ANNUAL REPRODUCTIVE CYCLES IN SELECTED AFRICAN MAMMALS IN RESPONSE TO ENVIRONMENTAL CUES J.D. SKINNER, RJ. VAN AARDE & RJ. VAN JAARSVELD, Mammal Research Institute,
University of Pretoria, Pretoria, 0002 - South Africa.
Introduction
The assumption that natural selection is an Optlmlslllg process, means that
reproductive seasonality in mammals evolved to maximise gene survival. Although the
constraints usually imposed on optimality theory are applicable, it can be assumed that
periodicity in reproduction represents an adaptation to fluctuation in the availability of
potentially limiting resources. In areas where these fluctuations in primary production are
the result of a predictable seasonal climatic cycle, such as seasonal rainfall, a seasonal
reproductive cycle becomes a viable strategem. Seasonal reproduction involves the temporal
placing of mating, gestation, parturition, lactation and weaning in such a way to make
maximum use of fluctuating resources (Skinner et at., 1984).
In order to ensure that the young are born during favourable environmental
conditions, the initiation of reproductive activity has to commence some time before the
favourable season, or during it, depending on the duration of gestation. Larger mammals
will tend to initiate reproductive activity earlier than small mammals, as gestation length
usually increases with size (Rowlands & Weir, 1984). A number of environmental cues
operate as proximate causes to initiate reproductive activity.
A large variety of African mammal species are seasonal breeders (Fairall, 1968 ;
Smithers, 1983). The thrust of this paper is not to review the occurrence of seasonal
breeding, but rather to examine some factors that influence their seasonal reproductive
cycles by referring to five interesting examples. The reproductive cycles of three ofthese is
controlled by the photoperiod.
Impala and Blesbok
impala (Aepyceros melampus) and blesbok (Damaliscus dorcas) occupy habitats in
southern Africa which are characterised by a predictable climatic cycle of dry winters and
wet summers. In order to capitalise on this fixed climatic cycle, they respond to the
shortening daylength to initiate breeding, conforming to the model proposed for the Suffolk
ewe by Karsch et at. (1984). The central mechanism in this model is the "LH pulse
generator", which processes both external and internal environmental signals. After
attaining puberty at 16 months, ewes experience a maximum of two oestrous cycles
annually, most conceiving during the first cycle.
Another environmental factor that has a profound effect on the expression of
seasonality in impala and blesbock, is social status. The ability of males of these two species
to respond to photoperiodic cues is complicated by the individual animal's social status. In
anaesthetised males, an LH-RH challenge resulted in higher testosterone responses in
territorial than bachelor males (Fig. 1).
31
J.D. Skinner, RJ. van Aarde, RJ. van Jaarsveld
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Figure 1.- Peripheral plasma testosterone concentrations in (a) territorial (e) and bachelor (0) b1esbok
and (c) territorial (e) and bachelor (0) impala at capture (-1 h) and 0,1 and 2 h after injection of 50 Ilg LH-RH
(oh). Equivalent LH concentrations for b1esbok are shown in (b). From Illius et at. (1983).
The lower LH-response to LH-RH in bachelor than territorial blesbok males suggests
that social stimuli affect the responses of pituitaries through the action of prolactin (Keverne,
1979 ; McNeilly, 1980). A social effect on the LH-pulse generator through the pineal gland
and melatonin cannot be excluded at this stage (Rieter, 1980).
Rock Hyrax
The herbivorous seasonal breeding rock hyrax (Procavia capensis) lives in rocky
areas throughout Africa. The rock hyrax has a variable mating season which corresponds
with latitude. In general, the mating season is later and longer in duration and parturition
takes place later in the lower latitudes (Millar, 1971).
Due to its wide distribution, the rock hyrax inhabits a wide range of habits in
southern Africa and is therefore subject to considerable variation in food availabiliti.
Nutrition appears to affect the onset of puberty and litter sizes decrease in years, and areas,
of diminished rainfall (Millar, 1971). In an experiment to determine the effect of different
planes of nutrition on spermatogenesis and androgenesis in males during the mating season
(Millar & Fairall, 1976), it was found that lower planes of nutrition caused decreased
reproductive activity (Table 1). Testicular weight, seminiferous tubule diameter and plasma
testosterone concentration were all significantly lower in hyrax fed the low-plane diet, while
plasma and pituitary U/ were lower, but not significantly so. Hypothalamic LH-RH did not
differ between the low and high-plane diets.
32
Annual reproductive cycles in selected african mammals in response to environmental cue"
TABLE 1
Comparison of testicular activity and hormone concentrations in sexually active hyrax
on a high or low plane of nutrition and wild sexually quiescent hyrax (no in parentheses) ­
From Millar & Fairall (1976).
-_._-­
~---
I
II
---_._---­
-
---­
~--.
-----------,­
-­
-
--­
-
------------­
Sexually active hyrax
'Sexually quiescent
High plane (3)
Low plane (3)
hyrax (5)
!
--1-------- ------,-----------­
Weight of testes (g)
Seminiferous tubules
diameter ()lID)
Plasma testosterone
(ng/ml)
Plasma LH (ng/ml)
Pituitary LH
(~gIand)
Hypothalamic LH-RI-I
(ng/gland)
Plasma cortisol
(ng/100ml)
I
86,2 ± 8,2ab
48,2 ± S,2ae
5,6 ± 1,8 be
II
192,3 ± Oyb
143,2 ± 7,6 ac
67,0± 3,9 bc
1,18 ± 0,06 D
2,5 ± 0,6:1
1,0 ± 0,3
13,6 ± 3,2ab
5,5 ± 2,8
2,9 ± 2,0
210,7 ± 40,5b
147,3 ± l1,7c
63,5 ± 21,9be
16,5 ± 4,3 b
21,5 ± 7,3 c
101,6 ± 13,goc
6,6 ± 0,7
5,6 ± 1,2
------
'---------~
I
3,4± 1,1
___
_
~__
______ _
~
___ .J
Values are means ± S.EM. ; means bearing identical superscripts differ significantly
(p 0,05) by Students t-test.
