Selected publications:
SCHMID, J. & GANZHORN, J.U. (1996): Resting metabolic rates
of Lepilemur ruficaudatus.. American Journal of Primatologie 38:169-174.
SCHMID, J. (1998): Tree Holes used for Resting by the Grey Mouse
Lemur (Microcebus murinus) in Madagascar: Insulation Capacities
and Energetic Consequences. International Journal of Primatology
19:797-810.
SCHMID, J. & KAPPELER, P.M. (1998): Fluctuating sexual dimorphism
and differential hibernation by sex in a primate, the gray mouse
lemur (Microcebus murinus). Behavioral Ecology and Sociobiology
43:125-132.
SCHMID, J. (1999): Sex-specific differences in activity patterns
and fattening in the gray mouse lemur (Microcebus murinus) in
Madagascar. Journal of Mammalogy 80(3):749-757.
SCHMID, J. (2000): Conservation Planning in the Mantady-Zahamena
Corridor, Madagascar: Rapid Assessment Program (RAP). In Isolated
Vertebrate Communities in the Tropics. (Edited by Rheinwald G.),
pp. 285-296. Bonn. Zool. Monogr. 46.
SCHMID, J. (2000): Daily torpor in the gray mouse lemur (Microcebus
murinus) in Madagascar: Energetic consequences and biological
significance. Oecologia 123:175-183.
SCHMID, J., RUFUS, T. & HELDMAIER, G. (2000): Metabolism and
temperature regulation during daily torpor in the smallest primate,
the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. Journal
of Comparative Physiology B 170: 59-68.
SCHMID, J. & Speakman, J. R. (2000): Daily energy expenditure
of the grey mouse lemur (Microcebus murinus): a small primate
that uses torpor. Journal of Comparative Physiology B 170:633-641.
Abstracts:
SCHMID, J. & GANZHORN, J.U. (1996): Resting metabolic rates
of Lepilemur ruficaudatus.
Abstract: Seventeen sportive lemurs (Lepilemur ruficaudatus) were
captured in a dry, deciduous forest in western Madagascar, and
the resting metabolic rates were measured. According to the data,
Lepilemur ruficaudatus has the lowest resting metabolic rate of
any primate and any mammalian folivore recorded so far.
SCHMID, J. (1998): Tree Holes used for Resting by the Grey
Mouse Lemur (Microcebus murinus) in Madagascar: Insulation Capacities
and Energetic Consequences.
Abstract: The insulation capacity of tree holes used by grey mouse
lemurs (Microcebus murinus) was studied in a primary dry deciduous
forest in western Madagascar, during the cool dry season. Tree
holes had an insulating effect and fluctuations of air temperatures
were less extreme inside the holes than outside. The insulation
capacity of the tree holes peaked between 0800 - 1100 h, when
ambient temperatures ranged between 25 - 30°C. To compare
between different tree holes, the mean difference between the
internal temperature (Ti) and the external temperature (Te) was
calculated for each tree hole. Thus, large differences indicate
good insulation capacities. The mean difference of tree holes
in living trees was significantly larger than of tree holes in
dead trees, which shows that insulation in living trees is more
effective. During the dry season, insulation capacity of tree
holes in living trees decreased and were lowest in July, whereas
the insulation capacity of holes in dead trees remained approximately
constant. Physiological studies under natural temperature and
light conditions in M. murinus revealed that daily torpor saves
around 40% of the daily energy expenditure compared to normothermia.
However, torpor can only be maintained up to the threshold body
and ambient temperature of 28°C at which M. murinus have to
terminate torpor actively. By occupying insulating tree holes,
mouse lemurs may stay longer in torpor. This increase their daily
energy savings by an extra 5%.
SCHMID, J. & KAPPELER, P.M. (1998): Fluctuating sexual
dimorphism and differential hibernation by sex in a primate, the
gray mouse lemur (Microcebus murinus).
Abstract: The aim of this study was to investigate reproductive
strategies and their consequences in gray mouse lemurs (Microcebus
murinus), small solitary nocturnal primates endemic to Madagascar.
Previous reports of sexual dimorphism in favor of males and females,
respectively, a high potential for sperm competition and pheromonal
suppression of mating activity among captive males, led us to
investigate mechanisms of intrasexual competition in a wild population.
Based on 3 years of mark-recapture data, we demonstrate that sexual
dimorphism in this species fluctuated annually as a result of
independent changes in male and female body mass. Male body mass
increased significantly prior to the short annual mating season.
Because their testes increased by 100% in the same period and
because their canines are not larger than those of females, we
suggest that large male size may be advantageous in searching
for estrous females and in enabling them to sustain periods of
short-term torpor. In contrast, to reports from captive colonies,
we found no evidence for two morphologically distinct classes
of males. Finally, we also show that most adult males are active
throughout the cool dry season that precedes the mating months.
