Primates

, Volume 55, Issue 2, pp 207–217

Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations

Authors

    • Department of AnthropologyUniversity of Colorado
  • Michelle Sauther
    • Department of AnthropologyUniversity of Colorado
  • Frank Cuozzo
    • Department of AnthropologyUniversity of Colorado
    • Department of AnthropologyUniversity of North Dakota
  • Nayuta Yamashita
    • Institute for Population GeneticsUniversity of Veterinary Medicine, Vienna
  • Ibrahim Antho Jacky Youssouf
    • Département de Sciences BiologieUniversité de Toliara
  • Richard Bender
    • Department of AnthropologyUniversity of Colorado
Original Article

DOI: 10.1007/s10329-013-0391-1

Cite this article as:
LaFleur, M., Sauther, M., Cuozzo, F. et al. Primates (2014) 55: 207. doi:10.1007/s10329-013-0391-1

Abstract

Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered “strictly diurnal”. We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010–April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25 % of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5 % of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53 % nighttime, 43 % daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.

Keywords

LemurCathemeralDietActivity pattern

Introduction

Adaptations to diurnal or nocturnal living are vast, and may affect variables such as life history, diet, sociality, morphology, predator and prey dynamics, and sensory functioning (see Enright 1970; Terborgh and Janson 1986). It would thus seem unlikely that primates, or any mammal, would be active both during the day and night, given that day-active adaptations may hinder an animal during the night, and vice versa (Charles-Dominique 1975; Halle 2006), however, there are many non-primate mammals that exhibit cathemeral activity patterns (e.g. carnivores, cetaceans, rodents, etc.; see Curtis and Rasmussen 2006). Although it is rare for primates to exhibit cathemeral activity patterns (i.e., periods of activity both during the day and at night), one haplorrhine genus, Aotus (Wright 1989; Fernandez-Duque 2003), and three strepsirrhine genera, Eulemur (see Overdorff and Rasmussen 1995), Hapalemur (see Tan 1999) and Prolemur (Tan 1999) are regarded as cathemeral. Cathemerality is disproportionately prevalent within some lemur taxa, which may suggest that Madagascar has, or at least had, some environmental properties favoring flexible activity patterns in the common ancestor of these genera (Tattersall 1982; Ganzhorn et al. 1999; Wright 1999; Curtis and Rasmussen 2006; Donati and Borgognini-Tarli  2006; Donati et al. 2013). The modern-day environment of Madagascar is regarded as “hypervariable” (Dewar and Richard 2007), although we do not know if these conditions were present when the trait may have been selected.

Teasing apart environmental factors promoting cathemeral activity patterns in lemurs have proved rather arduous (Curtis and Rasmussen 2006). Some of the difficulties lie in the impracticality of monitoring animal behavior over 24-h periods, and human researchers’ shortcomings in the nocturnal environment (Curtis 2006; Curtis and Rasmussen 2006). Moreover, ever-changing environmental factors, which are often coupled, make it difficult to tease out cause and effect (Curtis and Rasmussen 2002).

The proximate (and in some cases, ultimate) variables that are important contributing factors to cathemeral behavior in some lemurs include: temperature, humidity, rainfall, moon phase, luminosity, and day length (see Donati and Borgognini-Tarli 2006; Curtis and Donati 2013). Moreover, ultimate factors (non-mutually exclusive) which have been proposed to account for flexible activity patterns include: thermoregulatory benefits, wherein a cathemeral niche enables lemurs to minimize thermoregulatory costs and stressors associated with maintaining temperature homeostasis (Curtis et al. 1999; Mutschler 1999); predator avoidance, in which lemurs exploit a cathemeral activity pattern in order to reduce predator encounters and predation threat (Curtis and Rasmussen 2002); competition minimization, which acts to reduce competition when multiple large-bodied lemurs occupy the same territory (Tattersall and Sussman 1998; but see Overdorff 1993); and dietary needs, where cathemerality allows lemurs to best utilize low-quality food resources during times of food scarcity (Engqvist and Richard 1991; Overdorff and Rasmussen 1995; Donati et al. 2009). Each of these variables and hypotheses are important at either the proximate and/or ultimate levels for some lemurs during some time periods, however, in most instances, contrary or null evidence may also exist [e.g. avoidance of cold temperatures (Mutschler 2002), but see (Curtis et al. 1999); minimizing predator encounters (Curtis and Rasmussen 2002; but see Tarnaud 2006)]. The remaining task at hand is to examine the environmental conditions under which extant lemurs use cathemerality, such that we can better understand how this unusual activity pattern was selected for in lemurs, and subsequently in other primates.

