How Rainfall Variation Influences Reproductive Patterns of African Savanna Ungulates in an Equatorial Region Where Photoperiod Variation Is Absent
How Rainfall Variation Influences Reproductive Patterns of African Savanna Ungulates in an Equatorial Region Where Photoperiod Variation Is Absent
Joseph O. Ogutu 0 1
Norman Owen-Smith 0 1
Hans-Peter Piepho 0 1
Holly T. Dublin 0 1
0 1 International Livestock Research Institute , P. O. Box 30709, Nairobi, 00100, Kenya , 2 University of Hohenheim, Institute for Crop Science , 70599 Stuttgart, Germany, 3 Centre for African Ecology , School of Animal, Plant and Environmental Sciences, University of the Witwatersrand , Wits, 2050, South Africa, 4 IUCN ESARO , Wasaa Conservation Centre , P.O. Box 68200, Nairobi, Kenya, 00200
1 Editor: Mathew S. Crowther, University of Sydney , AUSTRALIA
In high temperate latitudes, ungulates generally give birth within a narrow time window when conditions are optimal for offspring survival in spring or early summer, and use changing photoperiod to time conceptions so as to anticipate these conditions. However, in low tropical latitudes day length variation is minimal, and rainfall variation makes the seasonal cycle less predictable. Nevertheless, several ungulate species retain narrow birth peaks under such conditions, while others show births spread quite widely through the year. We investigated how within-year and between-year variation in rainfall influenced the reproductive timing of four ungulate species showing these contrasting patterns in the Masai Mara region of Kenya. All four species exhibited birth peaks during the putative optimal period in the early wet season. For hartebeest and impala, the birth peak was diffuse and offspring were born throughout the year. In contrast, topi and warthog showed a narrow seasonal concentration of births, with conceptions suppressed once monthly rainfall fell below a threshold level. High rainfall in the previous season and high early rains in the current year enhanced survival into the juvenile stage for all the species except impala. Our findings reveal how rainfall variation affecting grass growth and hence herbivore nutrition can govern the reproductive phenology of ungulates in tropical latitudes where day length variation is minimal. The underlying mechanism seems to be the suppression of conceptions once nutritional gains become insufficient. Through responding proximally to within-year variation in rainfall, tropical savanna ungulates are less likely to be affected adversely by the consequences of global warming for vegetation phenology than northern ungulates showing more rigid photoperiodic control over reproductive timing.
Funding: The monitoring was funded by the World
Wide Fund for Nature-East Africa Program
(WWFEARPO) and Friends of Conservation (FOC). The
program also received financial, material or logistical
support from WWF-US, WWF-Sweden, the Darwin
Initiative (DICE), the University of British Columbia,
United States Fish and Wildlife Service, Kenya
Wildlife Service, Cottar’s Camp, Kichwa Tembo,
Keekorok Lodge/Balloon Safaris and Kerr and
Downey Safaris. Data analysis and writing were
partially supported by the National Science
Foundation (NSF) through Grant Nos: BCS 0709671
and DEB-0342820 and a grant from the Belgian
government (DGIC BEL011) to the International
Livestock Research Institute. JO was supported by
the International Livestock Research Institute (ILRI),
the University of Hohenheim, Biostatistics Unit and a
grant from the German Research Found (DFG,
Research Grant # OG 83/1-1). The funders had no
role in study design, data collection and analysis,
decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared
that no competing interests exist.
Large mammalian herbivores depend on a food resource that varies seasonally in amount and
quality because of corresponding seasonal patterns of growth and dormancy shown by plants
. Accordingly, their births are typically concentrated early in the growing season when food
quality is highest , thereby supporting the peak nutritional demands of mothers through late
pregnancy and early lactation . For medium- to—large ungulates, the corresponding
conception peak falls during late summer or early autumn. In north temperate latitudes, the
scheduling of oestrous cycling and hence conceptions is tightly governed by daily variation in the
photoperiod, and births are narrowly concentrated within a 2–3 week window .
Observations on animals held in zoos show that many tropical and subtropical ungulates also respond
to changing day length in their reproductive phenology [4,5]. However, near the equator
changing photoperiod is no longer a tenable cue for the timing of mating and hence
conceptions. In these circumstances, many ungulate species reproduce year-round [6,7,8].
Nevertheless, certain ungulate species retain a seasonal birth pulse even in the absence of much day
length variation, suggesting that other factors govern their reproductive phenology. Predation
on newborn offspring could contribute to narrowing the birth peak [9,10], but does not explain
the timing of births within the seasonal cycle.
