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Male African elephants (Loxodonta
africana) queue when the stakes are
high
C.E. O'Connell-Rodwell
Rodwell
e
a b
c
d
, J.D. Wood , C. Kinzley , T.C.
f
g
, C. Alarcon , S.K. Wasser & R. Sapolsky
h
a
Center for Conservation Biology, Stanford University, Stanford,
CA, USA
b
Department of Otolaryngology, Head & Neck Surgery, Stanford
School of Medicine, Stanford, CA, USA
c
Department of Psychology, University of Washington, Seattle,
WA, USA
d
The Oakland Zoo, 9777 Golf Links Rd, Oakland, CA, USA
e
Department of Medicine, University of California, San Diego, La
Jolla, CA, USA
f
School of Veterinary Medicine, University of California, Davis,
CA, USA
g
Center for Conservation Biology, Department of Biology,
University of Washington, Seattle, WA, USA
h
Department of Biological Sciences, Stanford University,
Stanford, CA, USA
Available online: 06 Sep 2011
To cite this article: C.E. O'Connell-Rodwell, J.D. Wood, C. Kinzley, T.C. Rodwell , C. Alarcon, S.K.
Wasser & R. Sapolsky (2011): Male African elephants (Loxodonta africana) queue when the stakes
are high, Ethology Ecology & Evolution, DOI:10.1080/03949370.2011.598569
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Ethology Ecology & Evolution iFirst: 1–10, 2011
Male African elephants (Loxodonta africana) queue
when the stakes are high
C.E. O’CONNELL-RODWELL 1,2,9 , J.D. WOOD 3 , C. KINZLEY 4 ,
T.C. RODWELL 5 , C. ALARCON 6 , S.K. WASSER 7 and R. SAPOLSKY 8
Downloaded by [Caitlin O'Connell-Rodwell] at 14:34 06 September 2011
1
Center for Conservation Biology, Stanford University, Stanford, CA, USA
Department of Otolaryngology, Head & Neck Surgery, Stanford School of Medicine,
Stanford, CA, USA
3
Department of Psychology, University of Washington, Seattle, WA, USA
4
The Oakland Zoo, 9777 Golf Links Rd, Oakland, CA, USA
5
Department of Medicine, University of California, San Diego, La Jolla, CA, USA
6
School of Veterinary Medicine, University of California, Davis, CA, USA
7
Center for Conservation Biology, Department of Biology, University of Washington,
Seattle, WA, USA
8
Department of Biological Sciences, Stanford University, Stanford, CA, USA
2
Received 16 March 2011, accepted 14 June 2011
Linear dominance hierarchies are thought to form within groups of social animals to minimize conflict over access to resources. Dominance in both male and
female African elephants (Loxodonta africana) is based mostly on intrinsic factors
relating to age, and dominance hierarchies have been described within and between
family groups of females. Very little is reported about male elephant social structure
and dominance has only been described at the level of one-on-one contests. We test
the hypothesis that male African elephants form linear hierarchies when resources
are limited by monitoring a known group of elephants in Etosha National Park,
Namibia, and measuring dominance interactions between males (outside the context
of reproduction) during the dry season of 4 consecutive years. We show that males
form a stable linear dominance hierarchy under normal arid conditions (in 2005 and
2007) when water is limited and resource competition is high. In unusually wet years
with increased water availability (in 2006 and 2008), there is no linearity to the dominance hierarchy, less interaction between individuals and more agonistic behaviors
exhibited, particularly in lower ranking individuals. This is the first study to quantify
the existence of a linear dominance hierarchy in male African elephants as well as
the effect of climatic fluctuations on dominance from year to year.
KEY WORDS:
linear dominance hierarchies, African elephant, climate fluctuations.
9 Corresponding author: Caitlin E. O’Connell-Rodwell, Center for Conservation Biology, Stanford
University, Stanford, CA 94305, USA (E-mail: [email protected]).