Activity patterns of ring-tailed lemurs

Although L. catta has been considered “strictly diurnal” (Jolly 1966; Sauther et al. 1999), mounting anecdotal (Jolly 1966; Sauther 1989) and empirical evidence (Traina 2001; Donati et al. 2012; Parga 2011), suggests a flexible activity pattern in this species. Jolly (1966) and Sauther (1989) noted nocturnal yapping (a call in response to a potential predator) by L. catta at both Berenty Private Reserve and Beza Mahafaly Special Reserve. Traina (2001) found that the nighttime activities of L. catta at Berenty included feeding, grooming, traveling, playing, mating, and fighting. Parga (2011) used GPS during a brief, one-week study of five, semi-captive, provisioned L. catta on St. Catherine's Island, Georgia, USA, and found animal ranging between the hours of 1900 and 0530. Most recently, Donati et al. (2013), documented nearly 1,000 (approximately 500 daytime and 500 nighttime) focal animal observation hours over a period of 5 months (October–February) of ring-tailed lemurs at Berenty, and found that these lemurs frequently engaged in nighttime activity. Moreover, these lemurs’ nocturnal activity levels were positively correlated with moon luminosity (Donati et al. 2013).

Lemur catta is regarded as an extraordinarily flexible primate in many aspects (e.g. habitat type, feeding behavior, sleep sites, see Gould 2006) and cathemeral behavior may represent another way in which this species is adaptable. Cathemerality in L. catta may thus play an important additional role in understanding the types of adaptations that enable extreme flexibility in this species.

The data presented here are part of a larger, ongoing project examining the biology, feeding ecology and nutrition in ring-tailed lemurs at the Tsimanampetsotsa National Park (e.g., Sauther and Cuozzo 2008; LaFleur 2012). We did not anticipate cathemeral activity in this species, as when this research was planned and undertaken, ring-tailed lemurs were considered diurnal (but see Traina 2001). Once nighttime activity was detected, we hypothesized that nocturnal activity levels would be favored or inhibited (high daytime temperature, low overnight temperature, food scarcity or brief abundance) by the extreme conditions specific to the spiny forest. In addition to (1) temperature and (2) diet, we proposed that (3) predation would influence nocturnal activity in ring-tailed lemurs. Although competition avoidance has also been proposed as a mechanism promoting cathemeral activity in lemurs, the hypothesis was not explored here as competition at the community-wide level is beyond the scope of this research.

Methods

Study site

Data were collected at Tsimanampetsotsa National Park (TNP), in southwestern Madagascar (24°03′–24°12′S, 43°46′–43°50′E) (Fig. 1), between September 2010 and April 2011. Lake Tsimanampetsotsa occupies 45 km2 of protected Ramsar wetlands (Convention on Wetlands of International Importance especially as Waterfowl Habitat), and the park extends to another 203 km2 of land protected by Madagascar National Parks. TNP represents the western-most escarpment of the limestone Mahafaly Plateau, and is largely characterized by dry, spiny, and xerophytic flora (Andrews and Birkinshaw 1998). Areas below the escarpment, along the margins of the Park’s large saline lake do display some mixed forest, including introduced trees (e.g., Casuarina). Most of the forest is not canopied, due to the sparse and dwarf vegetation, and tree species are primarily deciduous.
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Fig. 1

Maps of a Madagascar, b Tsimanampetsotsa National Park in relation to the Mozambique Channel, and c landmarks within the research area