For African elephants (Loxodonta africana), births tend to be concentrated early in the wet
season, and result from conceptions occurring also during the wet season, following a gestation
period of 22 months [11,12]. However, for rhinos (Ceratotherium simum and Diceros bicornis)
and giraffe (Giraffa camelopardalis), conceptions peaking during the wet season generate a
birth pulse early in the dry season, because for these species the gestation period spans
1516-months [13,14]. This suggests proximate control by conditions affecting oestrus and mating
rather than by the food quality around the time of births. In equatorial regions the ultimate
benefits from nutritional conditions during the time of peak demands cannot be anticipated
from the cue provided by changing day length. This raises the possibility that the reproductive
phenology of medium-sized ungulates could likewise become governed proximately by
seasonal variation in rainfall affecting the timing of conceptions where photoperiod cues are
The reproductive performance of ungulates in high northern latitudes appears to be
threatened by the effects of global warming on the timing of plant growth, disrupting the synchrony
between births and optimal nutritional conditions for late pregnancy and lactation . The
amplified variation in rainfall anticipated as a consequence of global warming  could also
be adverse for herbivores occupying tropical savanna ecosystems by disrupting seasonal
nutritional regimes. While low rainfall restricts plant growth and hence reduces the nutritional
value of plant parts, too much rainfall could also be detrimental by promoting the growth of
taller grass higher in fibre contents. Accordingly, our aim in this paper is to assess how annual
and seasonal variation in rainfall affects the reproductive schedules and performance of
ungulates inhabiting an equatorial region. Our analysis compares two ungulate species that retain
seasonally restricted births even in equatorial East Africa with two that produce offspring
yearround despite showing narrow birth peaks at higher southern latitudes. Rainfall variation
could potentially influence reproductive schedules and performance by (1) affecting recovery
in body condition from the previous pregnancy towards the threshold enabling oestrous
cycling; (2) influencing foetal growth and viability; (3) controlling the post-birth growth and
survival of offspring. Accordingly, our specific hypotheses were:- H1: The fertility of female
ungulates reproducing year-round should be less responsive to rainfall than species showing
narrow birth pulses. H2: Monthly fertility should depend on rainfall over some period
immediately prior to the time of conception if nutrition directly influences oestrous cycling and
establishment of the foetus. H3: Annual fecundity should depend on rainfall received through
some extended period prior to conceptions if body condition influences the proportion of
females that are able to conceive and support the foetus. H4: Survival from birth into the
juvenile stage should depend on preceding dry season rainfall affecting foetal growth and hence
birth mass, and on early wet season rainfall affecting post-natal growth.
Our study area was the Masai Mara National Reserve, covering 1530 km² in south-western
Kenya (1°130-1°450S, 34°450-35°250E). Rainfall can be partitioned between the early “short”
rains (Nov-Jan), and the later “long” rains (Mar-Jun), typically separated by a mild lull in
February . Rainfall was recorded over a network of 14 monthly storage and two daily gauges.
The annual rainfall total over 1965–2003 averaged 1010 ± 187 mm, including 785 ± 152 mm
during the eight wet season months and 214 ± 76 mm during the four dry season months.
Monthly temperatures varied little between a mean daily maximum of 24.8°C in February and
a mean daily minimum of 9.8°C in September. Grazing pressure keeps the grass standing crop
relatively low through October-February, with peak biomass reached in June . Leaf
concentrations of nitrogen start rising during September to a peak in December, and thereafter decline
as grass height increases and above-ground parts senesce through the long rains into the dry
Permission to conduct the monitoring was granted by the Office of the President of the
Republic of Kenya, the Narok County Government (formerly Narok County Council), the Kenya
Wildlife Service (KWS), Wardens of the Masai Mara National Reserve and the management of
the former Koyiaki Group Ranch.
Population surveys and demography. Monthly vehicle counts of resident ungulate
species were organised by the Masai Mara Ecological Monitoring Program from July 1989 to
December 2003. We used only the data for the years with complete breeding cycles spanning
1989 to 2002. The study area was subdivided into three census blocks using major rivers and
roads, each with a fixed transect [20,21]. During the 174-month monitoring period, counts
were missing for 17 months distributed over nine years, for a further five months on one
transect, and for one month on another transect. In this paper, we compare the reproductive
patterns of topi (Damaliscus lunatus korrigum) and warthog (Phacochoerus africanus), which
showed seasonally restricted births, with hartebeest (Alcelaphus busephalus) and impala
(Aepycerus melampus), which give birth year-round in East Africa (Fig A in S1 File), despite
reproducing seasonally in southern Africa. Topi and hartebeest have gestation periods of around 8
months, while the gestation period of impala is 6.5 months, and that of warthog 5.5 months
A combination of body size, coat colour, horn length and shape was used to assign
immature animals to five size classes; newborn, quarter, half, yearling and three quarter grown. The
newborn class represents animals judged to be under one month old. For analysis quarter and
half-grown animals were grouped as juveniles for impala and warthog. Animals were sexed
using the presence, size and shape of horns and other secondary sexual characters when
present, except for warthog which lack sufficient sexual dimorphism. Animals were highly visible
in the open grasslands, reducing misclassification into these age-sex classes. To reduce the
omission of potentially fecund young females, three-quarter-sized hartebeest and topi and
yearling plus three-quarter-sized impala and warthog were included in the adult class. The
monthly fecundity for each species was estimated by dividing the total number of newborns
recorded in each month by the corresponding number of adult females. In the case of warthog
we divided the total number of newborns by half the number of all adults to approximate the
proportion of the adults constituted by females.
