Geographic Variation in Populations of Microcebus ... - Springer Link

C 2006) International Journal of Primatology, Vol. 27, No. 4, August 2006 ( DOI: 10.1007/s10764-006-9055-y

Geographic Variation in Populations of Microcebus murinus in Madagascar: Resource Seasonality or Bergmann’s Rule? ¨ U. Ganzhorn1 Petra Lahann,1,3 Jutta Schmid,2 and Jorg Received March 10, 2004; revision August 23, 2004; 2nd revision March 22, 2005; 3rd revision June 8, 2005; accepted June 20, 2005; Published Online August 5, 2006

Gray mouse lemurs (Microcebus murinus) occur in western Madagascar from the evergreen littoral rain forests at the southern tip of the island to the seasonal dry deciduous forests of the west and northwest. The wide geographic distribution allows researchers to investigate whether ecogeographic variations reflect adaptations to ambient temperatures, as a proxy for constraints of thermoregulation, or to rainfall, as a proxy of food availability. We compared body mass, number of litters/yr, and longevity for 3 populations: 1 from the evergreen littoral rain forest of the south (Mandena: annual mean temperature 23◦ C, 1600 mm rain/yr), 1 from the dry deciduous forest of the west (Kirindy/CFPF: 25◦ C, 800 mm), and 1 from the dry deciduous forest of northwestern Madagascar (Ampijoroa: 27◦ C, 1200 mm). Body mass decreases with increasing ambient temperature from south to north (Mandena > Kirindy/CFPF > Ampijoroa). The number of litters/yr was highest in the littoral rain forest (2 or 3 litters/yr) and decreased with decreasing rainfall (Mandena > Ampijoroa > Kirindy/CFPF). Life expectancy is lowest in the littoral forest (13% recaptures of mouse lemurs between years) and high (ca. 30–40% recaptures between years) in the dry forests (Mandena < Kirindy/CFPF and Ampijoroa). We postulate that constraints of thermoregulation result in the latitudinal gradient of body mass. Reduced resource 1 Department

of Animal Ecology and Conservation, Biozentrum Grindel, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany. of Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany. 3 To whom correspondence should be addressed; e-mail: [email protected]. 2 Department

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productivity or seasonality is reflected in differences in reproductive rates, which seemed to be traded off against longevity. Thus body mass, longevity, and reproductive parameters respond differently to ambient conditions. KEY WORDS: body mass; lemurs; life history traits; littoral rain forest; Madagascar; Microcebus murinus; morphometry; reproduction.

INTRODUCTION Lemurs show substantial geographic size variation in Madagascar (Albrecht et al., 1990; Godfrey et al., 1999; Lehman et al., 2005; Ravosa et al., 1993). Forms of the evergreen rain forests are larger than congeneric species of the dry deciduous forests, and body mass declines within each vegetation type with decreasing annual rainfall or increasing length of the dry season. The picture holds for lemurs in general (Albrecht et al., 1990), for different Propithecus spp. (Lehman et al., 2005; Ravosa et al., 1993), and for size reduction of extant lemur species in historical times (Godfrey et al., 1999). Wright (1999; cf. Brockman and van Schaik, 2005) interpreted the changes in body mass as a consequence of resource productivity and resource seasonality, which might be a key component for the evolution of lemur life history traits. More seasonal habitats should favor smaller species that might still find enough to eat during the lean dry season whereas forest productivity might be insufficient to support larger species during the lean time. Ambient temperatures pose another constraint on body mass. Bergmann’s rule describes an increase in body mass of endotherms with decreasing ambient temperature, interpreted as a consequence of thermoregulation. Larger forms are favored metabolically in colder climates because of the more favorable surface-to-volume ratios of larger species, which reduces thermal radiation from the individual to the cold environment. Though the argument is based on energy requirements to maintain normothermy in cold climates, the same pattern might arise as a response to stressfully high temperatures. In woodrats and pocket gophers the tolerance of high temperature decreased with increasing body mass (Hadley, 1997; Smith et al., 1995). As a consequence significant changes in body mass occurred at very small changes of ambient temperatures of just a few degrees C during the Holocene (Brown and Lomolino, 1998), which matches the findings of Godfrey et al. (1999) for Malagasy lemurs. Researchers had not considered ambient temperatures as a possible factor influencing variation in body mass of lemurs. We investigated the possible contribution of resource productivity/seasonality and of ambient temperature on ecogeographic size variation

