Journal of Zoology
Journal of Zoology. Print ISSN 0952-8369
Masking of the zeitgeber: African wild dogs mitigate
persecution by balancing time
G. S. A. Rasmussen1,2 & D. W. Macdonald1
1 Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, The Recanati-Kaplan Centre, Tubney, Oxon, UK
2 Painted Dog Research, Natural History Museum PO Box 240, Bulawayo, Zimbabwe
Keywords
behavioural plasticity; diel activity;
interspecific competition; Lycaon pictus;
moonlight hunting; zeitgeber masking.
Correspondence
Gregory Rasmussen, Wildlife Conservation
Research Unit, Department of Zoology,
University of Oxford, The Recanati-Kaplan
Centre, Tubney House, Tubney, Oxon
OX13 5QL, UK
Email: [email protected]
Editor: Nigel Bennett
Received 12 June 2011; revised 29
September 2011; accepted 3 October 2011
doi:10.1111/j.1469-7998.2011.00874.x
Abstract
The African wild dog Lycaon pictus is endangered, with anthropogenic impacts,
pack size dynamics and competing predators explaining its decline. Relative to
solar and lunar events, analysis of diel activity in two parapatric Zimbabwean
populations revealed behavioural plasticity in response to human activity. In
Hwange, human presence was low; in Nyamandlovu, human presence and persecution were high. In both populations, Lycaon frequently hunted by moonlight,
with 3–4 lux of light restricting nocturnal hunting to 13 days/lunar month. With
diurnal hunts commencing at ‘civil twilight begin’ and ending at ‘astronomical
twilight end’, light intensity was confirmed as a limiting factor.
Nyamandlovu dogs exhibited behavioural plasticity, demonstrated by scattered rather than clumped organization when at rest, and masked the zeitgeber by
utilizing evenings and moonlight for more days under suboptimal light conditions
than did Hwange dogs. Significantly, different allocation of morning, evening and
moonlight hunts between Hwange (47%, 36%, 15%) and Nyamandlovu (28%,
31%, 41%), reduced the temporal potential for human encounter by 64%, but
increased this potential for hyaena and lion encounters by 70% and 37%, thus
highlighting the trade-off of this switch. Finally, we tentatively conclude that the
cue masking the ‘zeitgeber’ is risk, rather than gain related, and could be seen as
an evolutionary ‘emergency exit’, the understanding of which is important to
conservation in landscapes that are increasingly dominated by people.
Introduction
Daily rhythms are controlled by a circadian clock, entrained
to the overriding cue of light intensity (a ‘zeitgeber’ in the
terms of Lorenz & Kickert, 1981), and in evolutionary terms,
responding to a zeitgeber facilitates efficient use of the environment (Kronfeld-Schor et al., 2001). Here, it triggers appropriately timed, physiological and behavioural responses
(Heldmaier et al., 1989; Refinetti, Nelson & Menaker, 1992;
Aronson et al., 1993), and facilitates interspecific coexistence
(Schoener, 1974; Richards, 2002). Though temporal partitioning in communities has never been a strong focus of ecology
(Kronfeld-Schor & Dayan, 2003) and biologists are aware
that there is a degree of rigidity in the response to light, there
are few field data to reveal the plasticity of this endogenous
rhythmicity. In particular, little is known of what triggers are
likely to mask the zeitgeber, although there are examples
where one species causes another to adopt an opposite activity
pattern [e.g. mink Neovison vison : otter Lutra lutra and fox
Vulpes vulpes : rat Rattus norvegicus interactions (Fenn &
Macdonald, 1995; Harrington et al., 2009)].
Furthermore, in the context of landscapes increasingly
dominated by people, behavioural plasticity may reduce the
threats to a species but will incur a cost [e.g. hyaenas Crocuta
crocuta (Boydston et al., 2003)]. With the African wild dog or
painted hunting dog (Courchamp, Rasmussen & Macdonald,
2002) Lycaon pictus (hereinafter referred to as Lycaon) representing a monotypic genus and listed as endangered by the
International Union for Conservation of Nature/Species
Survival Commission (Woodroffe, Ginsberg & Macdonald,
1997), the aim of this article is therefore to explore (1) the
relationship between activity patterns of Lycaon and sympatric competition under ‘natural’ conditions of coexistence; (2)
plasticity in response to high anthropogenic activity; (3)
potential costs of sub-optimization and masking behaviours.
We present data from two parapatric Lycaon populations in
Zimbabwe, and their competitors. As circadian entrainment is
essentially light driven, we make our measurements relative to
solar and lunar light cues.
