The elephant has the largest brain of any terrestrial mammal [1]. Since species with large brains are generally reputed to possess considerable mental development [2,3], it is likely that the brain of elephants with its large olfactory lobe, hypothalamus and cerebral cortex [4,5], possesses the hardware necessary for complex cognitive functions-including sophisticated communication, social knowledge [6], social networking or “eavesdropping” [7-12] and the development of cultures, all of which influence “intelligence” [13]. A detailed study of visual communication in particular, could further elucidate their social relations and accompanying mental attributes.
It has been widely believed that human language has an over powering influence on cognitive [14-17]. As a result, many studies have either focused on assessing whether species can learn to use an artificial human-type, context-independent language [18-22]. Anderson [23], or testing if these species have human mental characteristics such as manipulating and deceiving [6].
Communication in elephants, like that of almost all behaviours of mammals, is flexible and adaptable [24,25]. The specific meaning of the message conveyed by a particular behaviour may be independent of the context in which it occurs, that is “context independent”, similar to much of human language. But it may be “context dependent”, where the meaning conveys the state of arousal of the communicant, but the detailed meaning is read from the context [26,27].
Another feature of elephant’s communication is that it often multi-sensory. A summary of how the different senses are used in communication follows.
Vocal communication has received most attention in a range of species including elephants (e.g. birds, whales, see forthcoming review on audition in mammals). Their auditory sensitivity ranges from infra sound to higher frequencies than humans [28]. Their vocalisations have been studied since the 1960’s [24,25, 27,29,30-32] and a number of studies have focused on the use of ultra-sound by elephants to communicate over several kilometers [33-37] identification of individuals by their vocalizations [33,38,39] and communication by sensitivity to seismic movements has also been demonstrated [40-42].
Olfactory and gustatory communication are often linked but have received less attention in elephants, although they have a very large olfactory sensitive area in the trunk, taste buds on the tongue and around the mouth, and a relatively large olfactory bulb in the brain [1,6,43], mentions that they receive and analyze a great deal of olfactory information which is important to them. The vomeronasal organ attached to the base of the brain is considered to be for the careful investigation of strong, pertinent or unfamiliar smells [44]. It is uniquely large in the elephant and has paired palatal ducts, a folded epithelium and a dorso-medial position of the neuro-epithelium indicating its complexity and links to the cerebral cortex [45], and elephants perform flehmen which is associated with the vomeronasal gland [46]. They have cutaneous glands around the temple and inter-digital glands that produce steroids as well as other secretions and have been found to secrete pheromones related to sexual status. Olfactory research has concentrated on sexual pheromones [45,47-50], but elephants have sweat glands well distributed over the body [51,52], which may produce individual smells. The multi-sensory trunk acts as a hand, a nose and a mouth thus multi-sensory information is inevitably acquired. Taste plays a major role in the choice of diets of course, and frequent tasting another (see below), is likely to be important in communication, but has been little investigated to date.
Some tactile communication has been studied with the salience of the trunk demonstrated [53-55]. Elephants are capable of extraordinarily complex manipulations with the trunk; within the blind area (see below), by touching and presumably smelling, they can sort beans that they wish to eat from those that they do not (personal video), or find rings in piles of hay with their trunks (Circus Knie). Communication by touching different parts of each other’s bodies also are important [53], but such movements also always have visual communicative cue.
Visual Communication has not been very carefully investigated in detail, although explicit trunk movements have been recorded. The first step is to study what they can see. First, they have dichromatic vision, like some colour blind humans [56], but further research is required. Due to the position of the eyes on either side of the large head, elephants have two large simultaneously observed monocular visual fields which enable him/her to acquire visual cues from a large area (300°). But they have a relatively small binocular visual field, approximately 25-60°, compared to the 100-120° of humans. The breadth of the head with the trunk protruding directly in front of the laterally placed eyes ensures that s/he has a blind spot of approximately 2m directly in front of the head [57,58]. Both the placing of the eyes, and the two simultaneous monocular visual field, presents a different visual appreciation of the world from humans’ relatively small monocular, but large binocular visual field.