However, when calculating the effective fertility dependent on prior rainfall we needed to
allow for females that were already pregnant, and thus not able to conceive. The pregnant
proportion was calculated by summing monthly fecundities back over the gestation period. The
effective monthly fertility in each month was calculated as the number of newborns divided by
the number of females excluding the pregnant proportion. Total annual fecundity was obtained
by summing monthly fecundities over the annual cycle (July-June). This sum should not
exceed 1 but may do so due to errors in age estimation within the newborn category. Age
estimation for the newborn category is much more difficult for hartebeest than for topi because
the young of hartebeest are not born in a narrow pulse like those of topi. The estimated age for
the newborn class is thus likely to be biased and the magnitude of this bias is expected to be
larger for hartebeest than for topi. To reduce such biases, we multiplied the summed
proportion of newborns by 0.8 for topi and 0.67 for hartebeest, allowing for the differences expected
in the relative biases for the two species. This adjustment ensured that the summed proportions
for newborn topi and hartebeest did not exceed 1 because both species only give birth to a
single young per year. No correction was needed for impala, and some estimates of annual
fecundity were allowed to exceed 1 because of the possibility that some females could give birth
twice during the course of a year. For warthog we multiplied the summed proportion of newly
born piglets per adult by 0.5 to account for multiple offspring per litter and by a further 0.5 to
approximate the sex ratio of adults. This adjustment is a rough approximation because we did
not know the actual mean litter size for our study area. The various adjustments that we made
to counteract biases do not affect statistical relationships because it is the relative value of the
fertility and annual fecundity estimates that matter, not their absolute values. For the two
seasonally breeding species, survival from birth into the juvenile stage was calculated by relating
the mean proportion of juveniles over three months following the end of the birth peak to the
summed proportion of newborns through the peak. Correspondingly, to estimate survival
from juvenile into yearling stage, the mean proportion of juveniles aged around 3 months was
related to the mean proportion of yearlings aged around 12 months after the birth peak. For
the two non-seasonal species, merely the proportions of newborns, juveniles and yearlings
relative to adult females averaged over blocks of three months were derived. For certain analyses,
fertility was assessed over periods representing early births, summed over August-October,
modal births, summed over November-December, and late births, summed through
Relationships with seasonal or annual blocks of rainfall. Relationships of monthly
fertility, annual fecundity and offspring survival with prior blocks of rainfall were assessed by linear
Effective monthly fertility was related to monthly rainfall averaged over a time window
spanning the month of conception identified by cross-correlation analysis and the distributed
lag nonlinear model . The effective monthly fecundity was grouped by the season (early wet,
late wet and dry seasons) in which conception occurred to test the hypothesis that rainfall
influences the likelihood of conceptions. We dummy coded the seasons of conception to
permit relating effective monthly fecundity to rainfall using possibly different functional
relationships (linear or quadratic terms in rainfall) for each season of conception in the same model.
We expanded the model by adding the wet season rainfall in the preceding year, the current
dry season rainfall or both rainfall components to the model with rainfall block and season of
conception as the only predictors but this did not improve the fit for any of the four species.
Biologically, very low rainfall post-conception may cause foetal losses and hence fewer
births. Because this mechanism is distinct from conception, we considered different functional
relationships with fecundity emanating from the rainfall blocks. Moreover, since the effect of
rainfall post-conception is contingent on conceptions, it cannot be assessed independently, but
rather as a modifier of the births that would otherwise have been generated by rainfall prior to
conception. As a result, we considered the separate contributions of rainfall for the block of
months pre-conception and block of months post conception, subdividing the overall best-fit
block accordingly. Specifically, we used rainfall averaged over lags 9–12 or 9–11 and 7–8 to
represent rainfall influences pre-conception and post-conception, respectively, for topi and
hartebeest with gestation lengths of 7.5–8 months. The corresponding rainfall blocks were
averages over lags 7–10 and 6–7 for warthog and impala with gestation lengths of 5.5–6
months. Dummy coding of conception seasons was similarly used to enable relating monthly
apparent fecundity to each of these rainfall blocks. The data sets used in all the statistical
analyses and plots are provided in (S1–S3 Datas). The complete monthly age- and sex-structured
counts of the four study species and four additional species (giraffe, ostrich Struthio camelus
massaicus, waterbuck Kobus ellipsiprymnus and zebra Equus quagga) covering July 1989 to
December 2003 are provided in (S4 Data). The rainfall data for the study area for 1965–2004
averaged over all the rain gauges are provided in (S5 Data).