Lycaon are eusocial (Sherman et al., 1994; Rasmussen
et al., 2008) kin-selected, obligate cooperative breeding canids
(Courchamp et al., 2002), living in packs of up to 20 adults.
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
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Masking the zeitgeber to mitigate persecution
Usually, only the alpha pair breeds, with the remaining adults
being reproductively suppressed. It is among the most endangered large carnivores in Africa, with most of the remaining
packs being in populations too small to be viable (Woodroffe
et al., 1997) and the question is raised as to why Lycaon populations not only declined faster than those of sympatric carnivores, but also have failed to recover (Creel & Creel, 1998).
Though causes of Lycaon mortality have been well documented, with anthropogenic mortality being recorded as a
significant factor depressing populations in some systems
(Woodroffe et al., 2007), the relationship between diel activity, how it could increase their conspicuousness and hence
vulnerability to anthropogenic impact (Rasmussen, 1999), has
not. This article investigates the hypothesis that the optimal
foraging conditions for Lycaon impose high temporal niche
overlap with humans, thereby putting them at greater risk
than some other sympatric carnivores.
To date, on the assumption that moonlight hunting does not
occur, the activity of Lycaon has been described as crepuscular
to diurnal (Saleni et al., 2007). Lycaon hunt small to large
ungulates (Childes, 1988; Creel & Creel, 2002; Rasmussen
et al., 2008), and occasionally livestock (Rasmussen, 1999).
Lycaon select for sick and weak individuals (Pole, Gordon &
Gorman, 2003), which considering the extreme energetic cost
of chasing may be a crucial life strategy (Rasmussen et al.,
2008). Hyaenas Crocuta crocuta and lions Panthera leo kleptoparasitize Lycaon, with this impact being particularly significant in packs of less than six individuals (Rasmussen, 2009), so
with lions also killing adults and pups, any changes in encounter with these predators is likely to have major implications.
It is plausible that changing pack dynamics will also affect
diel activity, time windows utilized and encounters with competitors to include humans, which as a consequence of shooting, cars and snares, contribute to 93% of all Lycaon mortality
in Zimbabwean ranch land (Rasmussen, 1997). This high figure
is not unusual for canids, for which anthropogenic mortality is
often the greatest threat. For example, human-induced mortality in wolves ranges from 80% in America (Ballard, Whitman &
Gardner, 1987; Fuller, 1989) to 92% in parts of Europe (Smietana & Wajda, 1997). Similarly, humans are responsible for
most coyote, Canis latrans mortalities (Windberg, Anderson &
Engeman, 1985; Gese, Rongstad & Mytton, 1989). As predators are known to respond behaviourally to levels of anthropogenic disturbance (Vila, Urios & Castroviejo, 1995; Ciucci
et al., 1997; Sillero-Zubiri & Macdonald, 1997; Kitchen, Gese
& Schauster, 2000; Boydston et al., 2003), it is likely that
Lycaon will too. In such cases, while behavioural plasticity can
facilitate survival, it will come at energetic cost.
Methods
Fieldwork was conducted in two parapatric study sites separated by 150 km: Hwange National Park in the north-west of
Zimbabwe, and adjacent areas, totalling 5500 km2 (April 1994
and December 2002); and the Nyamandlovu farming region
totalling 1000 km2 (April 1994 until June 1997), with Lycaon
densities being 0.93/100 km2 and 0.84/100 km2, respectively
(Rasmussen, 1997). Data for the Nyamandlovu study came
2
G. S. A. Rasmussen and D. W. Macdonald
from three packs coexisting with spotted hyaenas at a density
of 6/100 km2, with lions being occasional vagrants (this study).
Land use was 93% cattle ranching, 7% hunting safari area with
suitable prey species including kudu (Tragelaphus strepsiceros), duiker (Sylvicapra grimmea) and impala (Aepyceros
melampus; Childes, 1988; Rasmussen, 1997). Cattle stocking
rates (including calves) averaged 5.5/km2 in winter to 13.2/km2
in summer (Rasmussen, 1999) with trophy hunting of ungulates occurring from May to October. As the Nyamandlovu
ranching region was 60 km from the nearest town, light
sources for both study areas were the same.