This is in contrast to other solitary hibernating mammals, where
males typically emerge 1-2 weeks before females. Thus, this first
extended field study of M. murinus clarified previous conflicting
reports on sexual dimorphism and male reproductive strategies
in this primitve primate by showing that their apparent deviation
from predictions of sexual selection theory is brought about by
specific environmental conditions which result in sex-specific
life history tactics not previously described for mammals. A general
conclusion is that sexual selection can operate more strongly
on males without resulting in sexual dimorphism because of independent
selection on the same traits in females.
SCHMID, J. (1999): Sex-specific differences in activity patterns
and fattening in the gray mouse lemur (Microcebus murinus) in
Madagascar.
Abstract: The gray mouse lemur (Microcebus murinus) is a small,
nocturnal primate endemic to Madagascar and has evolved specific
activity patterns to survive the dry season, a period of low food
availability and low ambient temperatures. These patterns are
sex-specific. I determined seasonal fluctuations of body mass
and tail circumference in M. murinus under natural conditions
in a dry deciduous forest of western Madagascar in 1994--1995.
I compared those variables were among individuals during different
activity patterns. Based on mark-recapture and monitoring of sleeping
sites, 73.1% of adult females but only 18.9% of adult males remained
inactive for the several weeks to 4--5 months throughout the cool
dry season. Inactive females stored fat before the onset of the
inactive phase and lost 31.7% of their mass during the dry winter,
but inactive males hardly stored fat, and their body mass did
not change between onset and end of the period of inactivity.
Duration of inactivity was significantly longer for females than
males, due to earlier emergence of males. At the end of inactivity
and activity periods, respectively, body masses and tail circumferences
did not differ between inactive and active males and females.
Thus, M. murinus has evolved two different strategies to survive
the cool dry season: being generally active but combined with
daily torpor of <24 h, and remaining inactive for days to several
weeks, which might be associated with prolonged bouts of torpor.
SCHMID, J. (2000): Conservation Planning in the Mantady-Zahamena
Corridor, Madagascar: Rapid Assessment Program (RAP).
Abstract: Conservation International (CI) conducted a Rapid Assessment
Program (RAP) of the biodiversity of the humid forest within the
Mantady-Zahamena corridor in Madagascar. The RAP methodology is
designed to quickly provide information needed to catalyze conservation
activity and improve regional and national biodiversity protection.
The Mantady-Zahamena corridor links the protected areas of the
Parc National (PN) de Mantady and the Réserve Naturelle
Intégrale (RNI) de Zahamena. This region is of particular
interest and importance since not only does it comprise of primary
and secondary lowland rainforest as well as moist montane forest,
but it also connects two protected areas in the north and south.
Survey work was divided into two expeditions (expedition 1: November
7 - December 14, 1998; expedition 2: January 15 - 28, 1999). Four
camps were placed in different classified forests, and one site
was placed in PN de Mantady. At each site, presence and relative
abundance of lemur species were estimated using the line transect
method. A total of eleven lemur species (four diurnal, two cathemeral,
and five nocturnal species) were found in the corridor, including
the Aye-Aye, Daubentonia madagascariensis. Forest clearance and
settlement in the entire corridor are the major threats and might
explain relatively low densities and absence of certain lemur
species like Propithecus diadema diadema (Site 1) and Varecia
variegata variegata (Site 1 and 5). Exceptional biodiversity cannot
be maintained in areas where genetic exchange is impossible due
to geographic isolation and disconnection of forest blocks. The
most urgent and actually basic need is to stop forest fragmentation
and habitat destruction, with exceptionally high conservation
priorities on remaining lowland forests.
SCHMID, J. (2000): Daily torpor in the gray mouse lemur (Microcebus
murinus) in Madagascar: Energetic consequences and biological
significance.
Abstract: Patterns and energetic consequences of spontaneous daily
torpor were measured in the gray mouse lemur (Microcebus murinus)
under natural conditions of ambient temperature and photoperiod
in a dry deciduous forest in western Madagascar. Over a period
of two consecutive dry seasons, oxygen consumption (VO2) and body
temperature (Tb) were measured on ten individuals kept in outdoor
enclosures. In all animals, spontaneous daily torpor occurred
on a daily basis with torpor bouts lasting from 3.6 to 17.6 hours,
with a mean torpor bout duration of 9.3 hours. On average, body
temperatures in torpor were 17.3 ± 4.9 °C with a recorded
minimum value of 7.8 °C. Torpor was not restricted to the
mouse lemurs´ diurnal resting phase, and entries occurred
throughout the night and arousals mainly around midday, which
coincides with the daily ambient temperature maximum. Arousal
from torpor was a two-phase process with a first passive, exogenous
heating where the Tb of animals increased from the torpor Tb minimum
to a mean value of 27.1 °C before the second, endogenous heat
production commenced to further raise the Tb to normothermic values.