This area is highly seasonal, and is subject to high winds, frequent droughts and cyclones (Andriatsimietry et al. 2009). The majority of rainfall occurs between late December and February, with total rainfall rarely exceeding 400 mm per year (Donque 1975). The dry season is long and has an average duration of 9–11 months (Andriatsimietry et al. 2009). During this study, absolute temperatures at base camp ranged from 10.4 to 41.9 °C (Fig. 2), however, temperatures (as measured with a handheld mercury thermometer) were often significantly higher (up to 53 °C) in areas of the forest. We note that during days with hot periods, particularly when temperatures were greater than 45 °C, lemurs spent long periods of the mid-day resting in the shade, while panting and licking their hands and feet. Seasonal rains began on Dec 23, 2010, and the last seasonal rain occurred on February 17, 2011 (Fig. 2). A total of 232 mm of rain were recorded during this time period.
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Fig. 2

Monthly average temperature highs and lows and cumulative rainfall from September 2010 to April 2011 at Tsimanampetsotsa National Park

Study animals

Ring-tailed lemurs are the only large-bodied lemurs present in the northern portion of TNP, though nocturnal small-bodied mouse lemurs co-occur (Microcebus griseorufus). Focal animal groups included Vintany (n = 12–14 adults, 7 sub-adults and 4–7 infants) and ILove (n = 9–10 adults, 7 sub-adults, and 4–5 infants). The Vintany and ILove groups’ home ranges totaled 1.10 and 0.85 km2, respectively, and overlapped by approximately 0.02 km2. No other lemur groups’ home ranges overlapped with these. The two groups’ nighttime sleeping locations were within the overlap of their territories and were separated by approximately 0.8 km. Vintany group’s (VG) primary nighttime sleeping location was in a large Ficus tree, whereas the ILove group’s (IG) nighttime sleep spot was in small communal caves on the face of a 20-m high limestone cliff. Each group’s daytime ranging patterns varied as ephemeral resources became available; however, the groups used the same nighttime sleeping locations in almost all instances. Infants were born in the 3rd week of September 2010, with the exception of one infant that was born and died 2 weeks prior to the others. Infants began foraging and consuming plant foods during the 1st week of January, 2010, and continued nursing throughout the study.

Behavioral sampling

During daytime hours, ML (and assistants) collected 526 h of focal animal sampling data, and 275 h of scan sampling data (Altmann 1974) on the ring-tailed lemurs. Additionally, 67 h of scan data were collected at night. Daytime or diurnal periods are defined here as time periods following dawn and preceding dusk, and conversely, nighttime or nocturnal phases are those following dusk and preceding dawn. Daytime data were collected between dawn and dusk between September 2010 and April 2011, and nighttime data were collected during weeks bracketing full moons (three nights preceding and following the full moon), between 8 p.m. and 1 a.m., in October, November, and December 2010, and March 2011. Scan data were collected at 5-min intervals with the goal of including 10 adult animals in every scan. Animal locations were noted as being on or off the ground, and if off the ground the substrate was noted (shrub, tree, air, etc.). Nighttime data collection were not part of the originally planned methods of this research, and in order to maintain the originally scheduled feeding data collection schedule, ML (and assistant) were unable to equally distribute nighttime observations over the 24-h period and monthly moon phase. We acknowledge that the data collection schedule presented here may not be representative of the full nighttime repertoire of activity or behaviors of these ring-tailed lemurs and that we are missing the crepuscular periods (4 a.m.–6 a.m., 6 p.m.–8 p.m.) which may include particularly important activity peaks.

Data were pooled according to whether they occurred during the day or at night. Animal scores were categorized as either active or non-active. For the active data pools, the amount of time spent in each behavioral category, were compared between day and night samples. Behavioral categories included: feed/forage, locomote, groom, and other (which included vigilance, sit, displace(d), scent mark, stink fight). Moreover, the percentages of time spent on or off the ground were compared between day and night.

During focal follows, if an animal was feeding, the plant and plant part were noted. Time spent feeding on each plant part were calculated and averaged for months in the dry and wet seasons. Representative plant samples (same plant part and phenological stage) were collected for nutritional analyses at the Department of Animal Ecology and Conservation at Hamburg University. Detailed methods for determining amounts consumed by animals and nutritional data are presented elsewhere (see LaFleur 2012), although we discuss the acid detergent fiber (ADF) consumed by ring-tailed lemurs, in order to assess dietary quality during the study period. ADF content was determined via modified procedures for the “Ankom fiber analyzer” (Goering and van Soest 1970; van Soest 1994).