Hwange focal packs were those that either resided entirely
in areas contiguous with the park or occupied home ranges
within 60 km of the park border, lions [2.7/100 km2 (Loveridge et al., 2007)], hyaenas [10.2/100 km2 (Salnicki, 2002)]
leopards and suitable prey (Bougarel, 2004) being present
throughout the study area. Land use comprised 35% national
park, 25% photographic safari area, 35% hunting safari area
and 5% cattle ranching. Data came from 22 known packs, 13
of which were radio collared for all or part their study, and by
using foot tracking, a small number of unidentified units.
Study time, in months, for the known packs, ranged from 3.9
to 73.3, x = 29.5, sd = 20.11.
For this study, 18 dogs (11 males, 7 females) were chemically
immobilized with a ketamine : xylazine (Pfizer, Kent, UK)
dose of 180 mg : 33 mg. Only adults over the age of 14 months
were collared, with the individual being selected on the basis of
the safety of the shot. Alpha females were never collared even if
not suspected to be pregnant because ketamine is known to
cross the placental barrier. Darting was only undertaken in the
mornings in order to reduce the predation risk from interguild
competitors, and restricted to open habitats to reduce the
likelihood of losing an anaesthetized animal. Administration
of the drug was intramuscular in the rear quarter using
1.8 mm Dan-Inject syringes (Dan-Inject ApS., Copenhagen,
Denmark) with 2.0 mm, side-ported needles and a Dan-Inject
1M rifle. Uncollared dropout needles were used as a precaution
against either an incomplete injection leaving an uncaptured
animal with a needle left in (that it is not believed would fall
out), or an inter-os misplacement that if caused by a collared or
barbed needle would create excessive site trauma both on entry
and removal. Rectal body temperature, breathing, pulse rates,
oxygen saturation and capillary refill time were monitored
throughout the anaesthesia. Dogs were regularly turned to
reduce oedema, with this procedure being executed sternally
to avoid stomach torsion. Once recumbent, 1 mL vitamin
B complex (Alphasan, Woerden, Netherlands) was given
as a compensator for stress-induced losses, along with
Effortil (Boehringer Irgelheim Vetmedica GmbH, Irgelheim,
Germany) to improve cardiac output, mean systemic blood
pressure and aorto-coronary bypass flow were administered.
All procedures on anaesthetized animals were carried out in situ
with the dogs being laid on the non-thermal side of a heavy duty
‘All weather blanket’ (http://www.forestry-suppliers.com),
which could be reversed if a hypothermic condition arose.
Conversely, water from a knapsack sprayer was used to
counter any hyperthermic condition. As the depth of anaesthesia could not be measured, precautions were taken to reduce
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
G. S. A. Rasmussen and D. W. Macdonald
possible stress from awareness of close proximity with humans.
These measures involved the dogs being blindfolded and fitted
with earmuffs specially designed to allow easy removal by the
study animal in case of an unexpected recovery. As frequently,
other members of the pack were waiting as close as 10 m away,
no erect postures were adopted by assisting personnel
and communications were kept silent by using predetermined
hand signals. If extended anaesthesia was needed, top-up
ketamine : xylazine doses were 100 mg : 10 mg concomitant
with the fact that xylazine has a longer half-life than ketamine.
When vital reflex signs indicated that the ketamine (whose
half-life is shorter than xylazine) was nearly metabolized, the
immobilizations were reversed with 4–6 mg of atipamezole
(Pfizer) intramuscularly.
In order to reduce the need to re-anaesthetize an animal, the
collars (mass 425 g, 1.70% mean body weight mass, n = 18,
range 1.89–1.49%) from Sirtrack (http://www.sirtrack.com),
were designed to have a battery life of 6 years at the expense of
lower output. In order to spread the weight, reduce the likelihood of chafing and inhibit dorsolateral movement, belting
width was increases from the standard 35 mm to 50 mm. The
lower frontal section of the collar was pre-moulded to the neck
of the dogs, with the batteries spread from the transmitting
unit so that the weight of the batteries was evenly distributed
over the whole lower section of the collar. Finally, the antenna
was re-routed to exit at right angles to the collar and run along
the shoulder to minimize irritation or interference with the
dog’s movement. When a dog was no longer being monitored,
the collar was removed. All immobilized dogs were monitored
for 24 h post-anaesthesia to ensure safe return and integration
into their pack with no adverse effects being seen from either
procedures or the collar itself.
