Introduction And History

The primate order has traditionally been subdivided into diurnal and nocturnal species, a dichotomy that is broadly reflected in their taxonomic division into haplorhines and strepsirhines. The former are predominantly day-active, while the latter are predominantly night-active, with notable exceptions found in both groups. The focus of this chapter will be on the strepsirhine true lemurs (Lemuridae), the majority of which are neither diurnal nor nocturnal, but exhibit a mixture of daytime and nighttime activity.

In the 1960s, Petter (1962) first noted that the activity cycles of some lemurids (Varecia, Hapalemur, Eulemur) were neither diurnal nor nocturnal and preferred the use of the term "crepuscular." Studies conducted both in the field and in captivity during the 1970s revealed that this activity cycle was characterized by substantial nocturnal activity, in addition to peaks of activity around dawn and dusk, and bouts of diurnal activity (Table 1). The first rigorous, longer-term observations throughout the 24-hr period were conducted on Eulemur fulvus ssp. by Conley (1975) in captivity and by Tattersall (1979) on Mayotte, Comoros Islands.

Tattersall did much to stimulate further research, also proposing a new term, "cathemerality" (meaning "through the day"), to describe this activity rhythm (Tattersall, 1987): "The activity of an organism may be regarded as cathemeral when it is distributed approximately evenly throughout the 24 h of the daily cycle, or when significant amounts of activity, particularly feeding and/or traveling, occur within both the light and the dark portions of that cycle." More reports on cathemerality in lemurs appeared in the 1980s, marking the start of a plethora of studies since the 1990s (Table 1). Most notably, recent developments in technology

Deborah J. Curtis • School of Human & Life Sciences, Roehampton University, London SW15 4JD, United Kingdom

Table 1. Summary of studies reporting on cathemerality in the Lemuridae in the 1970s, 1980s, and 1990s to present

Species

Reference(s)

1970s

E. fulvus rufus E. f fulvus E. f albifrons Eulemur mongoz

E. f. mayottensis

Hapalemur aureus E. f. rufus E. rubriventer E. f. fulvus E. mongoz E. f. sanfordi E.coronatus E. f. albifrons

E. f. fulvus E. f. albifrons E. f. mayottensis E. f. sanfordi E. f. collaris E. f. albocollaris E. mongoz E.coronatus E. rubriventer E.macaco macaco L. catta

H. griseus griseus H. griseus alaotrensis H. simus Varecia variegata variegata

Sussman, 1975

Harrington, 1975; Tattersall and Sussman, 1975 Conley, 1975

Tattersall and Sussman, 1975; Tattersall, 1976; Sussman and

Tattersall, 1976; Harrington, 1978 Tattersall, 1977, 1979

1980s

Meier et al., 1987 Meyers, 1988 Overdorff, 1988 Andriatsarafara, 1988 Andriatsarafara, 1988 Wilson et al., 1989 Wilson et al., 1989 Erkert, 1989 1990s to present

Overdorff and Rasmussen, 1995; Donati et al., 1999, 2001;

Gerson, 2000; Kappeler and Erkert, 2003 Rasmussen, 1999; Ratsirarson and Ranaivonasy, 2002 Erkert and Cramer, 2006; Traber and Müller, 2006 Tarnaud, 2006 Freed, 1996

Donati and Borgognini-Tarli, 2006 Johnson, 2002

Curtis, 1999; Rasmussen, 1999 Freed, 1996

Overdorff and Rasmussen, 1995

Colquhoun, 1993, 1998; Andrews and Birkinshaw, 1998 Traina, 2001

Santini-Palka, 1994; Ratsirarson and Ranaivonasy, 2002

Mutschler, 1998; Olivieri, 2002

Santini-Palka, 1994; Tan in Wright, 1999

Morland in Hoffmann et al., 1992; Balko in Wright, 1999

have seen dedicated long-term and continuous 24-hr recording of cathemeral activity using accelerometer/data logger devices in the field (Kappeler and Erkert, 2003; Fernandez-Duque and Erkert, 2006).

Most data on cathemerality have been collected within the framework of behavioral and ecological studies, with little research into its physiological and morphological bases. Recent research into the evolution of primate activity patterns and visual morphological adaptations gives us an insight into how lemurs cope with the different challenges posed by night and day. Visual morphologies vary between diurnal and nocturnal primates (Martin, 1990; Kay and Kirk, 2000; Heesy and Ross, 2001; Kirk, 2006). Nocturnal primates generally possess a tape-tum lucidum, large relative orbit size, high degrees of retinal summation (large numbers of photoreceptor cells per ganglion), large curved corneas, and a high proportion of rods relative to cones, all of which increase sensitivity. Diurnal primates generally possess an area centralis (strepsirhines) or a fovea (haplorhines), small relative orbit size, low degrees of summation, small flattened corneas, and an increased proportion of cones to rods, all of which increase acuity. Cathemeral primates appear ambiguous as they exhibit a mixture of these characteristics (tape-tum generally absent or reduced; area centralis present or absent; high, low, or intermediate retinal summation; intermediate cornea size/shape; intermediate rod/cone ratios). It is precisely this intermediate visual morphology that permits these primates to cope with the different demands posed by night and day (Kirk, 2006).

Cathemerality is one of a number of lemur behavioral traits found in few, if any, other primates (Wright, 1999). The only other primate that exhibits regular day-night activity is Aotus azarai in seasonal habitats in the New World (Wright, 1989; Fernandez-Duque, 2003; Fernandez-Duque and Erkert, 2006). In this chapter, I will investigate the following questions: What are the proximate cueing mechanisms underlying cathemerality? What is its adaptive value? How and when might cathemerality have evolved in lemurs and why did it evolve?

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