (Tukey HSD: P = 0.003), group MAN-AB (P < 0.001), and group MANC (P < 0.001), and group STL-B had also higher values than group MAN-AB (P = 0.007) and group MAN-C (P = 0.021).

Discussion The annual and monthly home ranges of collared brown lemurs were larger in the degraded forest fragments of Mandena when compared to the less disturbed forest in


Fig. 4 Variation in monthly mean of daily distance traveled by the four focal groups of Eulemur collaris in Mandena and Ste. Luce from February 2011 to January 2012. Period of food abundance is in the gray background, lean period in the white background. Error bars represent standard deviations.

Ste. Luce. The more disturbed area, with the consequent lower food availability, seems to induce Mandena lemurs to expand their threshold of area requirement in search of fruiting trees. This expansion in response to habitat degradation matches with previous studies on Eulemur collaris (Donati et al. 2011a), other Eulemur species (Schwitzer et al. 2007, 2011), and other primates (McCann et al. 2003; Rodriguez-Toledo et al. 2003), but not with what has been observed in more folivorous lemurs (Irwin 2008; Martinez 2008). Looking at individual group differences, the very large area used by group MAN-C seems to play a major role in determining the differences between sites in terms of monthly ranges. In contrast, the other group in Mandena, group MAN-AB, showed an annual home range smaller than that of group STL-A, if we include February–May 2011 in the analysis. Thus, group MAN-AB seemed to behave similarly to the Ste. Luce groups. This may be explained by the habitat similarities of MAN-AB and the Ste. Luce lemurs, both located in the littoral forest, which contrasts with the large areas of swamp used by group MAN-C. However, smaller groups usually have smaller home ranges (Barton et al. 1992), and group MAN-AB contained less than half the number of the adult individuals (three to four) than the groups in Ste Luce (seven to eight). It is thus clear that the unit area required by a single animal in Mandena is much larger than in Ste. Luce, even if we only compare MAN-AB with the two groups in Ste. Luce, without taking into account group MAN-C. In support of this, the IAA shows that the home ranges of both groups at Mandena did not reach a plateau, in contrast to the home ranges of the groups in Ste. Luce, thus indicating that a longer sampling period would have resulted in even larger home ranges in the degraded area. Despite the shorter sampling period, group MAN-C had an exceptionally large home range, 112.54 ha with the MCP method, which stands at the upper limit of what has been previously reported in brown lemurs (Overdorff 1993; Overdorff et al. 1999; Vasey 1997). Further, the IAA showed that the true annual range of this group is probably even larger than what we recorded. Eulemur species living in Eastern rainforests are known to have the largest home ranges (between 85 and 100 ha) found so far for this genus (Johnson 2002; Overdorff et al. 1999; Vasey 1997), whereas home


ranges in Western dry forests are generally smaller, ranging from 2.8 to 18.2 ha (Bayart and Simmen 2005; Colquhoun 1993; Curtis and Zaramody 1998; Volampeno et al. 2011). This may be due to the overall less abundant and unpredictable fruit availability in eastern rainforests (Bollen and Donati 2005; Wright et al. 2005). However, recent data showed that Eulemur rufifrons in Kirindy may have large home ranges as well (23–443.7 using the MCP and 25.2–324.4 using the FK analyses) as a consequence of seasonal water scarcity (Scholz and Kappeler 2004). Thus, the genus shows extreme ranging flexibility in tracking food resource and water availability, and it is difficult to draw generalizations. The lack of a plateau in the IAA for Mandena home ranges suggests a different strategy of resource use by these lemurs than by the groups in Ste. Luce. The groups in Mandena seem to operate as area-minimizers, whereas the groups in Ste. Luce behave more as resource-maximizers (Mitchell and Powell 2004, 2012). The former strategy is typically used when food availability is low, whereas the latter when food availability is high (Hixon 1982; Schoener 1971). An area-minimizing strategy leads to an increase in home range size when resource availability decreases, as the resource accumulation/area ratio decreases while the resource threshold, i.e., the minimal amount of resources needed to satisfy animals’ requirements, remains the same. Animals adopting the resource-maximizing strategy, however, shift from a random to a more selective use of the forest when resource availability decreases, but no variation in home range size is expected (Mitchell and Powell 2004, 2012). Overall, the ranging pattern recorded in Ste. Luce was similar to that recorded in 2000 in the same area (Donati 2002; Donati et al. 2011a). Donati (2002) reported annual values of 96.8 ha for group STL-A and 20.5 ha for group STL-B in 2000, while we found 98.86 ha for group STL-A and 20.68 ha for group STL-B in 2011. This finding may be an indication that the habitat quality in the Ste. Luce forest fragment has not changed significantly over the last decade. Interestingly, one of the groups in the more preserved fragment, group STL-A, had the second largest annual home range since it moved outside of its usual range to an area rich in fruits of Sarcolaena multiflora in March/April 2011. The same group had a similar pattern, and also moved far from its usual ranging area in March/April more than 10 yr before (Donati 2002). This pattern does not seem to be unusual for brown lemurs even in less disturbed forests as migrations from familiar areas have also been recorded in Eulemur rufifrons in Ranomafana (Overdorff 1993; Wright 1999) and in Eulemur fulvus in Ankarafantsika (Sato 2013). In Mandena, monthly ranges were previously recorded in 2004 and in 2007 (Donati et al. 2011a). Mean monthly ranges recorded in Mandena in that study were 28.11 ± SD 13.28 ha, while we found in our study 23.70 ± SD 15.03 ha. This minor variation suggests again that collared brown lemur ranging areas have remained stable over the last 5 yr. In Mandena we observed larger monthly ranges during the season of abundance at the end of 2011, rather than during the previous season of abundance at the beginning of 2011. This pattern may be the result of phenological variations at this site, which showed a higher availability of ripe fruit from February 2011 to April 2011, rather than from November 2011 to January 2012. As expected, the groups in Mandena appear to move their threshold of area requirements depending on monthly fruit availability. However, the littoral forest fruiting pattern does not seem to be the only phenological determinant of the observed ranging fluctuations. For example, the ranging pattern of group MAN-C was heavily influenced by the availability of the flowers of Brexia madagascariensis. This swamp tree produced a large flower crop where the lemurs spent long feeding sessions. Our feeding observations clearly showed that in July, August, and October, when the home range of group MAN-C was at its minimum, Brexia was by far the preferred food item of this group (>33 % of feeding time).


The consumption of Brexia increased again in January 2012 (20.5 % of feeding time), when the ranging area of the group MAN-C shrank again. Brexia flowers accounted for