Geographic Variation in Microcebus murinus

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and life history traits of gray mouse lemurs (Microcebus murinus). The gray mouse lemur is a suitable model because it ranges from the evergreen littoral rain forests of the southern tip of Madagascar in the region of Tolagnaro (Fort Dauphin; Martin, 1972, 1973) at least up to the National Park of Ankarafantsika, with its deciduous forests and an extended dry season (Randrianambinina et al., 2003; Tattersall, 1982). Molecular analyses of mitochondrial DNA sequences indicate differences between populations of Microcebus murinus (Pastorini et al., 2001; Yoder et al., 2000), but they do not reach the specific level, offering the opportunity to study adaptations and flexibilities within instead of between species with different evolutionary histories. Primatologists have studied Microcebus murinus intensively at the northern limit of its range in the dry deciduous forests of Ampijoroa ` (Pages-Feuillade, 1988; Radespiel et al., 2001, 2003a,b; Rendigs et al., 2003; Schmelting et al., 2000). In the center of its range researchers have studied it north of Morondava (Charles-Dominique et al., 1980) and at Kirindy/CFPF (Eberle and Kappeler, 2002, 2004; Fietz, 1995, 1998, 1999; Ganzhorn and Schmid, 1998; Schmid, 1997; Schmid and Kappeler, 1998). We still know little from the evergreen littoral rain forest in the south at Mandena (Martin, 1972, 1973; Ramanamanjato and Ganzhorn, 2001). Ampijoroa, Kirindy/CFPF, and Mandena cover a wide range of resource productivity/seasonality and ambient temperatures (Ampijoroa: annual mean temperature 27◦ C, annual precipitation: 1200 mm; Kirindy/CFPF: 25◦ C; 800 mm; Mandena: 23◦ C, 1600 mm). We used annual rainfall as a proxy for productivity and seasonality. Because annual rainfall correlates closely with the number of dry months, it was not possible to separate resource productivity from resource seasonality. At rainfall < 2500 mm/yr forest productivity increases with rainfall and declines with increasing number of dry months (measured as the number of months with < 100 mm of rain; Kay et al., 1997; van Schaik et al., 2005). We investigated the effects of resource productivity vs. Bergmann’s rule, according to which we would expect a gradual decline of body mass and a monotonic change of reproductive traits from Mandena/Fort Dauphin (23◦ C) to Kirindy/CFPF (25◦ C) to Ampijoroa (27◦ C). According to the resource productivity hypothesis, body mass and reproductive characteristics should not follow the latitudinal gradient but change from Mandena (1600 mm) to Ampijoroa (1200 mm) to Kirindy/CFPF (800 mm rainfall/yr). To test the hypotheses we first extended Martin’s (1972) database on the natural history of Microcebus murinus in the evergreen littoral rain forest at the southern and eastern extreme of its range. We then compared our results with published data on morphological and reproductive traits of Microcebus murinus in Ampijoroa and Kirindy/CFPF.

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We used the comparison to understand better the role of resource productivity/seasonality and of ambient temperature in the evolution of ecogeographic variation in size and life history traits of lemurs.

METHODS Study Sites Mandena is an evergreen littoral rain forest (24◦ 56 S, 46◦ 59 E, 5–20 m above sea level), 10 km northeast of Tolagnaro (Fort Dauphin, Fig. 1). The study area of 8 ha (400 × 200 m) was in the degraded primary forest fragment M15/M16 of about 180 ha with thick undergrowth and a broken canopy at a height of ca. 10–15 m. Trails subdivide the site into 50 × 50 m quadrants. Rainfall averages 1600 mm/yr and there is no distinct dry season. The average temperatures per month are 20◦ –26◦ C with an annual mean of 23◦ C (Lewis Environmental Consultants, 1992; Ramanamanjato and Ganzhorn, 2001). Kirindy/CFPF (20◦ 03 S, 44◦ 39 E) and Ampijoroa (16◦ 35 S, 46◦ 82 E; Fig. 1) are dry deciduous forests in western and northwestern Madagascar. Kirindy/CFPF is 18–40 m a.s.l. with about 800 mm of rain/yr. The average temperatures per month are 21◦ –27◦ C with an annual mean of 24.7◦ C (Sorg and Rohner, 1996). Ampijoroa (200 m a.s.l.) is a forest on sandy soil with annual rainfall of 1200 mm. The average temperatures per month are 24◦ – 28◦ C with an annual mean of 27◦ C (Schmelting, 2000; Zimmermann et al., 1998). Rainfall at both dry forest sites is concentrated between December and March.