*Expressed in temls of NIAMDD-ovine-LH-S18.
The interpretation of these results is difficult, mainly due to the low samples sizes.
However, the inverse relationship between hypothalamic LH-RH content and plasma LH
concentration in this species (Table 1) suggests that the nutritional effects on reproduction
are primarily due to alterations in the secretion of LH-RH (Millar & Fairall, 1976) by the
LH-pulse generator.
Porcupines
Our fourth example refers to Africa's largest rodent, the Cape porcupine (llystrix
africaeaustralis). They are catholic in their habitat requirements, and are found throughout
southern Africa. Porcupines are predominantly nocturnal and avoid environmental extremes
by sheltering in subterranean burrows, rock crevices and caves (SlUnner ct al. 1984).
Porcupines in tl1e semi-arid Karoo of southern Africa are strictly seasonal breeders.
Litters are produced during the hot wet months between August and March when most
(81.7%) of the annual rainfall (440mm) is recorded (Skinner et ai., 1984). The mean date of
conception for this population is 21 september (± 18,6 days). Captive porcupines exposed
to natural illumination and a con<;tant food supply, breed throughout the year \'·(ith females
conceiving only once per annum. Funllermore females are polycestrous but do not cycle
while lactating and only conceive during the third to seventh 30-day cycle following the end
33
J.D. Skinner, RJ. van Aarde, RJ. van laarsveld
of lactation. In C011':;idering the time interval of events from one conception to the next in the
average female following Skinner et al. (1984) it is clear why females conceive only once a
year (Fig. 2).
PREGNANT
E
110
c:
01
90
z·
III
70
III
50
LACTATING
PREGNANT
CYCLING
~
ocr:
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30
10
0
N
D
J
F
M
A
M
J
J
A
S
0
N
D
MONTH
PREGNANT
LACTATING
CYCLING
­
93
­
120
-150
363
-
DAYS
DAYS
Figure 2.- Annual reproductive cycle of adult female porcupines. Adapted from Skinner et al. (1984).
The fact that this reproductive cycle lasts approximately one year in captivity, despite
the food abundance, means that the infertile cycles must have some function in the general
annual reproductive cycle. It has been postulated that these cycles, which show lower
progesterone levels than fertile cycles, are important for the priming of the uterus (Van
Aarde 1984). 1ms period could also play an important role in providing an opportunity for
the replenishment of resources following the extended gestation period characteristic of the
hystricomorpha (Rowlands & Weir, 1974).
The occurrence of a seasonal pattern of reproduction in the species as a whole
nevertheless indicates some kind of environmental selection pressure, with pregnancy
normally occurring after the increase in primary production in spring, and lactation exten­
ding into the late summer when resources are plentiful (Fig. 2).
Springhaas
The springhaas (Pedetes capensis) is a large bipedal rodent of uncertain taxonomic
position (McLaughlin 1967) occurring throughout southern Africa. Although capable of
breeding throughout the year, in the highland grassland plateau the relationship between
pregnant females and mean monthly temperature was highly significant (r = 0,84 ;
P <0,001 ; n = 10), the highest incidence of pregnancy occurring in the colder months. An
accurate gestation length has not yet been recorded but indications are that it is about 80
days.
34
Annual reproductive cycles in selected african manvnals in response to enviromnental cues
A peak in mating activity occurs in mid-winter but this is not reflected in any apparent
seasonal cycle in testicular endocrine or exocrine function in males (Table 2), the full
spermatogenic cycle being evident in all males.
TABLE 2
Mean ± s.d. plasma concentrations of LH and testosterone
(adapted from van der Merwe et af. 1980).
In
male springhaas
Months
N
LH
(ng/ml)
Testosterone
(ng/ml)
Jan.-Feb.
June-Aug.
Sept.-Nov.
6
13
18
0,73 ±0,87
1,97 ± 1,34
1,49 ± 0,88
0,94± 0,58
1,90 ±0,86
1,74± 0,87
I
Although Coe (1969) considered P. capensis a seasonal breeder, the short gestation
period would tend to preclude this unless nutritional cues are also important. Nutrition was
adequate for the animals in our study area but temperature appeared to have an influence
with significantly fewer births in the cold winter months. This may conversely be affected
by the lower LH and testosterone levels in the hottest summer months when ovarian
follicular activity from non-pregnant females also seemed to be supported although too few
specimens were available to enable conclusive deductions.
Conclusions
,The examples discussed indicate that where photoperiod is the proximate cue
.1utiating reproduction the pattern may also be confounded in males by factors such as social
status. It is much more difficult however, to identify cues other than photoperiod
particularly when one of these may confound the effects of another and where their
cummulative effects may provide the optimum situation. Despite the widespread occurrence
of seasonal breeding in African mammals, our knowledge concerning the factors that
influence or affect seasonality is scant. The development of techniques for the assesment of
endocrinological parameters in anaesthetised animals must be regarded as a high prority, if
we hope to unravel the multitude of factors that influence and initiate seasonal breeding in
African mammals.
35
JD. Skinner. RJ. van Aarde, R J. van J aarsveld
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