Once packs were located, they were followed for as many
days as possible. For the period of the study, a ceasefire agreement was negotiated with farmers in both study areas, but as
some land owners’ attitudes were hostile to both Lycaon and
the researchers, compounded by difficult terrain, poor road
network, dense habitat, lack of landowner compliance, vehicle
breakdown and punctures, some hunt follows were only partially completed. The collars included activity sensors such
that 15 beats per minute (bpm) = mortality, 30 bpm = rest,
45 bpm = active, with individual collared dogs having separate
frequencies. Once packs were located, using telemetry, they
were monitored by a field observer (G. R.) and national park
scout continuously doing shifts during the hours the dogs were
resting. This entailed remaining with the dogs throughout
their activity and rest periods at a distance of ⱖ50 m for up to
a maximum of 28 days. To determine hunt period time and
time windows utilized, data were recorded at 5 min scan intervals. Time event data collected were as follows: (1) commenced hunt, defined as leaving the resting site; (2) end hunt,
defined as the commencement of the first rest period greater
than 30 min; (3) hunt period (HP), denoted as the time interval
in minutes between consecutive rests for a morning, afternoon, moonlight or middle of the day activity period. Any
short periods of rest >10 min were subtracted from the time
interval of the rest-to-rest period, hunt period time (HPT) was
the duration of this interval, (4) number of HP per day (nHP)
Masking the zeitgeber to mitigate persecution
was defined as the sum of all HP recorded during the 24-h
period between 00:00 and 23:59 h.
Almanac data to equate the time of dog events in relation to
solar and lunar phases were compiled for all years and
obtained from http://aa.usno.navy.mil/ for the relevant latitudes and longitudes (Hwange: 18-30S 27-00E; Nyamandlovu
19-30S 28-30E). These event data were then related in minutes
to the pertinent solar and lunar events and denoted (-) =
before (+) = after. Definitions of the solar and lunar events
from http://aa.usno.navy.mil/ are as follow:
(1) Civil twilight is defined to begin in the morning, and to
end in the evening when the centre of the sun is geometrically
6 degrees below the horizon. This is the limit at which twilight
illumination is sufficient, under good weather conditions, for
terrestrial objects to be clearly distinguished.
(2) Nautical twilight is defined to begin in the morning, and to
end in the evening, when the centre of the sun is geometrically
12 degrees below the horizon. At the beginning or end of
nautical twilight, under good atmospheric conditions and in
the absence of other illumination, general outlines of ground
objects may be distinguishable.
(3) Astronomical twilight is defined to ‘begin’ in the morning,
and to ‘end’ in the evening when the centre of the sun is
geometrically 18 degrees below the horizon. Before the beginning of astronomical twilight in the morning and after the end
of astronomical twilight in the evening, the sun does not contribute to sky illumination. At the beginning or end of astronomical twilight, under good atmospheric conditions and in
the absence of other illumination, general outlines of ground
objects are not distinguishable.
(4) Moon transit time refers to the instant that its centre
crosses an imaginary line in the sky, the observer’s meridian,
running from north to south. For observers in low to middle
latitudes, transit is approximately midway between rise and
set, and represents the time at which the body is highest in the
sky on any given day.
(5) Twilight to sunrise and civil to astronomical twilight time
intervals were calculated from the almanac data compiled
using the mean value of all the study years.
(6) Percent of the moon illuminated was denoted as the fraction of the moon illuminated.
(7) Relationship to the nearest full moon in days before full
moon at transit time was denoted by ‘minus’ for days before
and plus for days after.
As there is no morphological evidence to imply that Lycaon
have any specialized night vision adaptation, the official definitions are believed appropriate for this canid.
Finally, in order to incorporate interspecific competition
into modelled time niche overlaps, activity data were collated
from the literature for lions and hyaenas, with human activity
being known from the local area.
Statistics
SPSS v.11 (SPSS Inc., Chicago, IL, USA) was used for all
statistical analyses. For the data pertinent to the utilization
percentage of the moon visible, non-parametric Kolmogorov–
Smirnov tests were used. All tests were two tailed with signifi-
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
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Masking the zeitgeber to mitigate persecution
G. S. A. Rasmussen and D. W. Macdonald
AM, PM and ML activity times in minutes differed significantly from each other F2,479 = 22.69, P < 0.0001 with mean
times as follows:
(n = 95) 100 min after MMT ( x = 100.6 min , sd = 73.4, min =
-74, max = 350). No hunts were recorded on nights when
available moonlight was obscured by cloud cover. In both
study areas during each lunar month, dogs hunted by moonlight a maximum of 13 days (7 days before the full moon to
6 days after). Kills (n = 63) occurred 36 min after MMT
( x = 36.0 min, sd = 81.7, min = 139, max = 269). ML activity
period time was ( x = 169.1 min , sd = 55.82, min = 55, max =
320).