Trapping We captured Microcebus murinus at Mandena in July 2000, monthly between October 2000 and February 2001, June and July 2001, and between February 2002 and January 2004. We set 160 Sherman live traps (7.7 × 7.7 × 23 cm) at 25-m intervals in an area of 400 m × 200 m, 2 traps at each place (1 at the ground and 1 at 1–2 m above the ground in the branches). We baited traps with banana and set them for 4 consecutive nights each month, per standard procedure for documenting population dynamics of Microcebus murinus over the years in Mandena and Kirindy/CFPF. We do not know whether this has negative effects on social interactions and whether or not and how it influences population dynamics. Outside the birth season and time of lactation we checked traps at dawn.


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Fig. 1. Distribution of Microcebus murinus (shaded) and geographical locations of Ampijoroa, Kirindy/CFPF and Mandena. (Modified from Tattersall 1982.)

During the birth season we checked traps repeatedly during the night (between November and February). We anesthetized captured mouse lemurs with subdermal injections of 0.03 ml of Ketavet [100 mg/ml]) for better handling. We sexed, weighed, and measured the anesthetized mouse lemurs according to Schmid and Kappeler (1994) and marked them individually with subdermally implanted microtransponders (type ID-100, Fa. Telinjet, D-Roemerberg). We determined the female reproductive condition via examination of nipples and vulva and by abdominal palpation to check for pregnancy. We anesthetized subjects for 10–30 min, kept them in Sherman traps with banana for recovery from anesthesia, and released them at dusk or at dawn at their respective trapping site.

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We included only adults in the morphometric and body mass comparison. We classified mouse lemurs with body mass < 45 g as juveniles and excluded them from analyses. They were also smaller than individual subjects as adults. If we captured an individual several times per month, we used its mean body mass for statistical analyses.

Observations We used detailed observations to determine time and number of litters. We equipped 12 (5 females and 7 males) Microcebus murinus with radiocollars (Biotrack, UK-Dorset; 2.5 g) and radiotracked them via a TR-4 Receiver with a RA-14K Antenna (Telonics, Mesa, AZ) between November 2000 and January 2001. We tracked the subjects between 1800 and 2400 h for 9–130 h in 23 nights and supplemented the observations with data collected between February–April 2002 and October 2003–March 2004 during 120 h of census walks.

Intersite Comparisons, Data Extraction, and Data Analysis We took data from the literature for comparisons between sites (Table I) and partially read from graphs. For statistical analyses we used EXCEL, SIGMA-PLOT, and SPSS, with results listed as mean ± standard deviation (SD). For the dry forest populations (Kirindy/CFPF and Ampijoroa), only means, standard errors, or standard deviations are published. To allow statistical comparisons, we transformed standard errors and standard deviations of the data from all sites into 95% confidence Table I. Origin of data used for comparisons between populations Comparison of Morphometric data Body mass Recapture data

Number of litters

Kirindy/CFPF

Ampijoroa

Schmid and Kappeler (1994; Table I) Zimmermann et al. (1998; Table I) Schmid (1997; Table II) Schmelting (2000, Fig. 6) Schmid and Kappeler (1998, Fig. 2) Ganzhorn and Schmid (1998; p. 794) Schmelting (2000; pp. 44–45) Lutermann (2001; p. 46) Reimann (2002; pp. 66–70) Ehresmann (2000; pp. 69–77) Eberle and Kappeler (2004)

Schmelting et al. (2000; p. 168) Lutermann (2001; Fig. 9)


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intervals. SAS/STATS (1987) recommends visual comparisons of multiple groups based on means and confidence intervals as a valid statistical procedure. RESULTS Morphology The morphological comparisons are based on 127 Microcebus murinus of Mandena, 52 of Kirindy/CFPF, and 57 of Ampijoroa (Table II) with the exception of body mass. According to the confidence intervals there is no significant difference in the hindfoot length between Mandena and Kirindy/CFPF. Data for Ampijoroa are not available for the measurement. Head length does not differ between all 3 regions. Head width is significantly larger in Mandena than in Kirindy/CFPF and Ampijoroa. Ear length is similar in Ampijoroa and Mandena, but both are significantly longer than in Kirindy/CFPF. The ear width is similar in Mandena and Kirindy/CFPF, but differs significantly from Ampijoroa. The tails of Microcebus murinus from Kirindy/CFPF are significantly longer than the tails of M. murinus from Mandena, which are significantly longer than tails of their conspecifics from Ampijoroa (Table II).