ISSN 0394-9370 print/ISSN 1828-7131 online
© 2011 Dipartimento di Biologia Evoluzionistica dell’Università, Firenze, Italia
DOI: 10.1080/03949370.2011.598569
http://www.informaworld.com
2
C.E. O’Connell-Rodwell et al.
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INTRODUCTION
Linear (or transitive) dominance hierarchies are thought to form within groups
of social animals to minimize conflict in the context of resource competition (BROOM
2002). Within these hierarchies, affiliative interactions are used to strengthen bonds,
avoid conflict and to appease, whereas agonistic interactions are employed to defend
and maintain a dominance rank (SAPOLSKY 1993).
There are good long-term data describing the nature and dynamics of male dominance hierarchies in mixed-sex societies of baboons (NOE & SLUIJTER 1995), mountain
gorillas (ROBBINS 2001), chimpanzees (MITANI et al. 2000) and hyenas (EAST & HOFER
2001). Although there have been such studies on female elephants (ARCHIE et al.
2006; WITTEMYER & GETZ 2007), little is known about the dynamics of dominance
hierarchies in all-male elephant groups outside the context of reproduction (POOLE
1982; PAYNE 2003; LEE et al. 2011). Dominance in both male and female elephants is
based mostly on intrinsic factors relating to age (POOLE 1989a; ARCHIE et al. 2006;
HOLLISTER-SMITH et al. 2007; WITTEMYER & GETZ 2007) and extreme sexual dimorphism in this species is indicative of a polygamous mating strategy with intense malemale competition (POOLE 1989b). Yet dominance has only been reported at the level of
one-on-one contests in male elephants, particularly in relation to musth and access to
estrous females as a sporadic resource (POOLE 1982), without an overall assessment of
the dynamics of a hierarchical structure or extrinsic influences on that structure.
Male elephants are born into tightly bonded matriarchal social groups, but leave
the family upon reaching sexual maturity around 14 years of age (MOSS & POOLE
1983; LEE et al. 2011). As elephants are not considered territorial (DOUGLAS-HAMILTON
1972), both family groups and males that have left their families maintain large home
ranges where food resources are widely distributed (THOULESS 1996; LEGGETT 2006).
Spatial segregation in elephants has been found to be associated with resource availability, where dominant individuals (or families) occupy preferred areas (WITTEMYER
et al. 2007, 2008), and adult males spend much of their time in areas occupied almost
exclusively by males (LEE et al. 2011). Although dominant individuals have been noted
within populations of adult male African elephants (Loxodonta africana) (POOLE 1989b;
LEE et al. 2011), stable linear hierarchies have not been documented.
In a 4 year study focused on the dry season (2 of which were drier than average,
and 2 of which were wetter than average), we predicted that male African elephants
form linear dominance hierarchies during times when resources are especially limited in order to avoid possible risk of injury from competing for access to resources.
We tested our prediction within a group of known male elephants of known age classes
in the context of access to water. We define and quantify the nature and stability of a
linear dominance hierarchy for male elephants across changing climatic conditions in
the semi-desert environment of Etosha National Park, Namibia.
MATERIALS AND METHODS
Study site and field conditions
This study was conducted at a remote permanent waterhole in Etosha National Park,
Namibia, that is closed to tourism. All observations took place from an 8 m tower with a 360◦
view of the 1 × 1 km clearing surrounding the waterhole at the height of the dry season (June–
July) from 2005 through 2008. The year of observation was categorized as a “dry year” (2005 and
Male African elephants queue when the stakes are high
3
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2007) or “wet year” (2006 and 2008) based on the annual rainfall measured at the weather station
in Namutoni, the closest tourist center to Mushara, during the previous wet season (the wet season
occurring November to April, and the dry season from May to October).