In relation to the percentage of the moon visible, Lycaon
hunted only with ⱖ49% of the moon visible on a rising moon
and ⱖ58% on a setting moon. Nyamandlovu dogs however
utilized lower light conditions more frequently (Fig. 1). Testing
for both percentage of hunts undertaken in relationship to
the available moon visible, and days before/after the full
moon, showed these population differences to be significant
(Kolmogorov–Smirnov z = 1.839 P = 0.002 and z = 1.567 P =
0.015). Use of a light meter (Extech Foot Candle/Lux Meter,
Extech Instruments Corp., Waltham, MA, USA) during the
moonlit hunts indicated that the limiting light condition was
between 3 and 4 lux. Attempts to use the meter for the solar
twilights failed to detect the breakpoint as the light conditions
changed so rapidly that the meter (designed for lower light
levels) would, in a time span too fast for the observer eye, go
from reading nothing to a light level off the scale.
Morning hunts
Midday hunts
AM hunts commenced closer to, and just before civil twilight (n
= 227, x = −7.4 min , sd = 33.1, min = -116, max = 137) than to
nautical twilight end ( x = 18.9 min , sd = 33.8, min = -98, max
= 166) thus indicating that because civil twilight is the limit at
which a terrestrial object can be clearly distinguished, light may
be deemed a limiting factor (see definitions). Hunts occurring
considerably earlier than civil twilight were facilitated by the
light of a setting moon. AM hunts ended 2 h after sunrise (n =
219, x = 118.3, sd = 59.5, min = 10, max = 283). Kills (n = 350)
occurred on average 54 min after sunrise ( x = 53.7, sd = 61.1,
min = -95, max = 280). Overall AM activity period time was
x = 145.0 min (sd = 53.3, min = 40, max = 320).
There were only three MD hunts ( x = 173.3, sd = 147.4, min =
60, max = 340) so no inferences could be drawn and they were
excluded from analyses.
cance = P < 0.05. Pearson’s correlations were used to test for
relationships between variables.
Results
In Hwange, 571 HP follows were attempted, with activity
being almost exclusive to three periods, morning (AM),
evening (PM) and when there was sufficient moonlight (ML).
Hunts close to midday (MD) were rare. Number of complete
hunts followed were AM = 206, PM = 185, ML = 90, MD = 3.
Partial hunts (p) followed were AMp = 38, PMp = 23, MLp = 24,
MDp = 3. Total activity pattern was complete for 316 days
resulting in the following HP allocation: 244 AM hunts (47%),
186 PM hunts (36%), 79 ML hunts (15%) and 5 MD hunts
(1%). In the Nyamandlovu study, though one dog was collared, farmland fences made hunt follows impossible and
though total activity time was not deduced, the HP allocation
was obtained as follows n = 99, AM hunts (28%), 186 PM
hunts (31%), 79 ML hunts (41%).
Activity in relation to time of day
Evening hunts
PM hunts commenced 1 h before sunset (n = 199,
x = 0 − 56.7 min, sd = 30.8, min = -136, max = 27), and ended
(n = 195) 5 min before astronomical twilight end ( x = −4.9, sd
= 47.2, min = -118, max = 158) when by definition there is no
utilizable light from the sun, again suggesting light as a limiting factor. Extended hunts, resulting in positive outliers, were
concurrent with a rising moon. Kills occurred on average
7 min after sunset (n = 258, x = 7.4 min, sd = 58.8, min = -174,
max = 236).
Spatial organization and pup provisioning
The two populations showed different behavioural patterns by
exhibiting different spatial organization when at rest and different pup provisioning patterns. In accordance with other
studies (Scott, 1991; McNutt et al., 1997; Creel & Creel, 2002),
the Hwange study packs rested as a group or at least in close
proximity to one another (<50 m); however, the Nyamandlovu dogs were never detected at rest as a group and on all
encounters following foot tracking (n = 43), were scattered,
often resting >200 m apart as singletons or as pairs. This was
evidenced from the multidirectional alarm calls of the dogs
upon being detected, as well as trackers pointing out where
individual dogs had been resting. With respect to pup provisioning in the Hwange study, in only five cases out of 155 AM
hunts did the dogs not return to the den after killing and
feeding successfully. By contrast in Nyamandlovu from 38
AM hunts, on no occasion, did they return to the den until
either sunset (n = 2) or after astronomical twilight end (n = 36).