Body Mass In Mandena, body mass of Microcebus murinus varied significantly between sexes and months (Table III; Fig. 2), which matches the results from Ampijoroa and Kirindy/CFPF (Fietz, 1998; Lutermann, 2001; Schmelting et al., 2000; Schmid and Kappeler, 1998). Therefore we compared body masses separately for each month and for males and females. There is no published datum for females of Microcebus murinus at Ampijoroa. The males of Microcebus murinus from the littoral forest in Mandena are significantly heavier than conspecifics in the dry forests in September, October, November, and December (Table III; Fig. 2). In June, July, and October males of Kirindy/CFPF are significantly heavier than males of Ampijoroa. Females from Mandena weighed significantly more from August to January than females in the dry forest of Kirindy/CFPF (Table III; Fig. 2). In Mandena reproduction starts earlier than in Kirindy/CFPF and the females have 2 or 3 litters/yr. Thus many females captured in September, October, and January were pregnant and therefore heavier than the

132.5 32.4 35.0 21.8 23.5 17.6

Tail length Hindfoot length Head length Head width Ear length Ear width

a Data from Schmid and Kappeler (1994). b Data from Zimmermann et al. (1998).

Mean

Variables (mm) 7.4 1.4 1.2 1.3 1.4 1.4

SD

Mandena n = 127

131.2–133.8 32.1–32.7 34.8– 35.2 21.6–22.0 23.3–23.7 17.4–17.8

C95% 143.9 32.2 35.2 21.2 22.4 17.5

Mean 9.0 1.2 1.4 1.0 1.6 1.1

SD 141.4–146.4 31.9–32.5 34.8–35.6 20.9–21.5 22.0–22.8 17.2–17.8

C95%

Kirindy/CFPFa n = 52

8.1 2.1 1.9 2.0 1.2

34.5 20.6 23.9 15.0

SD 128.4

Mean

33.9–35.1 20.1–21.1 23.4–24.4 14.7–15.3

126.2–130.6

C95%

Ampijoroab n = 57

Table II. Comparison of morphometric measurements of Microcebus murinus in Mandena, Kirindy/CFPF, and Ampijoroa (mean, standard deviation, and 95% confidence interval)

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64.8 ± 6.2 (58.3–71.3/6) 57.1 ± 5.9(52.9–61.3/10) 57.7 ± 3.9(54.1–61.3/7) 56.6 ± 3.7 (53.1–60.1/7)∗∗ 58.5 ± 6.4 (55.5–61.5/20)∗∗ 59.5 ± 7.5 (57.3–61.7/46) 64.7 ± 7.5 (61.2–68.2/20)∗,∗∗ 75.6 ± 11.0 (68.2–83.0/11)∗,∗∗ 72.2 ± 6.4 (68.9–75.5/17)∗,∗∗ 76.9 ± 7.9 (70.8–83.0/9)∗,∗∗

61.8 ± 2.3 (59.5–64.0/6) 58.3 ± 3.0 (54.8–61.7/5) 59.4 ± 11.5 (51.8–67.0/11) 58.7 ± 11.2 (55.0–62.4/38) 58.8 ± 13.1 (54.1–63.5/32) 58.1 ± 8.3 (55.1–61.1/31)∗∗ 59.3 ± 10.2 (55.8–62.8/36)∗∗ 58.7 ± 7.2 (55.8–61.6/26) 56.8 ± 7.6 (53.9–59.7/28) 64.9 ± 10.1 (62.0–67.8/50)∗∗ 51.2 ± 5.4 (47.8–54.6/12) 59.1 ± 6.3 (54.3–63.9/9)

Kirindyb

Males

56.5 ± 5.5 (52.0–61.0/8) 57.8 ± 5.9 (51.0–64.6/5) 53.3 ± 6.0 (47.3–59.3/6) 52.3 ± 6.3 (49.6–55.0/24) 51.3 ± (47.2–55.4/16) 48.8 ± 7.2 (45.3–52.3/19) 51.5 ± 6.5 (48.8–54.2/25) 55.8 ± 6.3 (52.7–58.9/18) 53.8 ± 6.0 (50.8–56.8/18) 54.3 ± 5.0 (52.1–56.5/23) 53.5 ± 6.5 (50.5–56.5/20) 55.5 ± 5.5 (51.6–59.4/10)