It has been maintained that elephants have poor vision [51,59,60], although visual signals, such as some trunk movements [24,25,60,61] and head, tail and ear movements [24-26,29,57], have been described. Some visual displays associated with must [62] and female reproduction has also been described although these visual cues may have a biochemical foundation [63].
It is well known that elephant as well as other domestic animals react to slight visual cues indicating intentions that are emotional states. They also show an ability to imitate others [58,64], indicating perhaps emotional contagion [65,66]. These abilities have been used for centuries [67], by their handlers. Thus, such critically assessed information or “folk knowledge” must be part of any good scientific investigations, if we wish to progress in our understanding [68-71], rather than just “discovering” what is already known.
One of the objects of this paper is to report the explicit behaviours in communication (the behaviours whose meanings are clear) and to investigate the responses they cause. The implicit behaviours which have often been ignored in scientific reports, (although their meaning is often known by those who deal with elephants) have also been recorded. First, both the explicit and the implicit behaviours must be defined, their meanings critically evaluated and their involvement with other senses recognized.
Studies of explicit behaviours related to competition between individuals and this often comes with a commitment to outlining a “dominance hierarchies” [72-74]. The inclusion of both afflictive and implicit behaviours in communication might suggest different interpretations of elephant’s social contract.
Non vocal signals are unlike vocalization in their communicative value because vocalizations are only made to communicate [29]. But, visual, olfactory, taste and tactile messages may have other functions and be performed without intent to communicate, even though a message concerning their emotional state may be transferred to others watching. For example when one elephant sees another putting his trunk out to smell a strange object, he receives the message that “there is something interesting there”, even though the behavior was probably performed from curiosity, rather than with intent to communicate. Thus, the communicative meaning of many messages can be complex.
For many movements and vocalizations, the meaning may act as an analogue system indicating the general level of arousal of the animal so the same behavior may occur in a variety of contexts [26,27,75]. The behavior itself does not convey why s/he is in this state. For example, the elephant shakes his/her head when s/he (i) has an irritation on the head, (ii) is scared, (iii) about to attack, (iv) excited, (v) anticipating something (vi) cannot obtain a desire goal. In essence, the animal indicates that it is aroused, but “uncertain” what to do next. This has been demonstrated for many vocalisations, including the elephant rumble [27], head and tail movements in ungulates, elephants and carnivores [26,29,30]. The cause of the arousal can be traced to frustration or approach avoidance conflict [26,30,54,76-80].
Whether the individual is interested, aggressive, and friendly or is experiencing other emotions such as curiosity, fear or embarrassment [81], will be read from the context. Thus, a better understanding of visual signals and the consequent mental aptitudes could further illuminate the elephants’ social contract.
Undeniably, such a study is difficult. It requires experienced observers who attend to details, are inter-observer reliable, familiar with the species and can recognize individuals. Different combinations of behaviours may be performed simultaneously so some behaviour may be missed. Although not all the olfactory messages, seismic vibrations or infra-sounds can be perceived by the human observer without special equipment, if information has been transferred it is likely that there will be some visual cues.
To date, there has been no quantitative analysis of the meaning of many of the visual messages conveyed by elephants, and the importance of their trunk for manipulation and multi-sensory communication needs further study although see Kiley-Worthington and Plotnick et al., [61,82]. As Langbauer et al., mention “more work needs to be done to elucidate the specific role of many signals”.
A total of 2410 interactions between the 6 elephants were observed over 213 hours, (that is 1278 elephant hours). This represents 1.89 interactions/elephant/hour.
The analysis of the meaning of the messages were restricted to the 22 most frequent behaviours, selected on the total number of times performed regardless if by an initiator or a recipient. These behaviours accounted for 73% of the recorded behaviours. Table 2 lists them and their frequencies.