Demography
Moonlight hunts
ML hunts maximized on moonlight by starting 1 h before the
moon was at its apex at moon meridian time (n = 119, MMT)
( x = −60.4 min, sd = 62.3, min = -204, max = 190), and ended
4
In spite of no dogs being shot during the period of study,
mean adult, yearling (AY) and adult, yearling, pup (AYP)
pack sizes were significantly lower in the Nyamandlovu region
(F(AY)1,2143 = 8.67, P = 0.003) (F(AYP)1,2143 = 43.77, P ⱕ 0.001).
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
G. S. A. Rasmussen and D. W. Macdonald
Masking the zeitgeber to mitigate persecution
Figure 1 Frequency of hunts undertaken by Lycaon pictus in relation to (a) the percentage visibility of the waxing and waning moon in the Hwange
and Nyamandlovu regions of Zimbabwe; (b) the number of days before and after full moon.
Means for the two regions follow: Hwange [n = 2045
( x AY = 5.65, sd = 2.7) ( x AYP = 11.52 , sd = 5.0)]; Nyamandlovu
[n = 99 ( x AY = 4.85 , sd = 2.7) ( x AYP = 8.16 , sd = 4.3)].
Activity in relation to pack size
Previously published data from the same population over the
same time period in Hwange during the denning season and
nomadic phase (Rasmussen et al., 2008) showed no significant
relationship between pack size and HPT, but significant differences between pack size and nHP. Based on the number of
weeks for which packs of given sizes were denned or nomadic
(Rasmussen et al., 2008), these data were used to calculate: An
annual mean HPT of 138 min; a relationship between nHP
and pack size. Multiplying the number of hunt periods per day
by the hunt period time gave the relationship between daily
HPT and pack size (Fig. 2)
Using nHP data, relative percentages of AM, PM and ML
hunts per day relative to pack size were determined. This gave
the results (Fig. 3), that as pack size increased, moonlight hunts
increased (r2 = 0.59, P = 0.05), AM hunts decreased (r2 = 0.60, P
< 0.001) and PM hunts showed no significant change (r2 = 0.121,
P = 0.643). Part of the decrease in AM hunts is explained by the
fact that post-ML hunts, the dogs were sated, as reinforced by
the data revealing that on only 27% of occasions did AM hunts
Figure 2 Number of hunt periods per day as a function of pack size for
Lycaon pictus in the Hwange region Zimbabwe (data from (Rasmussen
et al., 2008).
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Masking the zeitgeber to mitigate persecution
G. S. A. Rasmussen and D. W. Macdonald
thus enabled a time window utilization to be calculated for
AM, PM and ML hunts in both study areas (Fig. 4). It also
highlights both the contribution of the hitherto unstudied ML
time niche and the altered time dynamics of the behavioural
shift.
Interspecific competition
Lions are primarily nocturnal (Kruuk & Turner, 1967;
Schaller, 1972; Van Orsdol, 1984; Prins & Iason, 1989;
Stander, 1991), with main activity (activity > 20 min) commencing 1–2 h after sunset (astronomical twilight), peaking
between midnight and 04:00 h and ceasing at sunrise (Van
Orsdol, 1984). The same activity pattern was found in a study
of buffalo and their vigilance response to lion activity (Prins &
Iason, 1989). Studies also show that lions adjust their nocturnal hunting period to coincide with either moonless hours or
periods of cloud cover (Schaller, 1972; Van Orsdol, 1984). In
this study, out of 520 kills (AM = 281, PM = 198, ML = 39,
MD = 2), lions were present on only eight occasions (1.5%;
AM = 4, PM = 3, ML = 1).
Hyaenas are predominately nocturnal, commencing activity
after sunset and operating through the night from moonless to
full moon nights (Cooper, 1990), though in cooler weather,
they do hunt in daylight (Cooper, 1990). Therefore, it is more
likely that Lycaon will encounter hyaenas than lions. In this
study, hyaenas were present at 41 kills (7.9%) of which the
greater percent were AM and PM hunts (AM = 19, PM = 18,
ML = 4), and at one kill both hyaenas and lions were present.
Humans utilize very closely the time niche used by Lycaon
with ranchers and rural communities commencing work as
soon as there is available light, which by definition would
begin and end at civil twilight, with a slowing down of activities close to midday due to heat. This being the case, with the
exception of moonlight hunting, in terms of time overlap and
the 53-min interval between the end of civil and astronomical
twilight Lycaon mirrors the time niche of humans.
Modelling of time overlaps
Using the aforementioned data, time niche overlaps were
determined to be as follows:
Humans
Figure 3 Percentage of hunts undertaken as a function of pack size by
Lycaon pictus in the Hwange region Zimbabwe.