Metabolic rate during torpor (28.6 ± 13.2 ml O2 * h-1)
was significantly reduced by ca. 76 % compared to resting metabolic
rate (132.6 ± 50.5 ml O2 * h-1). On average for all M.
murinus individuals measured, hypometabolism during daily torpor
reduced daily energy expenditure by ca. 38 %. In conclusion, all
these energy conserving mechanisms with passive exogenous heating
during arousal from torpor, low minimum torpor Tbs, extended torpor
bouts into the activity phase of the nocturnal mouse lemurs, comprise
an important and highly adapted mechanism to minimize energetic
costs as a response to the unfavorable environmental conditions
and may play a crucial role for individual fitness.
SCHMID, J., RUFUS, T. & HELDMAIER, G. (2000): Metabolism
and temperature regulation during daily torpor in the smallest
primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar.
Abstract: Thermoregulation, energetics and patterns of torpor
in the pygmy mouse lemur, Microcebus myoxinus, were investigated
under natural conditions of photoperiod and temperature in the
Kirindy/CFPF Forest in western Madagascar. M. myoxinus entered
torpor spontaneously during the cool dry season when food availability
was low. Torpor only occurred on a daily basis and torpor bout
duration was on average 9.6 h, and ranged from 4.6 h to 19.2 h.
Metabolic rates (MRs) during torpor were reduced to about 86%
of the normothermic value. Minimum body temperature (Tb) during
daily torpor was 6.8 °C at an ambient temperature (Ta) of
6.3°C. Entry into torpor occurred randomly between 20:00 and
06:20 hours, whereas arousals from torpor were clustered around
13:00 hours within a narrow time window of less than 4 h. Arousal
from torpor was a two-step process with a first passive climb
of Tb to a mean of 27°C, carried by the daily increase of
Ta when oxygen consumption (VO2) remained more-or-less constant,
followed by a second active increase of VO2 to further raise the
Tb to normothermic values. In conclusion, daily Tb rhythms in
M. myoxinus further reduce the energetic costs of daily torpor
seen in other species: 1) they extend to unusually low Tbs and
consequently low MRs in torpor, and 2) they employ passive warming
to reduce the energetic costs of arousal. Thus, these energy conserving
adaptations may represent an important energetic aid to the pygmy
mouse lemur and help to promote their individual fitness.
SCHMID, J. & Speakman, J. R. (2000): Daily energy expenditure
of the grey mouse lemur (Microcebus murinus): a small primate
that uses torpor.
Abstract: We aimed to investigate the pattern of utilisation of
torpor and its impact on energy budgets in free-living grey mouse
lemurs (Microcebus murinus), a small nocturnal primate endemic
to Madagascar. We measured daily energy expenditure (DEE) and
water turnover using doubly labelled water, and we used temperature
sensitive radio collars to measure skin temperature (Tsk) and
home range. Our results showed that male and female mouse lemurs
in the wild enter torpor spontaneously over a wide range of ambient
temperatures (Ta) during the dry season, but not during the rainy
season. Mouse lemurs remained torpid between 1.7 - 8.9 h with
a daily mean of 3.4 h, and their Tsks fell to a minimum of 18.8
°C. Mean home ranges of mouse lemurs which remained normothermic
were similar in the rainy and dry season. During the dry season,
mean home range of mouse lemurs showing daily torpor was significantly
smaller than that of animals remaining normothermic. The DEE of
M. murinus remaining normothermic in the rainy season (122 ±
65.4 kJ d-1) was about the same of that of normothermic mouse
lemurs in the dry season (115.5 ± 27.3 kJ d-1). During
the dry season, the mean DEE of M. murinus that utilised daily
torpor was 103.4 kJ ± 32.7 kJ d-1 which is not significantly
different from the mean DEE of animals remaining normothermic.
We found that DEE of mouse lemurs using daily torpor was significantly
correlated with the mean temperature difference between Tsk and
Ta (r2 = 0.37) and with torpor bout length (r2 = 0.46), while
none of these factors explained significant amounts of variation
in the DEE of the mouse lemurs remaining normothermic. The mean
water flux rate of mouse lemurs using daily torpor (13.0 ±
4.1 ml d-1) was significantly lower than that of mouse lemurs
remaining normothermic (19.4 ± 3.8 ml d-1), suggesting
the lemurs conserve water by entering torpor. Thus, this first
study on the energy budget of free-ranging M. murnius demonstrates
that torpor may not only reflect its impact on the daily energy
demands, but involve wider adaptive implications such as water
requirements.
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