The use of the different sensory modalities in the interactions
The frequency of the use of the different sensory modalities is shown in table 3, followed by further details for each sensory modality.
|
Sensory Modality
|
Number of Different Behaviours
|
Frequency
|
% of Total (7542) Different Behaviours Observed
|
|
Visual only, as far as could be assessed
|
36
|
4307
|
58%
|
|
Visual, tactile/gustatory and olfactory
|
29
|
1314
|
18%
|
|
Visual & olfactory
|
7
|
1553
|
21%
|
|
Auditory - vocal
Auditory - non vocal
|
3
2
Total=77
|
37
111
Total=7344
|
0.5%
1.5%
Total=99%
|
|
Other behaviours whose sensory modality was not clear
|
27
|
143
|
1%
|
Table 3: The frequency of the use of the different sensory modalities.
Olfactory communication
The visual evidence of smelling included frequent movements of the trunk searching and investigating strange or interesting smells and possibly tastes 39% of all of the behaviours recorded in this study had an olfactory component: (18% visual, tactile, gustatory and olfactory, and 21% visual and olfactory). There may have been other olfactory messages without visual cues which the observers could not pick up.
Gustatory communication
It was not possible to completely separate taste from olfactory or tactile cues, but, there was a taste component in 18% of the interactive behaviours (Table 3).
Tactile communication
Tactile and gustatory cues could not be separated visually either as when touching, the trunk may also be tasting and smelling. The elephants also touched each other with other parts of the body. There was a tactile component in 18% of all the behaviours performed
Auditory communication
This was used very little in this group (0.5% of observations). It is possible that during the study, the elephants were using infra sound or seismic vibrations, but, visual signs would be likely to have been seen.
There are also a variety of non-vocal noises made by elephants without the larynx. These include blows, sighing, sniffing and puffs, stamping, breaking sticks and so on. Blow and puff accounted for 1% of the behaviours used in social interactions. Environmental noises made by individuals were not recorded.
Visual communication
There was a visual component in 97% of the behaviours recorded (Table 3: 58%+21%+18%). Even though other sensory cues were sometimes attached, over half (58%) had only visual cues as far as we could ascertain.
The use of the trunk
Sixteen different trunk movements were distinguished that were not related to feeding, although some of these were relatively rare (Table 4). These trunk movements accounted for 18.1% of all the interactive behaviours.
|
Trunk Movement
|
No. Times Exhibited by Performer, P
|
No. Times Exhibited by Recipient, R
|
Total Number of Times Exhibited, P+R
|
% of 7542 Behaviours
|
|
Swing trunk
|
182
|
108
|
290
|
3.9
|
|
Trunk up
|
103
|
78
|
181
|
2.4
|
|
Trunk to another’s mouth
|
121
|
54
|
175
|
2.3
|
|
Trunk extend to another
|
74
|
47
|
121
|
1.6
|
|
Trunk to vulva
|
72
|
15
|
87
|
1.2
|
|
Trunk to penis of other
|
56
|
29
|
85
|
1.1
|
|
Entwine trunks
|
37
|
41
|
78
|
1.0
|
|
Trunk to body of other
|
52
|
12
|
64
|
0.9
|
|
Trunk to face of other
|
34
|
29
|
63
|
0.8
|
|
Trunk to anus of other
|
17
|
43
|
60
|
0.8
|
|
Trunk to head/shoulder of other
|
35
|
23
|
58
|
0.7
|
|
Trunk to tail of other
|
36
|
6
|
42
|
0.5
|
|
Trunk to own mouth
|
19
|
19
|
38
|
0.5
|
|
Trunk to rear of another
|
12
|
1
|
13
|
0.2
|
|
Trunk down
|
4
|
4
|
8
|
0.1
|
|
Trunk to neck of other
|
7
|
1
|
8
|
0.1
|
|
Total
|
861
|
510
|
1371
|
18.1%
|
Table 4: The Use of the Trunk in communication. The different movements, their frequencies and the percentage of all the behaviours recorded.