AM = Time sympatry for whole HP
PM = Time sympatry for whole HP minus 53 min
ML = Total time allopatric
Hyaenas
follow ML hunts (n = 116). The rest of the resultant decrease in
AM hunts may therefore indicate either a preference, or need,
for larger packs to undertake ML hunts, which also coincidentally reduces their likelihood of encounter with humans.
Combining regressions from Figs 2 and 3, and the differences between activity pattern in Hwange and Nyamandlovu
6
AM = Time sympatry from civil twilight to sunrise
PM = Time sympatry from civil twilight to astronomical twilight
end
ML = Total time sympatric
Lions
AM = Time sympatry from civil twilight to sunrise
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
G. S. A. Rasmussen and D. W. Macdonald
Masking the zeitgeber to mitigate persecution
Figure 4 Data modelled from in Lycaon pictus in the Hwange and Nyamandlovu region Zimbabwe showing ratio of time allocations as a function
of total pack size.
PM = Time sympatry from civil twilight to astronomical twilight
end
ML = (Hwange = Time sympatry for 18% of ML activity;
Nyamandlovu = Time sympatry for 49% total ML activity)
Note well that these differences arise because Nyamandlovu dogs utilized days further from the full moon (Fig. 2) and
thus overlap more with lions.
These overlaps, shown in time sympatry (Fig. 5), demonstrate how by changing allocation of AM, PM and ML hunts,
Nyamandlovu dogs shifted their activities to reduce the probability of encounter with humans by 64%, but increase those
of encounters with hyaenas and lions by 70% and 37%, respectively. By introducing niche overlap factors, defined as the
time active when the interacting competitor was also active/
total activity time (Fig. 6), these changing dynamics further
highlight the consequence of switching to more nocturnal
activity, whereby encounters with humans decreases at the
cost of increased probability of hyaena encounters.
Discussion
This study of diel activity of Lycaon in relation to solar and
lunar events has not only revealed light as a limiting ecological
factor, but also demonstrates behavioural plasticity, and temporal activity that changes with pack size and anthropogenic
activity. It also highlights the importance of interpreting
events in the context of solar/lunar patterns rather than using
the arbitrary 24-hour clock. In theory, with the lunar month
not being synchronous with the solar month, only studies on
the equator where organisms respond exclusively to solar cues
and not lunar ones, are unlikely to fall foul of noise generated
using clock time. Even in latitudes as close to the equator as 5
degrees, the time differential over the year is 45 min. Furthermore, with some events being before twilight and some after,
the bias could be double this.
Previous Lycaon studies have not noted the utilization of the
moonlight niche (Mills, 1993; McNutt et al., 1997; Creel &
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
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Masking the zeitgeber to mitigate persecution
G. S. A. Rasmussen and D. W. Macdonald
Figure 5 Data modelled from the Hwange and Nyamandlovu region Zimbabwe showing the conspicuousness of Lycaon pictus to competing
predators and humans as a function of total pack size.
Figure 6 Niche overlaps (time conspecific active/Lycaon active) between Lycaon pictus, lions, hyaenas and humans in Hwange National Park and
Nyamandlovu farmland Zimbabwe.
8
Journal of Zoology •• (2011) ••–•• © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London
G. S. A. Rasmussen and D. W. Macdonald
Creel, 2002); however, this phenomenon is not exclusive to the
Hwange population. During the course of this study, this
behaviour was also opportunistically observed in the Lowveldt
region of south-east Zimbabwe, Mana pools and Kanyemba in
north-west Zimbabwe. Our results should be considered in the
light of four aspects of Lycaon biology: (1) larger packs are
more able to defend kills against hyaenas (Carbone, du Toit &
Gordon, 1997); (2) larger packs require more food, with larger
prey rather than an increased number of kills providing a more
economical option; (3) kudu, which form the most significant
part of Lycaon diet (Rasmussen et al., 2008), are nocturnal to
crepuscular and thus are more available in this time window,
and indeed in Rasmussen et al. 2008, it is also demonstrated
that larger packs select larger prey commensurate with pack
size; consequently with packs also commanding territories that
are parapatric in time (Rasmussen, 1997), intraspecific competition is deemed an unlikely cause for this finding; (4) due to low
light conditions, flight distances are smaller, and therefore, due
to the extreme cost of chasing (Rasmussen et al., 2008), this
time window is energetically more profitable. These points
apply equally to both the Hwange population and the Nyamandlovu one, between which we could detect no difference in
the hunting conditions. So as pack sizes in the Nyamandlovu
study were smaller, one would have expected less moonlight
activity, not more. The only observable difference between the
two areas lay in the extent of anthropogenic disturbance, so we
conclude that this explains the contrasting behaviour of the two
Lycaon populations.