As Etosha National Park has no rivers, access to drinking water during the “dry season” is
limited to permanent water holes in years with poor rainfall (dry years), but expands to include
ephemeral water sources in years with good rainfall (wet years). Local rain gauge information
was collected by park managers seasonally. Rainfall in 2006 marked a 30-year high, and the late
high rains in 2008 precipitated a 50-year flood of Etosha pan, creating many more access points
to quality drinking water within the region. The long-term average annual rainfall in Namutoni
is 436 mm (DE BEER et al. 2006). Average rainfall for dry years was 400 mm and for wet years
650 mm (Etosha National Park rain data archive, unpub. data).
Male elephant identification
All male elephants were identified based on individual differences in morphological characteristics such as ear tear patterns, tusk size and shape, tail hair shape, as well as overall size, color
and appearance. These differences are recorded in an ongoing photographic and morphological
identification database which has been compiled since 2004 and updated for any changes from
year to year.
Aging
Shoulder heights were measured on at least three separate occasions on 59 adult male elephants using a TrupulseTM 200 Laser Technology laser altimeter at a fixed distance (80 m) and
location (the source of fresh water) as well as shoulder position (perpendicular to the observation
tower). These data were compared for accuracy against a fixed object positioned at the same spot
with incremental measurements taped onto the object and visible from measurement distance.
Hind foot length measurements were also collected on 50 male individuals within the population.
As shoulder height (CROSE 1972) and hind foot length (WESTERN et al. 1983) correlate with age
(LEE & MOSS 1995), we placed bulls in broad age classes based on these measurements (1/4; 1/2; 3/4;
full), with 1/4 size being the youngest male and full size the oldest (Table 1). Shoulder heights were
measured on eight individuals in the 1/4 size class, nine in the 1/2 size class, 19 in the 3/4 size class
and 23 individuals in the full size class. The hind foot length measurements were collected on four
individuals in the 1/4 size class, six in the 1/2 size class, 14 in the 3/4 size class and 26 in the full size
class. All males included in the hierarchy study across years were placed within these age classes.
Table 1.
Average shoulder heights (n = 59) and hind foot lengths (n = 50) for male African elephants
corresponding with size categories and age range estimates.
Shoulder height mean (m)
Hind foot length mean (cm)
Size class
Estimated age
2.67
43.67
1/4
10–14.99 years
2.90
49.81
1/2
15–24.99 years
3.03
53.32
3/4
25–34.99 years
3.16
55.04
Full
≥ 35 years
4
C.E. O’Connell-Rodwell et al.
To control for age as a potential confounding factor, we ran a chi-square analysis to confirm that
an equivalent representation of age classes was included in the analysis in each year.
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Behavioral data collection
Behavioral data were collected from over 100 individually identifiable male elephants interacting at the waterhole from the time that the individuals entered the clearing of the waterhole
to the time that they left the clearing. The data were entered into a Noldus, The Observer® datalogger, using an ethogram developed for this study (Table 2). We recorded affiliative and agonistic
behaviors when at least two individuals were present at the waterhole. Behavior rates were generated from 104.08, 89.30, 65.40, 70.57 hr of observations from the 2005, 2006, 2007 and 2008 field
seasons respectively. We define affiliative behavior as soliciting proximity by approaching within a
body length with trunk held out, or actual active body contact of some kind, and agonistic behavior
as any form of aggressive act exhibited toward another individual.
Table 2.
Ethogram of affiliative and agonistic behaviors measured in this study. These particular behaviors represent a comprehensive suite of behaviors exhibited by male elephants at this location within the categories
of affiliative and agonistic. Musth behaviors as well as comfort and reproductive behaviors were also
measured but were not included in this study.