For topi, effective monthly fertility was mostly strongly related to the rainfall block 7–11 mo
prior to births, although this period spanned post-conception as well as pre-conception
months (Fig 1A, S1 and S2 Tables). However, the form of the relationship depended on the
seasonal period during which conceptions occurred. Early season fertility showed an
accelerating increase with rainfall prior to conception, while late season fertility showed no relationship
with generally high prior rainfall. Very few conceptions occurred during the dry season
months, when most females were already pregnant. Across all seasonal periods, fertility
remained low unless prior rainfall had exceeded about 250 mm summed over 4 months. A
reduction of fertility by low rainfall post-conception was supported statistically only for late
wet or dry season conceptions (S2 Table). Although high prior rainfall also appeared to depress
late conceptions, this was largely because the highest rainfall was associated with conceptions
occurring as late as Jan-Feb, after the seasonal peak. Rainfall in the month of conception had a
stronger effect on effective monthly fertility than rainfall prior to conception, suggesting that
the forage quality prevailing at the time of conception influences whether the foetus survives in
the first month.
For warthog, the strongest statistical relationship was with rainfall 6–10 months prior to
births, in this case spanning only the pre-conception period. Patterns largely replicated those
shown by topi, except for an apparent depressant effect of high prior rainfall on late season
conceptions (Fig 1B, S1 and S2 Tables). Few warthog conceived when prior rainfall had been
under about 300 mm. For hartebeest, there was a very weak although significant relationship
between monthly fertility and rainfall 7–10 mo prior to births, spanning the conception period
(Fig 1C). Separate relationships with rainfall blocks pre- and post-conception were not
apparent (S1 and S2 Tables), and conceptions frequently occurred even when prior rainfall had
Fig 1. Relationships between apparent fecundity and the best-supported rainfall block spanning conception months for each ungulate species for
the early wet (Nov-Dec), late wet (Jan-June) and dry (Jul-Oct) seasons of conceptions for a) topi, b) warthog, c) hartebeest and d) impala.
totalled <200 mm over the preceding 4 mo. Impala showed a very similar pattern to hartebeest
(Fig 1D, S1 and S2 Tables).
For topi, early season births (Aug-Oct) were positively related to early season rainfall (Sep-Feb)
prior to conception (Fig 2A). Consequently, modal (Nov-Dec) and late (Jan-Mar) births
appeared to be negatively related to early season rainfall (Fig 2B and 2C), while late births
showed no relation with late season rainfall (Mar-Jun) preceding the time of conception (Fig
2D, S3 Table). For warthog the relationship between early births and early season rain was
positive but much weaker than for topi (Fig A in S2 File, S3 Table). For hartebeest and impala,
early season births were unrelated to early season rainfall. Modal or late season births and
Fig 2. Relationships between a) early births (August-October), b) modal births (November-December), c) late births (January-March) and e) annual
fecundity and early rainfall (September-February) in the current year; d) late births and late rainfall (March-June), f) annual fecundity and g)
juvenile survival and annual rainfall (Nov-Jun) in the current year; h) juvenile survival and i) yearling survival and early rainfall in the preceding
year for topi. The patterns for topi well illustrate those for the other species.
annual fecundity appeared to be negatively related to seasonal or total annual rainfall for these
two species, as for topi (Fig A in S3 and S4 Files, S3 Table).
Total annual fecundity was related neither to early season rainfall nor to the total annual
rainfall for female topi (Fig 2E and 2F, S3 Table). However, offspring survival into the juvenile
stage was positively related to the preceding annual rainfall total (Fig 2G) and, less strongly, to
the current early season rainfall (Fig 2H). Further survival into the yearling stage appeared
similarly dependent on the early season rainfall in the current year (Fig 2I). For warthog there
were indications of humped relationships with prior rainfall especially for survival into the
juvenile stage (Fig A in S2 File). Hartebeest and impala both showed negative relationships
between annual fecundity and early season rainfall, although little or no relationship was
evident with the annual rainfall total (Fig A in S3 and S4 Files). For impala the neonate proportion
during the early season appeared positively related to early rains preceding conception. No
other significant relationships with rainfall were evident either for impala or for hartebeest (S3
Table). Survival into the juvenile stage increased linearly with increases in the preceding dry
season rainfall during gestation only for warthog (F1,7 = 6.14, P = 0.0423) but was not
significantly correlated with the early wet season rainfall post-birth for all the four species.
Our results reveal two distinct patterns, one represented by the two ungulate species that show
clear seasonal peaks in births, and the other by the two ungulate species with births widely
spread throughout the year. For topi and warthog, very few females conceived unless prior
rainfall over the preceding block of 4–5 months had exceeded a threshold value of around 250–
300 mm. For hartebeest and impala, the effect of rainfall on the effective fertility was very
weak, with the result that conceptions continued to occur during the dry season months despite
little prior rainfall. Correspondingly, more female topi conceived earlier in years when
preceding rainfall had been higher, while warthog showed a similar trend, albeit less strongly. In
contrast, hartebeest and impala showed no effect of prior rainfall on the proportion of females
conceiving during this period. Topi and warthog showed a consistently positive relationship
between prior annual rainfall and offspring survival after birth, but prior rainfall had no effect
on the survival of newborn hartebeest and impala. In general hartebeest and impala were
unresponsive to rainfall variation during the course of the year in their reproductive performance,
in contrast to topi and warthog. The observation that the rainfall influence extended through
the conception month for topi suggests that foetal loss post-conception in response to low
rainfall around this critical time might contribute to the effective fertility that we calculated. We
found only weak indications that exceptionally high rainfall inhibited conceptions and hence
subsequent births by producing excessively fibrous forage.