Camera trap data

Moultrie Game Spy I-40 Infrared Flash Game Cameras (Moultrie Feeders, Alabaster, AL) were stationed near the two lemur groupsʼ sleeping sites (see Table 1 for total numbers of cameras in use and the number of camera trap days). The lemur groups were highly habitual in their patterns of locomotion when entering or exiting their sleep sites, and these cameras enabled us to see when the lemurs left and returned to these sites. Additionally, cameras were stationed along forest paths and/or in trees (n = 1–5) in areas that were frequented by one of the lemur groups, but these photographs were not included in the tallies of nighttime activity. Rather, they provided information on predators and the extent of nighttime ranging in the ring-tailed lemurs. The total number and position of cameras in use varied, as cameras required repairs or repositioning.
Table 1

Monthly tallies of the number of cameras employed, camera trap days, number of photo events, and the average rate of capture for nighttime camera events

 

Number of cameras in use

Camera trap days

Number of photo events

Photo event/per camera trap day

Septa

4

72

2

0.03

Oct

4

124

21

0.17

Nov

6

180

39

0.22

Dec

5

155

50

0.32

Jan

4

124

46

0.37

Feb

5

140

45

0.32

Mara

6

120

50

0.42

aDates include September 12–30, March 1–24, 2011

Camera trap photo events of lemurs at night serve as a proxy for nighttime activity levels (van Schaik and Griffiths 1996). Cameras were set to pause for 30 s between shots and to take 3 photos per trigger. The color of the photos varied according to the level of ambient light available, in that during the day photos were in full color, at dawn and dusk photos were in grayscale, and at night the photos were in black and white. “Night” was defined here by the appearance of black and white photographs, while “dawn” and “dusk” were defined as the appearance of grayscale photographs during times near sunrise and sunset, respectively. Here, we have chosen not to use the astronomical definitions, because we feel that the camera traps more accurately capture the light conditions experienced by the animals.

Following the methods of van Schaik and Griffiths (1996), only the first of consecutive photos containing one (or more than one) of the same individual(s) was included in the data, and a lapse of 1 h was used to delineate each photo event. We used 1 h to separate events because during behavioral observations, we noted that during nighttime activity animals tended to leave and return to their sleep sites within an hour. Thus, any triggers within 1 h could signify the same activity period, but triggers more than 1 h apart likely represented separate activity events. This method aids in achieving statistical independence between photo events (van Schaik and Griffiths 1996).

The average nighttime activity level (as measured through photo events) was calculated as per the following formula (van Schaik and Griffiths 1996):
$${\text{Average nighttime photo rate per 24 h period}} = \frac{\text{number of nighttime photos in one 24 h period}}{\text{number of cameras per 24 h period}}$$
Similarly, the average lemur nighttime activity level (as measured through photo rate) per month was calculated as per the following formula:
$${\text{Average nighttime photo rate per calendar month = }}\frac{\text{number of nighttime photos in one month per lemur group}}{\text{number of days in a month * number of cameras per day}}$$

Environmental data

Percentage of moon illuminated for the southern hemisphere was taken from the United States Naval Observatory Astronomical Applications Department website (2011). Temperature minima and maxima, along with millimeters of rainfall, were recorded daily at base camp using an Acurite digital weather station and rain gauges (Heidenhain Corporation, Schaumburg, IL, USA).

Phenological data were collected once per month on a total of 195 trees/shrubs, using methods reviewed by Ganzhorn et al. (2007). Nine 25 m × 1 m plots were established within home ranges of the lemur groups. All woody trees or shrubs within 1 m perpendicular on either side of the line were marked with a numbered tree tag. Presence and abundance of mature leaves, young leaves, flowers, and fruits (along with ripeness) were recorded as a score from 0 to 4, where coverage of 0 = bare tree, 1 = up to 25 %, 2 = 25–50 %, 3 = 50–75 % and 4 = more than 75 %. For each month, a “phenology score” was created by taking the average score from each tree and then an average from all trees. This value was rounded to the nearest whole number.