Further discussion on the use of the trunk is below.
Analysis of the meanings of different behaviours
When studying communication, as a rule, only behaviours with an explicit message are recorded, such as aggressive (e.g. fighting with the tusks, barging and tusking another, trunk pushing) and withdrawal and avoiding. Affinitive behaviour such as touching or rubbing another, are explicit, but have less frequently been recorded. Showing interest in another is explicit, but has rarely been recorded. There are much other behaviour used in interactions which have an “implicit” or hidden meaning which we will unravel. Meanings can be accessed from an analysis of the recipient’s responses, but this is not always clear, as the responses vary. Nevertheless, it can be the first step. Table 5 shows the three most common responses to the 22 most frequently performed behaviours.
|
Behaviour Performed
|
Number of Times Recorded
|
Number of Different Types of Responses
|
Most Common Response
|
Second Most Common Response
|
Third Most Common Response
|
|
Approach/contact make
|
690
|
76
|
Ignore310
|
Contact break106.
|
Tail wag69
|
|
Tail wag
|
359
|
68
|
Ignore73
|
Tail wag 66**
|
Contact31
|
|
Contact activity (walk, stand or lie)
|
339
|
56
|
Ignore137
|
Contact 117**
|
Tail wag49
|
|
Flap ears
|
335
|
59
|
Ignore73
|
Flap ears 66**
|
Tail wag54
|
|
Contact break (general)
|
80
|
39
|
Ignore 60
|
Tail wag11
|
Follow7
|
|
Swing trunk
|
217
|
50
|
Ignore88
|
Tail wag34
|
Swing Trunk 29**.
|
|
Turn body towards
|
161
|
52
|
Ignore 40
|
Tail wag27
|
Flap ears18
|
|
Tusk - to- tusk
|
198
|
35
|
Tusk-to-tusk 84**
|
Entwine trunks18
|
Ignore10
|
|
Trunk up
|
169
|
57
|
Ignore29
|
Trunk up 14**
|
Tail wag11
|
|
Trunk to own mouth
|
141
|
44
|
Ignore41
|
Contact break20
|
Trunk to own mouth 13**
|
|
Trunk extend
|
104
|
40
|
Ignore19
|
Flap ears12
|
Tail wag12
|
|
Entwine trunks
|
79
|
21
|
Entwine trunks 28**
|
Tusk-to-tusk17
|
Contact break4
|
|
Tusk to body
|
55
|
37
|
Contact break24
|
Ignore14
|
Leap away13
|
|
Both ears back
|
45
|
28
|
Tail wag6
|
Flap ears4
|
Contact break 3
|
|
Head nod
|
56
|
26
|
Ignore 17
|
Tail wag10
|
Head nod 8**
|
|
Ears pricked
|
58
|
25
|
Ignore 14
|
Prick ears 8**
|
Tail wag8
|
|
Blow
|
74
|
35
|
Tail wag8
|
Flap ears5
|
Trunk to mouth5
|
|
Tail up
|
59
|
26
|
Ignore 28
|
Tail wag 5
|
Ears back 4
|
|
TOTAL number
Responses in category.
|
3467
|
826
|
1051
|
554
|
348
|
Table 5: The number of times each of the 22 most common behaviours were performed, the number of different behaviours elicited, and the 3 most common responses.
Note: Bold=Behavior ignored by recipient. Dyadic movements by definition, excluded from analysis. Italic: Are reciprocal **=t test significant at P<0.01
Approach, the most commonly exhibited behavior (690 times), caused 76 different behavioural responses (Table 5). All the behaviours had a number of different responses (column 3).
The implicit behaviour, tail wagging or swishing, was the second most common response. It was often performed with other behaviours (33.2%). See below for discussion.