The distinction in reproductive phenology between topi and hartebeest was surprising,
considering that they are allied phylogenetically in the same antelope tribe (Alcelaphini) and seem
at least superficially similar in their grass dependency. However, the distribution of hartebeest
extends into drier regions of southern Africa than that of tsessebe (D.l. lunatus, conspecific
with topi). In southern Africa, both these antelope species show seasonal birth peaks timed
early during October-November, around the start of the rains [23–26]. Topi likewise breed
seasonally in the Tanzanian section of the Serengeti ecosystem (1° to 3° S), but with peak births
occurring a month earlier than in Mara, consistent with the earlier start of the short rains in
the Serengeti. Hartebeest reproduce year-round in Serengeti, with weak bimodal peaks in
AugSep and Dec, similar to the pattern in Mara. Wildebeest (Connochaetes taurinus) in Serengeti
exhibit a narrow concentration of births during February-March when the migrants throng the
short grass plains. Their conceptions evidently do not respond to the early season rains
experienced while they are still migrating southwards. Instead, conceptions are deferred to the early
dry season after the initiation of the return migration northwards. Zebra show a peak in births
during the late rains in both Serengeti and southern Africa, although this is somewhat diffuse,
probably because their 12-month gestation disrupts the seasonal synchrony of successive
Warthog show a narrow seasonal concentration of births in Serengeti as well as in southern
Africa. However, warthog give birth in all months where there is sufficient rainfall year-round
(e.g. in western Uganda, Zaire and Congo Brazzaville, [27,28]. Impala reproduce year-round in
Serengeti, with weak bimodal peaks in births in Jun-Aug and Oct-Jan . In southern Africa
south of the Zambezi River, impala consistently show a narrow birth peak, with 80% of lambs
born within a 2-week window extending from late November into early December
Variability in reproductive seasonality is also evident among other ungulate species.
Although sable antelope (Hippotragus niger) show a birth peak spread over about two months
in southern Africa, the timing of this peak varies from January-March in South Africa ,
Botswana  and Zimbabwe [32,33] to June-September in Zambia [34, 35] and Angola .
Near the equator in Kenya sable breed throughout the year . Sable reproduce year-round
in zoos, indicating a lack of photoperiodic control. However, roan antelope (Hippotragus
equinus), which likewise lack responsiveness to photoperiod in zoos , produce calves
through most months of the year in both eastern and southern Africa , as also do
waterbuck [6,39,40]. Other species giving birth throughout the year in southern Africa include
bushbuck (Tragelaphus scriptus) and nyala (Tragelaphus angasi), dependent largely on browse with
a different seasonal pattern of growth to grasses . Gemsbok (Oryx gazella), which are
grazers inhabiting arid savanna regions where rainfall patterns are erratic, reproduce in all months
of the year .
Year-round reproduction is the null response expected in equatorial latitudes where day
length variation is minimal, subject to minor variation from prevailing nutrition. This is the
pattern typical of impala, hartebeest and certain other ungulate species in equatorial East
Africa. In tropical India where monsoon rainfall generates seasonality in forage availability and
quality, chital (Axis axis) give birth early in the wet season when forage quality is highest, while
the much larger gaur (Bos gaurus) produces offspring throughout the year . Apparently
gaur are able to satisfy their minimum forage requirements all year round, while lactating chital
do so for less than 40% of the year . The antelope that breed year-round in southern Africa
are either grazers associated with habitats retaining some green grass year-round (e.g.,
waterbuck typically occur near water, while roan antelope favour grassy dambos or vleis ,
browsers like bushbuck, or occupy arid environments where the seasonal growth of grass is
unpredictable from year to year, like gemsbok.
For megaherbivores, sensitive stages of reproduction are spread through the year as a
consequence of prolonged gestation and slow growth to maturity of offspring. Despite this,
megaherbivores show distinct peaks in births resulting from a rise in conceptions during the early rains
[2,14]. Hence oestrous cycling in these species seems to be influenced proximally by the
prevailing nutritional regime, rather than governed ultimately by the conditions anticipated
around the time of births. The underlying mechanism appears to be the suppression of
oestrous cycling by low or deteriorating food quality [2,14,43]. A similar mechanism might
operate for topi and warthog, which in Mara rarely conceived when prior rainfall had totalled less
than 300 mm over the preceding few months. As a consequence of the dry season suppression,
a surge in conceptions occurs once early season rains alleviate this constraint, delayed by the
period required by females to recover their body condition. Accordingly, conceptions become
shifted earlier in years with higher early season rains, as previously reported by [7,44], but
without much effect on annual fecundity due to seasonal compensation. Annual variation in
recruitment was governed mainly by offspring viability through the early post-birth period,
rather than by the effects of rainfall on fertility. Hartebeest did not show much seasonal
reduction in fertility, perhaps because they are less strongly dependent on green grass than topi, as
implied by their wider distribution into drier regions. Impala are less responsive to rainfall
because they can obtain green browse through the dry season.