Affiliative behaviors
Backs into
One elephant gently backs into another in an effort to create body contact
Ear on face
One elephant puts its ear over the head/face of another
Ear on rear
One elephant puts its ear over the rear of another
Foot to body
One elephant touches another using its foot, most often seen with hind
foot reaching out
Gentle sparring
In head to head position, pushing back and forth, usually using tusks and
trunk, can be rough
Head to body
One elephant touches the body of another elephant with its head
Head to head
One elephant touches the head of another elephant with its head
Other body
One elephant touches the body of another with its body
Tail to body
One elephant touches the body of another (anywhere including head)
using its tail
Trunk to temporal
One elephant uses its trunk to touch the temporal gland of another
elephant
Trunk to body
One elephant uses its trunk to touch the body of another (not including
head and/or temporal gland)
Trunk to head
One elephant touches the head of another elephant with its trunk
Trunk to mouth
One elephant touches, then puts its trunk in the mouth and/or reaches its
trunk out to the mouth of another within one body length
Trunk wrap
Two elephants intertwine trunks
Lean
One elephant presses all or part of its body against another
Push
One elephant pushes another in an affiliative “herding” fashion usually as
they leave the waterhole
(Continued)
Male African elephants queue when the stakes are high
5
Table 2.
(Continued)
Rub
One elephant scratches/moves one body part (e.g. ear against rump) of
another
Agonistic behaviors
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Charge
One elephant rushes towards other, usually with head held up and ears
held out and may stop short of its target and “Trunk throw”, “Foot toss”,
or other; may be associated with a vocalization
Chase
Persistent, prolonged and aggressive follow, either at a walk or fast walk
Combat
Aggressive contact between two elephants; rushing towards one another
with trunks curled under to increase tusk contact, may lower head on
approach
Displacement
One elephant forces another to change its position and move away
possibly so initiator can occupy the position; displacement may occur
with body contact (shove, tusking, trunk slap) or without (within 1, 2, 3,
or 4 body lengths, or greater than 4 body lengths)
Aggressive ear flat
Aggressive threat moving both ears forward and back
Ears held out
Aggressive threat – both ears held in extended position often with “Head
held up”
Foot toss
Distant threat, either after mock “Charge”, “Head shake”, “Trunk toss” or
on its own. One front foot is tossed in the direction of the offending
elephant, kicking the air
Head held up
Head raised higher than shoulders, often with “Ears held out”
Head shake
Abrupt shaking of the head, causing ears to flap
Head thrust
Abrupt throwing of the head forward towards adversary
Lunge
Abrupt forward step with head thrust towards adversary
Open mouth
Holding mouth open, usually accompanied by “Head held up” and “Ears
held out”
Stand off
Two adversaries stand facing each other, possibly proceeding and/or
during combat
Trunk throw
Trunk swung out towards adversary
Back up
Stepping back while facing an adversary, may repeatedly step forward then
back
Ear fold
Bending ear just above midline, may be associated with “Ears held out”
and “Head held up”
Dominance hierarchy
A linear hierarchy was constructed based on the displacement of individuals by an aggressor. The first step taken in calculating the dominance hierarchy was to determine if the hierarchy
was linear. We implemented a script in Matlab that followed the methods described by DE VRIES
(1995) to test for linearity. This is a randomization test that was designed explicitly to handle
missing dominance interactions. The script ran through 10,000 iterations to generate the h (an
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6
C.E. O’Connell-Rodwell et al.
unbiased estimate of Landau’s h) and a P-value. If the P-value was not significant, no further
tests were run. If there was significance, the displacement matrix was then run through a ranking algorithm that is also designed to cope with unknown interactions in the displacement matrix
(WITTEMYER & GETZ 2006). Total possible interactions were the total number of dyadic interactions possible for the number of bulls present in that year. Unknown interactions were the number
of dyads that were not observed. Because it is difficult to rank individuals with few displacement
interactions (either as the winner or loser), bull elephants with less than ∼ 5 displacement interactions were excluded from the matrix, which resulted in ∼ 60% of the interactions being unknown
for dry years. For those linearity tests that were not significant (in wet years), we decreased the
percent unknown to 29% by excluding more bulls with the fewest displacement interactions and
ran the linearity test again. This was done to ensure that the lack of significance was not due to a
lack of power because of fewer males visiting the waterhole in wet years (Table 3).