Ampijoroac

Kirindyb 66.8 ± 2.0 (65.4–68.1/11) 68.3 ± 2.8 (66.6–69.9/12) 74.8 ± 20.4 (46.5–103.1/4) 69.9 ± 17.7 (63.3–76.5/30) 62.4 ± 17.2 (54.8–70.0/22) 60.8 ± 15.9 (50.8–70.8/12) 59.4 ± 5.8 (55.3–63.5/10) 51.4 ± 4.5 (45.2–57.6/4) 50.1 ± 2.7 (47.4–52.8/6) 61.0 ± 6.5 (58.4–63.6/26) 53.5 ± 7.3 (49.9–57.1/18) 73.3 ± 10.7 (67.2–79.4/14)

Females

99.3 ± 12.0 (88.8–109.8/8)∗ 83.3 ± 6.5 (67.1–99.5/4) 74.6 ± 8.2 (67.8–81.4/8) 80.9 ± 11,3 (75.1–86.7/6) 66.7 ± 13.1 (58.4–75.0/12) 64.3 ± 9.0 (60.5–68.1/24) 66.5 ± 16.1 (60.7–72.3/32) 66.3 ± 6.5 (61.9–70.7/11)∗ 68.0 ± 9.7 (64.8–71.2/37)∗ 91.8 ± 16.0 (81.0–102.6/11)∗ 105.6 ± 18.9 (97.0–114.2/21)∗ 87.0 ± 7.9 (82.2–91.8/13)∗

Mandenaa

Note. Values are means ± standard deviation and (95% confidence interval/sample size). a Data supplemented by data from J.-B. Ramanamajato. b Data from Schmid (1997) and Schmidt and Kappeler (1998). c Data from Schmelting et al. (2000). ∗ Significantly (p < 0.05) heavier than Kirindy/CFPF; ∗∗ significantly (p < 0.05) heavier than Ampijoroa.

January February March April May June July August September October November December

Mandenaa

Table III. Body mass of Microcebus murinus from Mandena, Kirindy/CFPF and Ampijoroa

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Lahann, Schmid, and Ganzhorn 110 Mandena males Mandena females Kirindy/CFPF males Kirindy/CFPF females Ampijoroa males

100

body mass (g)

90

80

70

60

50

40 Jan

Feb

Mar

Apr

May Jun

Jul

Aug Sep

Oct

Nov Dec

month Fig. 2.

Comparison of body mass of Microcebus murinus captured in Mandena, Kirindy/CFPF and Ampijoroa (values are monthly means).

nonpregnant females in Kirindy/CFPF. Despite the differences resulting from different times of pregnancy, Microcebus murinus from Mandena were heavier than M. murinus in Kirindy/CFPF, which were heavier than M. murinus in Ampijoroa (Fig. 2).

Population Characteristics and Reproduction Between 2000 and 2003 we caught 171 Microcebus murinus (97 females, 74 males) 565 times in 16,000 traps (160 traps × 4 nights × 25 mo) in Mandena. Trapping success in the littoral rain forest of Mandena ranged from 1% to 13% (minimum in February and March and maximum in June and July). In the dry deciduous forests the trapping success was higher. In Ampijoroa mouse lemurs occupied 3% (January) to 30% (September) of traps and in Kirindy/CFPF, ca. 20% of traps (Ganzhorn and Schmid 1998; Reimann, 2002; Schmelting, 2000). In Mandena we recaptured 13% of the subjects (16% females and 9% males) after 12 mo. We recaptured only 2 females and 1 male after 24 mo


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Table IV. Occurrence of breeding activity in Microcebus murinus in Mandena Month September October November December January February March April May June July August

births

Observed and captured juveniles 30–40 g

Observed and captured subadults40–50 g

0 2 19 0 3 9 0 2 0 0 0 ?

0 0 0 10 2 5 7 1 4 4 1 ?

0 0 0 2 5 3 9 3 7 12 6 ?