A further influence on seasonal reproductive patterns could be whether offspring hide or
follow their mothers shortly after birth. For followers a narrowing of the birth peak is favoured
by predator swamping , while for hiders this mechanism is unimportant. Topi calves are
followers and warthog piglets follow the mother after emerging from their burrows while still
highly vulnerable to predators. In contrast, hartebeest calves lie out for an extended period and
impala lambs for at least several days [22,45,46].
Nevertheless, the minimum monthly rainfall of around 50 mm during the dry season in
Masai Mara is vastly higher than the dry season rainfall experienced in southern African
savannas, where zero rainfall may be recorded during several successive months. This raises the
possibility that the seasonally restricted reproduction typical of many ungulate species in southern
Africa might be an outcome of the nutritional suppression of oestrus during the acutely dry
season, rather than governed by photoperiodic cues. This could help explain the unusually
early birth peaks shown by tsessebe, hartebeest and warthog in southern Africa. Other grazers,
such as wildebeest, have birth peaks better synchronized with the availability of high quality
forage, and corresponding mating peaks scheduled following the end of the wet season.
In conclusion, our findings highlight the influences of seasonal and annual variation in
rainfall on the reproductive phenology of tropical savanna ungulates. Species responding flexibly to
variable rainfall patterns are less likely to be threatened by reproductive mismatch due to the
effects of global climate change on plant phenology than ungulates inhabiting high northern
latitudes where day length more rigidly controls the timing of births. Nevertheless, widened
annual variation in rainfall could threaten populations of savanna herbivores by affecting
S4 Data. Age and sex-structured sample counts of seven species of ungulates and ostrich
along three road transects in Masai Mara National Reserve and its adjoining pastoral
ranches (Koyiaki and Siana) from July 1989 to December 2003.
S1 File. The monthly distribution of births among topi, warthog, hartebeest and impala in
the Mara-Serengeti ecosystem, adapted from  (Fig A). Three adult, one yearling and one
quarter-size topi, illustrating differences in body size, horn shape, horn size and body colour
used to group the animals into size-classes. Photo credit: Niels Mogensen (Fig B).
S2 File. Relationships between a) early births (August-October), b) modal births
(November-December), c) late births (January-March), e) annual fecundity and early rainfall
(September-February); d) late births and late rainfall (March-June), f) annual fecundity and g)
juvenile survival and annual rainfall (Nov-Jun); h) juvenile survival and early rainfall in the
preceding year for warthog (Fig A). An adult female warthog with a quarter-size young (Fig
B). Photo credit: Reto Buehler.
S3 File. Relationships between a) early births (August-October), b) modal births
(November-December), c) late births (January-March), e) annual fecundity and early rainfall
(September-February); d) late births and late rainfall (March-June), f) annual fecundity, g)
neonate survival, i) juvenile survival, j) yearling survival and annual rainfall (Nov-Jun); k)
neonate survival, juvenile survival and yearling survival and juvenile early rainfall in the
preceding year for hartebeest (Fig A). One adult male and two three-quarter size male Coke’s
hartebeests (Fig B). Photo credit: Niels Mogensen.
S4 File. Relationships between a) early births (August-October), b) modal births
(November-December), c) late births (January-March), e) annual fecundity and early rainfall
(September-February); d) late births and late rainfall (March-June), f) annual fecundity and g)
juvenile survival and annual rainfall (Nov-Jun); h) juvenile survival and early rainfall for
impala (Fig A). A full-grown and a young male impala, showing differences in horn size and
shape used to group males into size classes (Fig B). Photo credit: Reto Buehler. A female impala
in the company of three newborn lambs (Fig. C). Photo Credit: Reto Buehler.
S2 Table. Relationships between effective monthly fertility and selected rainfall blocks
spanning pre-conception (Rain7_8 for topi and hartebeest and Rain6_7 for warthog and
impala) and post-conception (Rain 9_11 for topi, Rain9_10 for hartebeest and Rain7_11
for warthog and impala) months grouped by season of conception. Significant effects are
shown in bold face font.
S3 Table. Results of linear regression of early births in August-October (EbirthsAO),
modal births in November-December (MbirthsND), late births in January-March
(LbirthsJM), annual fecundity (Annfecund), neonatal (NeonAD), newborn (NJsurv),
juvenile (Juven) and yearling (Yearl) survival on early rains spanning September-February
(ErainsSF), late rains spanning March-June (LrainMJ) and annual rains covering
September-October (AnRain) based on monthly ground counts conducted in the Masai Mara
National Reserve from July 1989 to December 2002. Significant effects are shown in bold
The Masai Mara Ecological Monitoring Program was designed and supervised by Dr. Holly T.