We used predator signs (camera trap photos, direct sightings, and opportunistically collected scats) to estimate the relative abundance of predators throughout the study period, which are reliable indicators of relative predator abundance as long as effort is consistent and standardized (Macdonald et al. 1999). Signs as indicators of abundance have been used to detect changes in populations of canids, felids, mustelids, procyonids, and ursids (see Gese 2001). The total numbers of predator signs were tallied monthly to create an estimate of predator presence.

Data analyses

Behavioral data

Chi-square analyses were used to assess variation between and within groupsʼ scan sampling scores of behavior during active periods of the day and nighttime, including feed/forage, locomote, groom, and other. Additionally, a Chi-square test was used to examine variation in the scan sampling data for the location of an animal relative to the ground. Sample sizes of these scan data were large (e.g. 4,000), which can increase the power of Chi-square, and thus artificially decrease the p value. Because of this, Cramer’s V was used for determining the strength of association within significant Chi-square data. In these instances, findings were only considered meaningful when Chi-square p values were equal to or less than 0.05, and Cramer’s V was greater than or equal to 0.15. Student’s independent t-test was used to assess variation in the average daily fiber intake during the dry and wet seasons, and a p value of 0.05 was considered statistically significant.

Camera trap and environmental data

We used linear regression to examine the relationship between nighttime activity and moon illumination, a variable that cannot be analyzed as an average per month. We also used linear regression to examine relationships between average monthly nighttime activity levels and the following: average temperature high and low, average precipitation, average daytime activity budgets, phenological score of plant parts, and predator presence. With these data, p-values that were less than or equal to 0.05 were considered significant. SPSS 19.0 was used for all statistical analyses.

Results

Behavioral data

When compared to nighttime active periods, during the day the lemurs spent more time traveling, but less time feeding, grooming, or engaging in other activities (Fig. 3). These differences in activity patterns between the day and night were significantly different from each other (χ2 = 335.68, df = 3, p < 0.001; Cramer’s V = 0.16). Moreover, during the day animals spent more time on the ground (25 %) when compared to the night (5 %) (Table 2), which was also significant (χ2 = 1033.97, df = 3, p < 0.001; Cramer’s V = 0.26). We found no differences between the lemur groups for activity pattern or time spent on the ground.
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Fig. 3

Activity budgets for the day (left) and night (right) active periods of ring-tailed lemurs

Table 2

Location scores from animals during active periods of the day and night

Location

Day

Night

% of daytime

% of nighttime

Off ground

8,097

4,600

72

95

Ground

2,763

244

25

5

During nighttime observation periods, females initiated activity by leaving their sleeping spot, and were followed by other group animals. Activity bouts usually lasted 1 h or less, before females went back to their sleeping spot, and there were up to three activity events like this per night. Both groups of lemurs ranged extensively throughout the day (2.02 km on average), yet during nighttime observations, most animals stayed within a 0.1 km diameter of their groupʼs sleep site. That being said, on two occasions we saw lone males leave their group at night, and there is one camera trap photo of a male in the “momma” baobab tree which is farther than 0.1 km from either of the groups’ sleep sites.

Plant food abundance changed dramatically over the study period, with lowest availability in September and October and highest in December and January (Table 3). During daytime observations animals concentrated on foods that were temporally abundant, however, at the night, proximity to sleep site appeared to limit which species were consumed. Average daily fiber intake was higher during the dry season (39 g/day), when compared to the wet season (29 g/day), although these data were not statistically significant (t = 0.809, df = 85, p = 0.421). Predator signs were most abundant in October and December, while markedly absent in February and March (Table 3).
Table 3

Monthly values for average phenological score (where 0 = lowest and 4 = highest), and predator presence (number of predator signs)

Month

Phenology

Predator presence

Sept

1

4

Oct

1

14

Nov

2

4

Dec

3

12

Jan

3

4

Feb

2

0

Mar

2

0

Camera trap and environmental data

Nighttime activity occurred several times each month beginning (Fig. 4), and there was significant variation between the nighttime activity levels per month, with an increasing trend throughout the study period (χ2 = 81.241, df = 6, p < 0.001). From 915 camera trap days, there were 253 separate nighttime photo events of ring-tailed lemurs (Table 1). Significant correlations were found between the lemurs’ nighttime activity and minimum temperature (r2 = 0.835, N = 6, p = 0.002), suggesting that these lemurs require a certain temperature minimum before they will engage in nighttime activity. No other significant relationships were found, including any between plant phenology and predator signs.
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Fig. 4