Since rank can temporarily rise when males are in musth, a heightened aggressive and
sexually active state (POOLE & MOSS 1981), we noted periods of musth and analyzed fecal testosterone levels (WASSER et al. 2000) to confirm that this confounding state did not impact the
hierarchy during observation periods. Musth was associated with testosterone levels > 300 ng/g
in this population, along with diagnostic behaviors described elsewhere (GAINSWINDT et al. 2005).
To determine whether musth had an influence on rank during years with linear dominance
hierarchies, we ran a regression between rank and testosterone levels.
Aggression/affiliation rates
Individual aggressive and affiliative events were recorded using Noldus Observer software.
These events were then summed for each individual and divided by the total number of hours
of observation for that individual during that year (field season), giving us a measure of number
of aggressive/affiliative events per elephant per year. For these statistical tests, we reduced our
analysis to a core group of 12 bull elephants that were present at the water hole in all 4 years.
We ran a repeated measure GLM to test whether aggressive or affiliative rates varied across years,
with bull as a random variable.
Table 3.
Linear dominance hierarchy scores for male elephant interactions in dry (2005 and 2007) and wet years
(2006 and 2008). h is an unbiased estimate of Lanudau’s index h which measures the degree of hierarchy
linearity, with 1 being perfectly linear. Significance was calculated with the de Vries linearity test run
through 10,000 iterations (DE VRIES 1995). Total possible interactions are the total number of dyadic
interactions possible for the number of bulls present in that year. Unknown interactions are the number
of dyads that were not observed. For those years when the test was not significant, the test was re-run
with fewer bulls to decrease the percent unknown dyadic relationships and thus determine whether lack
of significance was due to low power. Those results are given in parentheses.
Year
Landau’s h
P-value
Bulls in
matrix (n)
Total dyadic
relationships possible
% Unknown dyadic
relationships
2005
0.25
0.0001
30
435
61%
2006
0.34 (0.66)
0.0976 (0.0764)
14 (8)
91 (36)
59% (29%)
2007
0.30
0.0204
20
190
61%
2008
0.29 (0.54)
0.3295 (0.3210)
12 (7)
66 (21)
59% (29%)
Male African elephants queue when the stakes are high
7
Aggression over access to water (displacements)
To test whether there was a difference in aggression over water in dry years, we calculated
all the displacements (over access to water) for each year. This was then divided by the number
of hours of observation in that year for each bull. The data were log transformed to meet the
assumption of the test. A repeated measures GLM was run on the data to test whether there was a
difference in aggression over water (displacement) across years.
50
45
40
35
30
25
20
15
10
5
0
Aggression
Affiliation
Rainfall
2005
2006
2007
2008
800
700
600
500
400
300
200
100
0
Rainfall (mm)
Mean shoulder heights were 2.67 ± 0.19 m; 2.90 ± 0.11 m; 3.03 ± 0.12 m; and
3.16 ± 0.10 m for 1/4, 1/2, 3/4 and full sized males respectively. The mean hind foot length
was 43.67 ± 2.28 cm; 49.81 ± 3.28 cm; 52.32 ± 3.16 cm; and 55.04 ± 2.45 cm for 1/4–
full size classes respectively. A one-way analysis of variance (ANOVA) was performed
on both shoulder height (F3,55 = 33.51, P = 0.0001) and hind foot length (F3,46 = 22.81,
P = 0001), showing significant differences between size classes. Pair-wise comparisons
were performed using a Tukey 95% simultaneous confidence interval test on all size
classes for both shoulder height and hind foot length; the only one that was not significant was between the 3/4 and 1/2 size classes (P = 0.0597; P = 0.0502 respectively).
Shoulder height and hind foot length results (Table 1) reflect those of two recent studies on aging, although the bulls in our population appear slightly taller per age class
(MOSS 2001; SHRADER et al. 2006). Each male included within the hierarchy analysis
fell within these age class differentiations, and age class compositions between years
were not significantly different (χ 2 = 2.326; df = 6; P = 0.887).