Ignore as a response
Curiously, the most common response was to ignore the directed behavior, defined as “no observable change of behaviour exhibited by the recipient within one minute of the performer’s directed behaviour” (see Table 1). All the behaviours that were not of their nature dyadic (e.g. tusk to tusk, trunk entwine) were ignored at some point, a total of 712 times (20.5%). Table 6 shows the most and least commonly ignored behaviours.
|
Performed Behaviour
|
Number of Times Ignored
|
Total Number of Times this Behaviour is Performed
|
Percentage Each Behaviour is Ignored
|
|
Most often ignored (more than 20% of occasions performed)
|
|
Contact break (general)
|
310
|
677
|
60%
|
|
Follow
|
73
|
220
|
50.3%
|
|
Approach/contact make
|
137
|
335
|
45.8%
|
|
Head nod
|
73
|
210
|
43.6%
|
|
Contact activity (walk, stand or lie)
|
102
|
150
|
40.9%
|
|
Flap ears
|
88
|
182
|
37.6%
|
|
Ears pricked
|
40
|
111
|
36.8%
|
|
Turn body towards
|
10
|
103
|
36%
|
|
Swing trunk
|
29
|
103
|
35.7%
|
|
Turn head towards
|
23
|
121
|
34.7%
|
|
Tail wag
|
73
|
145
|
33.2%
|
|
Head shake
|
26
|
75
|
32.8%
|
|
Tail up
|
8
|
27
|
29.6%
|
|
Trunk up
|
19
|
74
|
28.2%
|
|
Trunk extend
|
20
|
61
|
25.7%
|
|
Least commonly ignored (less than 20% of occasions when performed)
|
|
Trunk to own mouth
|
14
|
77
|
19%
|
|
Tusk to body of other
|
3
|
23
|
18%
|
|
Blow
|
4
|
37
|
16.7%
|
|
Both ears back
|
17
|
39
|
13%
|
Table 6: The most and least commonly ‘ignored’ of the 22 most frequent behaviours.
The less ignored behaviours are likely to be those with the strongest messages. These include: (i) putting the trunk into his own mouth. (ii) Tusking another’s body, which caused a leap away, but could also be ignored? The least ignored of all were “blow” and “both the ears back”. The most common responses to both were tail wagging, and/or putting the trunk in his own mouth (Table 5).
Why so many behaviours are frequently ignored is discussed below.
Do as done by, imitation or reciprocity (Table 5 italic)
Many responses were reciprocated significantly more than expected (Table 5 in italic). In fact, reciprocal/imitative behaviours were one of the three most frequent responses for 7 of the 19 most common behaviours (Table 5 and details Table 7). All except for “blow” and “tusk to body of the other” were significantly reciprocated (Chi
2, P<0.01).
|
Performed Behaviour
|
Total Times Elicited by Performer, Frequency
|
Same Behaviour Elicited by Recipient, Frequency
|
Same Behaviour Elicited by Recipient, %
|
Value of Chi2
|
P Value
|
|
Contact activity
(walk, stand or lie)
|
335
|
117
|
34.9
|
13.96
|
0.001
|
|
Flap ears
|
210
|
66
|
31.4
|
31.08
|
0.001
|
|
Tail wag
|
220
|
66
|
30.0
|
29.87
|
0.001
|
|
Ears pricked
|
38
|
14
|
21.1
|
16.02
|
0.001
|
|
Head nod
|
56
|
8
|
20.5
|
9.03
|
0.001
|
|
Swing trunk
|
182
|
29
|
15.9
|
15.16
|
0.001
|
|
Head shake
|
92
|
8
|
8.7
|
6.61
|
0.025
|
|
Trunk up
|
169
|
14
|
8.3
|
8.46
|
0.005
|
|
Tail up
|
27
|
3
|
11.1
|
22.45
|
0.001
|
|
Trunk to mouth
|
121
|
13
|
10.7
|
10.33
|
0.001
|
|
Both ears back
|
23
|
2
|
8.7
|
11.08
|
0.005
|
|
Blow
|
30
|
2
|
6.7
|
1.69
|
NS
|
|
Turn head towards
|
75
|
3
|
4.0
|
5.01
|
0.025
|
|
Contact break (general)
|
150
|
5
|
3.3
|
5.82
|
0.025
|
|
Tusk to body
|
77
|
2
|
2.6
|
1.09
|
NS
|
|
Approach/contact make
|
677
|
17
|
2.5
|
9.92
|
0.001
|
|
|
|
|
|
|
|
Table 7: “Do-as-done-by”, reciprocity or imitation by responder.