We now turn to the potential costs of sub-optimization and
masking behaviours. Firstly, increased foraging time associated with moonlit hunts, which due to the hypercursorial
nature of this species, will represent appreciable energetic cost
(Rasmussen et al., 2008). Furthermore, with light being a limiting factor, the costs of this suboptimal strategy is likely to
reduce hunting success and cause even longer hunting hours
than the model predicts. Secondly, a twofold increase in the
probability of hyaena encounters will significantly increase
kleptoparasitic cost (Carbone et al., 1997). While it may be
hard to quantify the ‘cost’ of the behavioural adaptations,
either due to social deficit incurred by spreading out when
resting up (rather than sleeping in physical contact or close
proximity as they usually do) perhaps resulting in reduced pack
cohesion, or the lowered security for the pups, it is likely that
such costs exist. Equally, rich literature on human shift workers
demonstrates that diametric utilization of the diel cycle entails
severe costs in health and performance (Van Reeth, 1998), so
similar costs could affect the dogs. The accumulated impacts of
these factors on the Nyamandlovu population may be reflected
in the pack sizes AY and AYP being significantly less by 0.8 and
3.4, respectively. Nonetheless, in the short term at least, it
appears that the tactic has some success insofar as the population persisted and produced dispersers. One of which that had
originated from the source Hwange population, survived for 4
years, successfully dispersing a total of 570 km Hwange, Nyamandlovu, West Nicholson, Beitbridge, ending up in Messina
South Africa, where it was shot. This is to date the longest
distance a dog has been recorded to disperse, and perhaps
facilitated by masking the zeitgeber.
Masking the zeitgeber to mitigate persecution
In terms of likelihood of encounter, hyaenas represent a
greater threat to Lycaon than do lions, and it is unlikely that in
Nyamandlovu, Lycaon could switch diel activity so radically if
other predators were at the higher density typical of Hwange.
In that event, Lycaon would be trapped between an anthropogenic rock and a kleptoparasitic hard place. The latter is
particularly pertinent, for had the other predators been
present to the same degree, they too probably would have
become even become more nocturnal as documented for
hyaenas elsewhere (Boydston et al., 2003). Under these circumstances, it seems likely that niche overlaps would be even
higher than predicted by our model.
Turning to the significance of triggers that mask the zeitgeber, while behavioural plasticity is not unique, the few published field studies on temporal shifts suggest that the masking
behaviour represents a response to extreme risk rather than
gain. This study, and those of (Fenn & Macdonald, 1995) and
(Boydston et al., 2003) now add weight to the argument that
‘zeitgeber masking’ functions to ameliorate direct mortality
risk rather than accrue foraging gain. Furthermore, we argue
that the zeitgeber is only masked in extremis and this is also
supported by a study on spiny mice (Acomys cahirinus and
A. russatus), where (Kronfeld-Schor & Dayan, 2003) it was
proposed that while the rigidity of endogenous rhythmicity
ensures that species are not misled by minor environmental
disturbances, this may also be an evolutionary constraint.
Therefore, any signal that is capable of masking it might, by
inference, be of major survival significance. Consequently, we
suggest that the mechanism that masks the zeitgeber can be
thought of as an evolutionary ‘emergency exit’ which, if successful, might evolve into a mechanism of entrainment over
time.
Overall, these results highlight the value of understanding
not only temporal activity and interspecific interactions, but
also the role of the zeitgeber. Furthermore, insofar as there are
good reasons that circadian entrainment represents an adaptation of organisms to their environment, it should be recognized that when it is masked, the accrued energetic losses may
become the ‘last straw on the camels back’. Consequently,
when the zeitgebers ‘emergency exit’ is taken, it should sound
a warning of conservation risk.
Acknowledgements
We are grateful to the Director General of the Parks and
Wildlife Management Authority for permission to conduct
research and logistical support in Zimbabwe. To national
parks scout Felix Banda, Peter Blinston and Jealous Mpofu
for fieldwork; Greg Gibbard and Esther van der Meer for
assisting with data cleaning and almanac work, Paul Johnson;
Phil Riordon, Jorgelina Marino and to the referees for their
insightful comments.
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