Camera trap photos of ring-tailed lemurs engaging in nighttime activities

Discussion

This study of wild Lemur catta at Tsimanampetsotsa National Park documents that these animals are active during the night. Nocturnal activity has now been documented in gallery forest ring-tailed lemurs (both anecdotally Jolly 1966; Sauther 1989) and systematically (Traina 2001; Donati et al. 2013), the ring-tailed lemurs of St. Catherine’s Island (Georgia, USA) (Parga 2011), and in the spiny forest habitats of this research, thus indicating that this genus should be considered cathemeral. These data provide context for evaluating the functional relevance of cathemeral activity in a comparative framework and with reference to the hypotheses of thermoregulation, predator avoidance, and dietary need.

Thermoregulation

The thermoregulation hypothesis predicts that cathemerality is an adaptive response enabling animals to minimize thermoregulatory stress and costs associated with maintaining temperature homeostasis (Curtis et al. 1999). This can result in behavioral avoidance of activity during overly hot or particularly cold ambient temperatures. Ellwanger and Gould (2011) note that daytime activity rapidly declines in L. catta once daytime ambient temperatures surpass 40 °C. Furthermore, Mutschler (2002) noted that H. alaotrensis avoided activity during particularly high daytime temperatures coupled with an increase in nighttime foraging. At TNP, however, very hot days were not significantly related to nighttime activity in the ring-tailed lemurs. This will be explored further below, with reference to the diet hypothesis.

Overnight low temperatures affect the activity patterns in some lemurs. Huddling and avoidance of activity during cold temperature periods have been seen in Hapalemur griseus alaotrensis (Mutschler 2002), and in the only cathemeral haplorrhine primate, Aotus aotus azarai (Fernandez-Duque 2003). However, the opposite cases, where correlations occur between low nighttime temperatures and nighttime activity, have been reported in several species of Eulemur (mongoz [Curtis et al. 1999), rufus [Curtis et al. 1999], rubriventer [Overdorff and Rasmussen 1995]). Donati and Borgognini-Tarli (2006) point out a divide in the activity patterns of cathemeral lemurs, relative to the level of seasonality in the habitat. Correlations between increased nocturnal activity and low overnight temperatures tend to occur in forests with low seasonality and small relative annual temperature fluctuations (3–4 °C), whereas the avoidance of activity during cold nights occurs in highly seasonal habitats where overnight temperature lows can be dramatic (up to 20 °C) (Donati and Borgognini-Tarli 2006), although there are exceptions to this statement (see Curtis et al. 1999). The ring-tailed lemurs in this study were more likely to be active at night when nighttime temperatures were warmer (>24 °C), and may have been limiting nighttime activity when temperatures were cooler (<21 °C). Ring-tailed lemurs live in the most seasonal forests in Madagascar, which can have sub-zero nighttime temperatures during cool portions of the year (Sussman 1991). Furthermore, ring-tailed lemurs are well known for using sunning behavior (Jolly 1966), and lemurs generally have behavioral and physiological adaptations that appear to reduce costs of homeostasis, such as low basal metabolic rate (Daniels 1984; Donati et al. 2011). Though ring-tailed lemurs can tolerate much cooler conditions, it is possible that the TNP lemurs prefer warmer temperatures and avoid the metabolic costs associated with maintaining body temperatures when ambient temperatures dip below 21 °C. If so, thermoregulation may be an important factor in the cathemeral behavior of ring-tailed lemurs and may vary depending on the habitat and amount of annual fluctuation in temperature.