Dublin and executed by Paul Chara, John Naiyoma, Charles Matankory and Alex Obara. The
World Wide Fund for Nature-Eastern Africa Program (WWF-EARPO), the Kenya
Meteorological Department and Prof. K.E. Holekamp provided the rainfall data. We thank Drs. A.R.E
Sinclair, R. Hilborn and S.A.R. Mduma for advice on ageing and sexing animals. We are
grateful to the Office of the President of the Republic of Kenya, the Narok County Government
(formerly Narok County Council), the Kenya Wildlife Service (KWS), Wardens of the Masai Mara
National Reserve and the management of the former Koyiaki Group Ranch for permission and
collaboration in conducting this research. We thank the associate editors and two reviewers for
constructive and helpful comments and suggestions.
Conceived and designed the experiments: HTD. Performed the experiments: HTD. Analyzed
the data: JOO NOS HPP. Contributed reagents/materials/analysis tools: HTD JOO NOS HPP.
Wrote the paper: JOO NOS HPP HTD.
1. Owen-Smith N. Adaptive herbivore eEcology. From resources to populations in variable environments . Cambridge : Cambridge University Press ; 2002 .
2. Owen‐Smith N , Ogutu JO . Controls over reproductive phenology among ungulates: allometry and tropical‐temperate contrasts . Ecography 2013 ; 36 : 256 - 263 .
3. Oftedal OT . Pregnancy and lactation . In: Hudson RJ, White RG, editors. Bioenergetics of wild herbivores. Florida: CRC Press ; 1985 . pp. 215 - 238 .
4. Zerbe P , Marcus C , Codron D , Lackey LB , Rensch E , Streich JW , et al. Reproductive seasonality in captive wild ruminants: implications for biogeographical, photoperiodic control, and life history . Biol Rev . 2012 ; 87 : 965 - 990 . doi: 10.1111/j.1469-185X.2012.00238.x PMID: 22780447
5. Skinner JD , Moss DG , Skinner DC . Inherent seasonality in the breeding seasons of African mammals: evidence from captive breeding . Trans Roy Soc S Afr . 2002 ; 57 : 25 - 34 .
6. Sinclair ARE , Mduma SAR , Arcese P. What determines phenology and synchrony of ungulate breeding in Serengeti? Ecology 2000 ; 81 : 2100 - 2111 .
7. Ogutu JO , Piepho H-P , Dublin HT , Bhola N , Reid RS . Rainfall extremes explain interannual shifts in timing and synchrony of calving in topi and warthog . Pop Ecol . 2010 ; 52 : 89 - 102 .
8. Ogutu JO , Piepho H-P , Dublin HT. Reproductive seasonality in African ungulates in relation to rainfall . Wildl Res . 2015 ; 41 : 323 - 342 .
9. Estes RD . The significance of breeding synchrony in the wildebeest . Afr J Ecol . 1976 ; 14 : 135 - 152 .
10. Rutberg AT . Adaptive hypotheses of birth synchrony in ruminants: an interspecific test . Am Nat . 1987 ; 130 : 692 - 710 .
11. Moss CJ . The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya . J Zool . 2001 ; 255 : 145 - 156 .
12. Wittemyer G , Rasmussen HB , Douglas-Hamilton I. Breeding phenology in relation to NDVI variability in free-ranging African elephant . Ecography 2007 ; 30 : 42 - 50 .
13. Hall-Martin AJ , Skinner JD , Van Dyk JM . Reproduction in the giraffe in relation to some environmental factors . Afr J Ecol . 1975 ; 13 : 237 - 248 .
14. Owen-Smith RN. Megaherbivores : The influence of very large body size on ecology . Cambridge : Cambridge University Press ; 1988 .
15. Post E , Forchammer MC . Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch . Trans Roy Soc Lond, Ser B . 2008 ; 363 : 2369 - 2375 .
16. Allan RP , Soden B. Atmospheric warming and the amplification of precipitation patterns . Science 2008 ; 321 : 1481 - 1484 . doi: 10.1126/science.1160787 PMID: 18687921
17. Ogutu JO , Piepho H-P , Dublin HT , Bhola N , Reid RS . El Niño-Southern Oscillation, rainfall, temperature and Normalized Difference Vegetation Index fluctuations in the Mara-Serengeti ecosystem . Afr J Ecol. 2008a; 46 : 132 - 143 .
18. Boutton TW , Tieszen LL , Imbamba SK . Biomass dynamics of grassland vegetation in Kenya . Afr J Ecol. 1988a; 26 : 89 - 101 .
19. Boutton TW , Tieszen LL , Imbamba SK . Seasonal changes in the nutrient of East African grassland vegetation . Afr J Ecol. 1988b; 26 : 103 - 115 .