Aggression rates were significantly higher in wet years compared to dry years
(GLM: F3,24 = 6.33; P = 0.003) while affiliation rates did not differ across the 4 years
(GLM: F3,24 = 1.58; P = 0.221) (Fig. 1). The increased rate of agonistic behaviors in wet
years was predominantly exhibited in subordinates (Fig. 2). There was no relationship
between rank and fecal testosterone levels during years with linear dominance hierarchies (in 2005, testosterone vs rank R2 = 9.6%, P = 0.326; in 2007, R2 = 1.3%, P = 0.722
(see WASSER et al. 2000 for radioimmunoassay analysis methods)).
Behavioral events / hour
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RESULTS
Fig. 1. — Rates of agonistic and affiliative interactions between male elephants during the dry seasons
of 2005 to 2008 (rates generated from 104.08, 89.30, 65.40, 70.57 hr of observations respectively, entered
into a Noldus, The Observer® datalogger using an ethogram developed for this study). Error bars are
95% CI. Rates of agonistic behavior in the wet years of 2006 and 2008 were significantly higher than
rates in the dry years of 2005 and 2007 (F3,24 = 6.33; P = 0.003). There was no significant difference in
affiliation rates across all years (F3,24 = 1.58; P = 0.221).
8
C.E. O’Connell-Rodwell et al.
affiliative Behavior index aggressive
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Climatic impacts on behavior
1.00
0.80
0.60
0.40
0.20
0.00
–0.20
–0.40
–0.60
Dry years (2005 & 2007)
–0.80
Wet years (2006 & 2008)
–1.00
1
3
high
5
7
Rank
9
11
low
Fig. 2. — Regression lines for dry and wet years showing that changes in aggression are mostly being
driven by subordinate bulls (dry: R2 = 20.3%, P = 0.027; Wet: R2 = 3.2%, P = 0.525). The behavioral
index is calculated with the following formula: (Aggressive events − Affiliative events ) / (Affiliative events
+ Aggressive events). A negative number indicates that an individual was more affiliative than aggressive
in terms of number of events. A positive number indicates an animal that is more aggressive. A value of
1 indicates that only aggressive events were recorded for that individual.
A stable linear dominance hierarchy formed in the dry years of 2005 and 2007,
whereas in the wet years of 2006 and 2008 there was no linearity to displacements
events within the hierarchy (Table 3). This relationship held for wet years with fewer
individuals even when we decreased the percentage of unknown interactions (by
decreasing the number of bulls in the matrix) to increase the power of the test (see
Table 3 numbers in parentheses).
DISCUSSION
Strategies differ as to how hierarchies are formed and maintained as well as the
nature of their stability (BROOM 2002). Dominance in male elephants is thought to be
based mostly on intrinsic factors relating to age (POOLE 1989b). As the males within our
hierarchy study were of equivalent age across years, we expect that dominance would
be relatively stable from year to year, but that environmental factors could eliminate the
pressure for strict linearity within the dominance hierarchy in years with little resource
competition.
We document that male elephants form linear dominance hierarchies under arid
conditions, a phenomenon most likely selected to minimize conflict over access to water
as well as to reduce stress in the population. High ranking individuals remained relatively stable from year to year with little change in behavior. The increase in aggression
seen in subordinates (who tended to be younger) in wet years when no hierarchy was
observed was independent of musth status, and suggests that interaction within a linear
hierarchy might moderate aggression in younger individuals, highlighting the potential benefit of structure that a hierarchy may provide for younger males. This seems
Male African elephants queue when the stakes are high
9
particularly apparent as younger males are highly social and appear to choose the
company of elders, suggesting the importance of mature males in society (SLOTOW
et al. 2000; EVANS & HARRIS 2008), a pattern that has implications for other healthy
male societies including humans.
ACKNOWLEDGEMENTS
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Work was supported by Stanford University faculty and student VPUE grants, Utopia
Scientific, the Oakland Zoo, the Scheide Fund, and facilitated by the Namibian Ministry of
Environment and Tourism and Noldus Software Company, Leesburg, VA.
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