Predator avoidance

The predator avoidance hypothesis predicts that animals will alter their activity patterns over the 24-h period as a mechanism for evading predation (Curtis et al. 1999). Day-active lemurs can be subject to significant levels of predation, both from diurnal raptors (Karpanty 2006) and cathemeral fossa (Hawkins 2003), but also domestic dogs, forest cats (Sauther et al. 2011), and humans (Golden 2009). Decreasing daytime activity may be an effective means for lemurs to minimize predation by diurnal raptors (van Schaik and Kappeler 1996; Curtis et al. 1999; Curtis and Rasmussen 2002). This may be especially important in deciduous forests when there is little or no canopy coverage, and raptors can easily see animals on the ground (Curtis et al. 1999). Several authors (Curtis et al. 1999; Donati et al. 1999; Rasmussen 1999) have noted a seasonal correlation between Eulemur spp. nighttime activity and lack of canopy in deciduous forests, along with a lack of seasonal shift in cathemeral activity by Eulemur spp. in non-seasonal evergreen rainforest. However, seasonal patterns in cathemerality have also been reported in Eulemur spp. in non-seasonal forests that do have leaf coverage year-round (Donati and Borgognini 2006). Ring-tailed lemurs in this study did not decrease daytime activity when leaf coverage was low and, in fact, nighttime activity was highest when there was the most leaf coverage. TNP is characterized by patchily distributed trees and dwarf flora, which may result in similar detection rates of lemurs by raptors, regardless of available foliage.

Colquhoun (2006) suggested that activity over a 24-h period may aid in the lemurs’ ability to be temporally cryptic and less predictable to predators, including fossa. However, other authors point out that all cathemeral lemurs tend to be predictably active during dawn and dusk (Curtis et al. 1999; Curtis and Rasmussen 2002; Donati and Borgognini 2006), which would presumably negate temporal crypsis (Donati and Borgognini 2006). The data presented here did not show relationships between cathemerality in ring-tailed lemurs and the relative presence of and cathemeral activity of fossa or other predators. It is possible that within this dry spiny habitat, although relative abundance of predators appears to fluctuate, absolute abundance of predators is low, and not influencing cathemeral patterns in these lemurs, or that relative abundance of predators does not directly correlate to the predation pressure experienced by the lemurs. It is also worth noting that the two resident breeding pairs of Polyboroides radiatus failed to rear chicks during the study period, and thus these raptors were unlikely to make nest deliveries of prey in the absence of offspring (Karpanty, personal communication), which would make finding prey remains unlikely, but could also temporarily relax predation pressure on lemurs.

Alternate lines of evidence suggest that L. catta were altering their activity patterns in order to evade predation. First, during nighttime activity, animals had a marked aversion to traveling on the ground. Ground travel is likely associated with increased predation by nocturnal cats, and potentially by fossa, and may be why lemurs avoided the ground at night (Curtis 2006). Second, nighttime activity was low during and following the birth season. Immature animals are particularly vulnerable to predation, as they donʼt necessarily have the skills or stealth required for detecting or evading predators. During this study (on October 26, 2010), a 4-week-old infant was found dead below the Vintany group’s sleep site. Given the state of decay, the infant had likely died the previous night. The infant’s ventral torso and abdominal internal organs were absent (presumably consumed by the predator) and it was not possible to determine its sex. There were two puncture wounds on the infant’s neck, with a distance of 16 mm between them. The punctures were likely from a wild forest cat (Felis sp.) or a fossa (Cryproprocta ferox), given that both of these animals can have an inter-canine distance of 16 mm (Sauther et al. 2011). Camera trap images show that the Vintany group was active after dark on October 20–23 and 25 (11:25 p.m., 11:41 p.m.), and then not again until November 21, 2010 (27 days later). On October 26 and October 27, 2010, the Vintany group did not sleep at their usual tree, but instead spent both nights sleeping north of the research camp, at the base of the Mahafaly plateau, which was approximately 1.2 km away. These are the only instances that we are aware of when Vintany did not sleep in their usual Ficus tree. The circumstances surrounding this infantʼs death are unknown and there are no camera trap images of predators, but this incident suggests that in response to an overnight predation event by a forest cat or fossa, the Vintany group avoided their usual sleeping spot for two nights and nighttime activity for nearly a month. In addition to the predated infant, the remains of three adult ring-tailed lemurs were found in predator scat (fossa and forest cat) from within the group’s overlapping home ranges. Of course, these remains could have been the result of scavenging rather than direct predation, but the lemurs’ behavior along with the evidence at hand (presence of predators, lemur bony remains found in predator scat) suggest animals are subject to predation, engage in predator avoidance, and that anti-predator behaviors and cathemerality should be explored further in future research.