20. Ogutu JO , Piepho H-P , Dublin HT , Bhola N , Reid RS . Rainfall influences on ungulate population abundance in the Mara-Serengeti ecosystem . J Anim Ecol. 2008b; 77 : 814 - 829 .
21. Ogutu JO , Piepho H-P , Dublin HT , Bhola N , Reid RS . Dynamics of Mara-Serengeti ungulates in relation to land use changes . J Zool . 2009 ; 278 : 1 - 14 .
22. Skinner JD , Chimimba CT . The Mammals of the Southern African Subregion . Cambridge : Cambridge University Press ; 2005 .
23. Fairall N. The reproductive seasons of some mammals in the Kruger National Park . Afr Zool . 1968 ; 3 : 180 - 210 .
24. Skinner JD , Van Zyl JH , Van Heerden JAH . The effect of season on reproduction in the black wildebeest and red hartebeest in South Africa . J Reprod and Fertil (Suppl) 1973 ; 19 : 101 - 110 .
25. Skinner JD , Van Zyl JH ; Oates LC . The effect of season on the breeding cycle of plains antelope of the western Transvaal highveld . J S Afr Wildl Manage Assoc 1974 ; 4 : 15 - 23 .
26. Anderson JL . 1979 Reproductive seasonality of the nyala Tragelaphus angasi: The interaction of light, vegetation phenology, feeding style and reproductive physiology . Mamm Rev 1979 ; 9 : 33 - 46 .
27. Brown CE . Rearing wild animals in captivity and gestation periods . J Mammal . 1936 ; 17 : 10 - 13 .
28. Clough G . Some preliminary observations on reproduction in the warthog , Pharcochoerus aethiopicus Pallas. J Reprod and Fertil (Suppl) 1969 ; 6 : 323 - 337 .
29. Moe SR , Rutina LP , du Toit JT. Trade-off between resource seasonality and predation risk explains reproductive chronology in impala . J Zool . 2007 ; 273 : 237 - 243 .
30. Murray MG . The rut of the impala: Aspects of seasonal mating under tropical conditions . Z Tierpsychol . 1982 ; 59 : 319 - 337 .
31. Child G . Report to the Government of Botswana on an ecological survey of north-eastern Botswana . FAO report PA 2563 , 1968 ; 133pp .
32. Child G , Wilson VJ . Observations on ecology and behaviour of roan and sable in three tsetse control areas . Arnoldia Rhodesia 1964 ; 16 : 1 - 8 .
33. Wilson VJ . The large mammals of the Matapos National Park . Arnoldia Rhodeia 1969 ; 4 : 1 - 32 .
34. Ansell WFH . The breeding of some larger mammals in northern Rhodesia . Proc Zool Soc Lond . 1960 ; 134 : 251 - 274 .
35. Ansell WFH . Additional breeding data on Northern Rhodesian mammals . Puku 1963 ; 1 : 9 - 19 .
36. Estes RD , Estes RK . The biology and conservation of the giant sable antelope (Hippotragus niger variani Thomas , 1916 ). Proc Acad Nat Sci Phila 1974 ; 126 : 73 - 104 .
37. Sekulic R. Seasonality of reproduction in the sable antelope . Afr J Ecol . 1978 ; 16 : 177 - 182 .
38. Wilson DE , Hirst SM . Ecology and factors limiting roan and sable antelope populations in South Africa . Wildl Monogr 1977 ; No 54. Washington, DC: The Wildlife Society.
39. Spinage CA . Reproduction in the Uganda defassa waterbuck, Kobus defassa ugandae Neumann . J Reprod and Fertil 1969 ; 18 : 445 - 457 .
40. Ogutu JO , Piepho H-P , Dublin HT , Bhola N , Reid RS . Dynamics of births and juvenile recruitment in Mara-Serengeti ungulates in relation to climatic and land use changes . Pop Ecol . 2011 ; 53 : 195 - 213 .
41. Ahrestani FS , Van Langevelde F , Heitkönig I , Prins HHT . Contrasting timing of parturition of chital Axis axis and gaur Bos gaurus in tropical South India-the role of body mass and seasonal forage quality . Oikos 2012 ; 121 : 1300 - 1310 .
42. Knoop MC , Owen‐Smith N. Foraging ecology of roan antelope: key resources during critical periods . Afr J Ecol . 2006 ; 44 : 228 - 236 .
43. Laws RM , Parker ISC , Johnstone RCB . Elephants and their habitats . Oxford: Clarendon Press ; 1975 .
44. Ogutu JO , Piepho H-P , Dublin HT. Responses of phenology, synchrony and fecundity of breeding by African ungulates to interannual variation in rainfall . Wild Res . 2014 ; 40 : 698 - 717 .
45. Gosling LM . Parturition and related behavior in Coke's hartebeest, Alcelaphus buselaphus cokei Günther . J Reprod and Fertil (Suppl) 1969 ; 6 : 265 - 286 .
46. Estes RD . The Behavior Guide to African Mammals. Los Angeles and London: University of California Press.