Note. We predicted dates of birth from captured and observed pregnant females.

and none after 3 yr. In Kirindy/CFPF and Ampijoroa recapture rates were ca. 30–40% in subsequent years (Ehresmann, 2000; Ganzhorn and Schmid, 1998; Lutermann, 2001; Schmelting, 2000). In Mandena recapture rate of the mouse lemurs was 44% in ≤ 6 mo (50% for females and 30% for males), indicating that the individuals were not simply trap-shy. Thus, high turnover rates characterize the Mandena population of Microcebus murinus.

Number of Litters In the littoral rain forest of Mandena female Microcebus murinus give birth to 2 and probably 3 litters/yr. From October 2000 to February 2001, 2 of the radiotracked and marked females had 2 litters and raised them successfully. Most females captured in October were pregnant and lactating in November. The first parked infants appeared in December and we captured juveniles in December and January (Table IV). Thus, the first litter was born in November. In January and February capture rates were low. Captured females were pregnant in January and lactating in February. We again found parked infants in February and captured juveniles in March (Table IV). Thus, the second litter was born in January and February. In April (2002 and 2004) we captured 2 pregnant females. We captured some juveniles in May and June. Therefore it is likely a third litter was born in April and May (Table IV). In Kirindy/CFPF Microcebus murinus reproduce only once per year at the end of December and the beginning of January (Eberle and

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Kappeler, 2004) while in Ampijoroa the gray mouse lemurs have 2 litters/yr (Lutermann, 2001; Schmelting et al., 2000).

DISCUSSION We documented substantial geographic variation in life history traits of Microcebus murinus. We investigated whether the variability is due to abiotic conditions (temperature constraints), which might be reflected in Bergmann’s rule or more likely due to differences in resource productivity/seasonality. The results indicate that both components (abiotic and biotic) contribute to the ecogeographic variation in life history traits of Microcebus murinus.

Morphology and Body Mass The changes in body mass of Microcebus murinus are consistent with Bergmann’s rule. Body mass increased monotonically with decreasing mean temperatures from Ampijoroa (27◦ C) to Kirindy/CFPF (25◦ C) to Mandena (23◦ C). Other morphometric measurements yielded inconclusive results, possibly because of difficulties in comparing external measurements of live individuals taken by different people. We list the results for completeness but do not consider them further. It is unclear whether the increase in body mass toward lower temperatures is an adaptation to conserve energy in a cooler climate because of lower surface-to-volume ratios (adaptations to the cold: the original argument for Bergmann’s rule), or whether smaller animals have an evolutionary advantage over larger species at higher temperatures (adaptations to high temperature: Hadley, 1997; Smith et al., 1995). In any case the patterns in body mass variation are consistent with the idea that adaptations for temperature regulation are important for mouse lemurs and are reflected in their body mass. Researchers have also recorded shifts in size or body mass in relation to the number of sympatric species within the same guild. Competition might be reduced in communities with fewer species. Small species might exhibit ecological release if larger competitors are absent (i.e., they get bigger; Brown and Lomolino, 1998). In Ampijoroa and Kirindy/CFPF Microcebus murinus lives sympatrically with 1 congeneric species and 1 or 3 more cheirogaleids, respectively (Ampijoroa: Microcebus ravelobensis, Cheirogaleus medius; Kirindy/CFPF: Microcebus berthae, Cheirogaleus medius, Mirza coquereli, Phaner furcifer pallescens). Based on an analysis


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of distribution patterns and microhabitats, there is evidence of competition between the congeneric mouse lemurs and mixed evidence for competition between Microcebus murinus and Cheirogaleus medius in Kirindy/CFPF (Ganzhorn and Kappeler, 1996; Schwab and Ganzhorn, 2004). In Mandena, Microcebus murinus is sympatric with Cheirogaleus medius and C. major, both larger than M. murinus, and thus should face similar or even more intense competition from larger species than M. murinus at the other sites. Further, there is no smaller congeneric species in Mandena. Thus, if differences in body mass between populations reflect character displacement due to competition, Microcebus murinus in Mandena should be smaller at least than the individuals in Kirindy/CFPF. Because Microcebus murinus in Mandena is larger than M. murinus in Kirindy/CFPF, competition as a driving force for changes in body mass is unlikely. Variation in body mass is also inconsistent with the resource productivity/seasonality hypothesis. The most appropriate argument on impacts of seasonality on body mass is not clear. If in more seasonal environments food patches were small and sufficient to maintain small species with lower food requirements (in absolute terms) but insufficient to support larger species with higher food requirements, then seasonality would favor smaller species. Low food availability during the lean season and possibly low quality of food possibly favor larger species because they are metabolically better adapted to cope with reduced food availability than smaller species. Though Albrecht et al. (1990) and Lehman et al. (2005) favor the idea that small species can cope better with seasonal environments than larger species because they are more likely to find enough food during the lean season, Cowlishaw and Dunbar (2000) consider smaller species more sensitive to seasonality than larger species because of the capacity of larger species to sustain prolonged periods of food shortage. Albrecht et al. (1990) and Lehman et al. (2005) note that it is necessary to develop the arguments still further to include resource quantity, quality, and their distribution in space and time. Because of lack of quantitative data, one cannot resolve the issue. However, regardless of whether individuals become smaller or larger with increasing seasonality, we expect a gradual change of body mass with seasonality, which is not the case in Microcebus murinus. Therefore changes in body mass follow Bergmann’s rule and are more likely related to ambient temperature than to seasonality.