Dietary needs

The diet hypothesis predicts that cathemerality is an adaptive response that enables animals to best utilize low-quality food resources during times of scarcity (Engqvist and Richard 1991; Overdorff 1993). For this hypothesis to be true, we would expect to see more cathemeral activity during periods when animals were eating markedly fibrous foods, or when food resources were most limited. Donati et al. (2009, 2007) note that low food availability and a highly fibrous diet were able to explain a significant portion of activity variation in E. collaris and E. collaris × E.f. rufus hybrids. However, many other authors have found no such associations (Curtis et al. 1999; Donati et al. 1999; Fernandez-Duque 2003). Rather than using nighttime activity as a mechanism to deal with food scarcity or highly fibrous foods (Engqvist and Richard 1991; Overdorff 1993), we suggest that with reference to diet, cathemeral lemurs may simply increase their caloric intake through nighttime feeding. Nocturnal activity, however, may be limited by other factors, such as thermoregulatory capacities or predator avoidance, which may explain why ring-tailed lemurs in this research were least active at night during the times when foods were most scarce.

We argue herein that L. catta is a cathemeral primate species. Warm overnight temperatures appear to promote nighttime activity in the ring-tailed lemurs at TNP. Ultimate factors of cathemerality in these ring-tailed lemurs likely enable animals to minimize thermoregulatory costs, increase food intake, and avoid predators. Cool nighttime temperatures and infant vulnerability to predation likely both deter nighttime activity during some months, though we are unable to completely separate the two factors. Given the potential importance of cathemerality on lemur ecology, cathemeral behavior should be investigated further in any species in which occasional flexible activity pattern has been reported. This information would be particularly pertinent for Varecia which, along with Lemur, is regarded as diurnal, but has been reported as nighttime active (Morland in Hoffmann et al. 1992; Balko in Wright 1999; Britt in Donati and Borgognini 2006). If Varecia were cathemeral along with Eulemur, Hapalemur and now Lemur, parsimony would predict that the ancestral state of the Lemuridae clade is also cathemeral. This knowledge could advance our understanding on the evolution of flexible 24-h activity patterns in lemurs, and therefore other primates, given their shared physiology and phylogeny.

Acknowledgments

The authors thank the government of Madagascar, Madagascar National Parks and the University of Toliara, Madagascar, for granting us permission to work at Tsimanampetsotsa National Park. We are grateful for the excellent research assistance provided by Megan Hoopes and Bronwyn McNeil. We thank the Beza Mahafaly animal darting team (Enafa Efitroaromy, Edidy Ellis, and Elahavelo) and the Tsimanampetsotsa National Park ecological monitoring team (Razanajafy Olivier, Lauren, Stephan), and local experts Fiti and Francisco. We are extremely appreciative to the Lanto, Bakira Ravorona, and their families for their facilitation, assistance, and friendship. We thank the University of Hamburg and Joerg Ganzhorn for the plant food nutritional analyses. We also thank Chia Tan and two anonymous additional reviewers for their feedback, which improved this manuscript. Last, we thank the lemurs of Tsimanampetsotsa, without whom this research would have not been possible. We, the authors, confirm that there is no conflict of interest that has influenced our objectivity. Grant sponsorship: NSF DDIG 1028708, NSERC PGS 296264, National Geographic Society Committee for Research and Exploration Grant 88011, and American Society of Primatologists 2009 Small Research Grant awarded to MML. NSF BCS 0922645, ND EPSCoR, University of North Dakota Faculty Seed Money Council Award, University of Colorado (IGP, CRCW), International Primatological Society, Primate Conservation Inc., American Society of Primatologists, to MLS and/or FPC. All data presented in this manuscript complied with the protocols approved by the Institutional Animal Care and Use Committee at the University of Colorado Boulder (Protocol number 1002.09), and the ethical standards of treatment as laid down by the Primate Society of Japan.

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© Japan Monkey Centre and Springer Japan 2013