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Cathemeral Activity Patterns of the Blue-Eyed Black Lemur Eulemur Macaco Flavifrons in Intact and Degraded Forest Fragments

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Cathemeral Activity Patterns of the Blue-Eyed Black Lemur Eulemur Macaco Flavifrons in Intact and Degraded Forest Fragments ENDANGERED SPECIES RESEARCH Printed October 2007 Vol. 3: 239–247, 2007 Endang Species Res Published online September 12, 2007 Cathemeral activity patterns of the blue-eyed black lemur Eulemur macaco flavifrons in intact and degraded forest fragments Nora Schwitzer1, Werner Kaumanns1, Peter C. Seitz2, Christoph Schwitzer3,* 1Working Group Primatology, Zoologischer Garten Köln, Riehler Strasse 173, 50735 Köln, Germany 2Department of Biophysics, Technische Universität München, James Franck Strasse, 85748 Garching, Germany 3Bristol Zoo Gardens, Clifton, Bristol BS8 3HA, UK ABSTRACT: This study describes the activity pattern of the blue-eyed black lemur Eulemur macaco flavifrons for the first time and investigates the parameters, such as season or habitat, that may influ- ence the distribution of activity over the 24 h cycle. Four groups of E. m. flavifrons in 2 forest frag- ments with different degrees of degradation were followed for 24 h mo–1 over a 7 mo period between July 2004 and July 2005. Blue-eyed black lemurs exhibited a bimodal activity pattern which peaked during the morning and evening twilight. The groups consistently showed activity bouts both during the day and at night, a behaviour that corresponds to Tattersall’s (1987) definition of cathemerality. The proportion of illuminated lunar disc and the nocturnal illumination index were positively associ- ated with the amount of nocturnal activity. Total activity, both diurnal and nocturnal, was signifi- cantly higher in the secondary than in the primary forest. In view of our results, the cathemeral behaviour of E. m. flavifrons may best be explained as flexible responses to a framework of varying environmental factors, each of which may enhance or inhibit activity within the lemurs’ range of adaptability. This temporal behavioural plasticity may be an adaptation to an erratic and severe climate with frequent droughts and cyclones and unpredictable resource availability. KEY WORDS: Eulemur macaco flavifrons · Cathemerality · Activity pattern · Nocturnal illumation index · Primary forest · Secondary forest Resale or republication not permitted without written consent of the publisher INTRODUCTION macaco, E. mongoz, E. rubriventer, E. rufus and E. san- fordi (Wright 1999, Vasey 2000, Donati & Borgognini- Until about 30 years ago, primates were classified as Tarli 2006, Colquhoun 2006). Tattersall (1987) formally either diurnal or nocturnal (Curtis et al. 2006). Begin- introduced the term ‘cathemeral’: ‘the activity pattern ning in the late 1970s, however, it was found that some of an organism can be regarded as cathemeral when it lemur species of the genus Eulemur regularly exhib- is about evenly distributed over the 24 h daily cycle, or ited both nocturnal and diurnal activity; i.e. they were when significant amounts of activity, particularly feed- active throughout the 24 h cycle (Curtis & Rasmussen ing and/or travelling, occur within both light and dark 2006, Tattersall 2006). This pattern was first described portions of the cycle’ (p. 201). A cathemeral activity in the wild by Tattersall (1979) for Eulemur fulvus on cycle has since also been reported in a number of the island of Mayotte, between northern Madagascar other lemur genera, such as Hapalemur alaotrensis and northern Mozambique. Later the pattern was also (Mutschler et al. 1998, Mutschler 2002) and Prolemur also described for the congeneric species E. albifrons, simus (Tan 2000, Grassi 2001), and in neotropical owl E. albocollaris, E. collaris, E. coronatus, E. macaco monkeys of the genus Aotus (Wright 1994, Kinzey *Corresponding author. Email: [email protected] © Inter-Research 2007 · www.int-res.com 240 Endang Species Res 3: 239–247, 2007 1997, Fernandez-Duque 2003). Furthermore, cathe- secondary forest. The aims of our study were to merality may occur in 2 howler monkey species, provide a description of the blue-eyed black lemurs’ Alouatta pigra and A. palliata (Dahl & Hemingway activity pattern in their natural environment and to 1988, Wright 1994, Curtis & Rasmussen 2002, investigate parameters that may influence the dis- Mutschler 2002, Fernandez-Duque 2003, Kirk 2006). tribution of activity over the 24 h cycle. Furthermore, In the genus Eulemur, cathemerality may occur in 3 we aimed to compare the behaviour and activity different modes (Curtis & Rasmussen 2002): (1) varying budgets of this taxon in the dry and wet seasons seasonally, with nocturnal activity predominantly and when living in primary or secondary forest exhibited during one season and diurnal activity pre- fragments. dominating during another (Tattersall 1979, 1987, Curtis & Zaramody 1998, Rasmussen 1998a,b, Curtis et al. 1999, Curtis & Rasmussen 2006, Tarnaud 2006); MATERIALS AND METHODS (2) shifting seasonally, from diurnal activity in the austral summer to 24 h activity in the austral winter Study site. The study was conducted in the Ankarafa (Rasmussen 1999, Donati et al. 1999, Donati & Bor- Forest, situated in the SW part of the UNESCO Bios- gognini-Tarli 2006); (3) 24 h activity throughout the phere Reserve and Protected Area on the Sahamalaza year with no link to photoperiod and seasonal varia- Peninsula. Sahamalaza is part of the Province tion of food resources (Colquhoun 1997, 1998). In the Autonome de Mahajanga, NW Madagascar, and third group, the duration of nocturnal activity is posi- extends from 13° 52’ S to 14° 27’ S and from 47° 38’ E to tively correlated with lunar phase and nocturnal illu- 47° 46’ E (WCS/DEC 2002). The Ankarafa Forest mination index (Colquhoun 1997, Donati et al. 2001a,b, includes primary and secondary forest fragments Donati & Borgognini-Tarli 2006, Fernandez-Duque & which harbour one of the largest populations of blue- Erkert 2006). eyed black lemurs still remaining in the wild. The pre- According to Erkert & Cramer (2006), Eulemur alb- sent study was conducted in 1 primary forest fragment ifrons is endogenously regulated by a circadian timing and 1 secondary forest fragment. system that seems to obey the same rules as for noc- Climate and nocturnal luminance. The climate at turnal mammals, where the daily light:dark cycle is the the study site is strongly seasonal with a cool, dry sea- most efficient zeitgeber and synchronises this endo- son lasting from May to September and a hot, rainy genous rhythm to the external 24 h day. In a 14 mo season from October to April. Mean annual precipita- study on E. collaris in the Malagasy littoral forest, tion is 1600 mm, with the most rain falling in January Donati & Borgognini-Tarli (2006) demonstrated that and February. Average monthly temperatures range dusk seems to act as the primary zeitgeber, coordi- from 20.6°C (August) to 32.0°C (November) with a nating the onset of the animals’ evening activity mean annual temperature of 28.0°C. throughout the entire year. During the study period, cloud cover and wind The blue-eyed black lemur Eulemur macaco flav- strength were recorded qualitatively. Categories used ifrons is a critically endangered lemur taxon (CR A1cd, for assessing cloud cover were sunny (no clouds), B1+2bc; Ganzhorn et al. 2000) that exclusively inhab- cloudy (≤25% of the sky clouded), overcast (>25% but its the few remaining forest fragments on and east of ≤75% clouded), and heavily overcast (>75% clouded). the Sahamalaza peninsula (Sofia region, NW Mada- Wind strength was recorded as windy, stormy, rainy, gascar). The subspecies was only rediscovered in 1983 rainswept or thunderstorm. after more than a century of uncertainty about its exis- The nocturnal illumination index Inorm was calcu- tence, and it is still one of the least-studied lemurs lated using a modified version of the method given in (Koenders et al. 1985, Meier et al. 1996). Whereas the Curtis et al. (1999). For each night t the duration of other taxa of this genus (including the nominate sub- moonshine (dM) between sunset and sunrise was mul- species E. m. macaco) have all been described as tiplied with a value corresponding to the illuminated showing activity patterns that involve both day and fraction of the moon (fM), which was modelled by a night activity, E. m. flavifrons remains the only Eule- sine curve matching the given dates for new, full, mur whose activity pattern in the wild is still unknown. waxing and waning moon. Data for moon phase and In captivity, blue-eyed black lemurs show cathemeral times for sunset and sunrise as well as moonrise and activity similar to that of other Eulemur species moonset were obtained from the US Naval Ob- (Schwitzer 2003). servatory Calendar (http://aa.usno.navy.mil/), using For this study, we collected data on the behaviour Ankarafa’s geographical coordinates (47° 45’ E, and activity budgets of 4 groups of blue-eyed black 14° 22’ S, GMT + 3 h) (Donati & Borgognini-Tarli lemurs living in 2 different forest fragments, one 2006). The index was normalized to the average over mainly primary forest and the other predominantly the calendar year I0. Schwitzer et al.: Cathemeral activity of Eulemur macaco flavifrons 241 Sky condition (clouds) was taken into account by significant sampling bias because even quiet feeding multiplying with a factor C between 0 (heavily over- was indicated by debris falling to the ground (Curtis et cast) and 1 (clear sky) using the following equation: al. 1999). Our nocturnal observations may have slightly underestimated the active time of the lemurs because I (t) = d f C/I norm M M 0 individuals sitting still with their eyes open (classified where I0 = ∑dMfMC)/# days in calendar year. During as active during the day) are likely to have been nocturnal observations the illumination index ranged recorded as inactive during the night. Judging from between 0.2 and 2.8. diurnal activity budgets, however, this should only Observations. Four groups of Eulemur macaco flav- have underestimated the lemurs’ nocturnal activity by ifrons were followed for 24 h mo–1 during each of 7 less than 5%. In this study, we considered activity to be selected mo between July 2004 and July 2005, alto- nocturnal if it occurred between 6 pm and 6 am even gether representing 600 h of observations spanning though day length ranges from 11 h 20 min (dry sea- the dry and the rainy season.
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