Reproduction and Lifespan Population-specific differences in reproduction match the resource productivity/seasonality argument. The number of litters/yr increases with

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decreasing seasonality. In the highly seasonal Kirindy/CFPF with 800 mm of annual rainfall, Microcebus murinus have 1 litter/yr. In Ampijoroa, with 1200 mm of rain, the number of litters increases to 2, and in the least seasonal evergreen littoral rain forests of Mandena with 1600 mm rainfall, Microcebus murinus has 2 and most likely 3 litters/yr. The best explanation for the differences is an extension of the time of food availability suitable for pregnancy and lactation as annual rainfall increases. Thus, the availability of food resources is likely to shape the trait. The increased number of litters/yr seems to be traded against life expectation in the evergreen littoral rain forests. According to interannual recapture rates, mouse lemurs from the littoral forest do not live as long as mouse lemurs from the dry deciduous forests. Under the assumption that populations are stable, the observed differences in population dynamics match the general trade-off between longevity and reproductive rates (Reznick et al., 2000) when comparing Mandena (low recapture rates between years and 2 or 3 litters/yr) with Kirindy/CFPF (higher recapture rates and 1 litter/yr). The population dynamic of Microcebus murinus at Ampijoroa requires further explanations. In Ampijoroa recapture rates match recapture rates at Kirindy/CFPF but individuals have 2 litters/yr, which should result in different population growth at the different sites. Detailed analyses of the phenomenon have to wait until data on lifetime reproductive success are available for all sites. Cause and effect of the differences in reproductive strategies are not clear either. Do individuals die earlier because they reproduce more often per year or do they reproduce more often because they die earlier in the littoral forest? Parasitological studies show that Microcebus murinus have much higher loads of gut parasites in the littoral rain forest of Mandena than in dry deciduous forest of Kirindy/CFPF (Schad et al., 2004, 2005; B. Raharivololona and N. Schwensow, pers. comm.). But it is unknown whether the increased parasite load results in increased mortality. In conclusion, ecogeographic variation in life history traits of populations of Microcebus murinus are linked to thermoregulation and resource productivity/seasonality. Thermal constraints result in a clinal latitudinal gradient of body mass, with smaller individuals occurring at the sites with higher ambient temperature. Resource availability seems to be reflected in differences in their reproductive rates and longevity. Gray mouse lemurs reproduce more often but do not live as long in the evergreen littoral rain forest as in the dry deciduous forest. Thus, Microcebus murinus shows substantial behavioral variation and specific adaptations to local conditions, which offers considerable potential to study links between environmental conditions and the evolution of life history traits in lemurs.


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ACKNOWLEDGMENTS We conducted the study under the accord de Collaboration between ´ the Laboratoire de Paleonthologie et Anthropologie et Biologie Animale of the Universite´ d’sAntananarivo and the Department Ecology and Conservation, University of Hamburg. We thank the Commision Tripartite ` pour la Production Animale et des Eaux et Forets ˆ for and the Ministere permission to work in Madagascar. We thank QIT Madagascar Minerals and their environmental team, headed by Manon Vincelette and JeanBaptiste Ramanamanjato, for help and support. Refaly Ernest helped greatly with trapping of subjects in Mandena. We thank the reviewers who helped to improve the manuscript substantially. The DAAD (German Academic Exchange Service) and by the Deutsche Forschungsgemeinschaft (Ga 342/8-1, Schm1391/2-4) supported the study in part.

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