Why reciprocity is so common is discussed below.
Batching the behaviours according to their meaning
The meaning of explicit behaviours is evident. Here they are batched into 3 categories, 1) those related to aggression and avoidance, 2) affiliation and 3) showing interest in the other.
Much implicit behaviour are originally related to skin irritation, such as tail wagging, head nodding or shaking, scratching, and ear flicking (further discussion below). These behaviours were frequent, but their meaning in social interactions is not obvious. These results indicate that these behaviours show some arousal because of indecision/ uncertainty of what to do (approach or avoid: frustrated). Therefore, they are placed in the 4th category labeled “uncertain” or indecision. Category 5 is behaviours that occurred too in frequently to analyze.
To summarize, the batched categories are:-
Socially positive behaviours
Interest/Attention that is turning the attention to the other and affiliative behaviours. Socially positive behaviours foster group cohesion: “sticking” together. (a) Affiliation, friendly behavior (24.27%), significantly higher than expected (Chi2, P<0.01), and (b) interest (22.94%). These 2 categories accounts for 47.66% of all the behaviours recorded, almost half.
Socially negative behaviours
Aggression and also avoid and withdraw-Socially negative behaviours relate to unpleasantness to another, its avoidance or prediction (such as avoiding and withdrawing). Socially negative behavior promotes group division or “splitting”. Socially negative behaviours accounted for 18.4%, significantly less than expected (Chi2 p<0.05).
Uncertainty or indecision
These are frequently performed behaviours that often occur during frustration or approach-avoidance conflict which indicates some arousal, usually caused by indecision. Interestingly, this category was the most common: 29.27%, significantly more than expected (Chi2, P<0.01).
Unclassified behaviours
The communicative meaning of these behaviours remains unknown due to their infrequent performance.
The behaviors in each category are listed in table 8. Table 9 shows the frequency that the different categories were recorded in the interactions.
|
Interest
|
Affiliation
|
Aggression and Avoidance
|
Uncertainty
|
Unclassified
|
|
Approach
Ears forward pricked
Ears back
Look at
Trunk extend to
Tail up
Puff
Turn body towards
Turn head towards
Walk faster
Trot
Circle another
Trunk up
Smell other from a distance
|
Rest head/neck on other
Rumble
Contact make
Contact walk
Contact stand
Stand over
Follow
Grab others tail
Mount with or without erection
Rub against another
Rub head against other,
Smell & touch other
Smell penis or vulva,
Touch anus, penis, vulva, face, body, neck, nose, shoulder, tail
Nibble head, body
Playing
Entwine trunks
Trunk to others mouth
|
Barge into other
Push another’s body or tum
Tusk to head, rear or body of the other
Tusk to tusk
Throw trunk at, or smack with trunk
|
Ears Flap
Head nod
Head throw
Head shake
Chew
Tail wag & swish Blow
Paw & Stamp
Raise leg
Swing leg
Trunk to own mouth
Swing own trunk
|
Rest leg
Lie down
Urinate
Defeacate
Graze
Dust throw
Walk
Pull tree & eat leaves.
|
Table 8: The behaviours batched in the five different categories relating to their meaning.
|
Batched Behaviour
|
Total Performed
P
|
% Total Performed
|
Total Recipient Responses RR
(excluding ignore)
|
% of Recipient Responses Recorded
|
Total
% of
P+RR
P+RR
|
|
Affiliative
|
1569
|
30.51**
|
1018
|
21.47
|
2587
|
24.27
|
|
Interest
|
1341
|
26.77
|
1104
|
21.24
|
2445
|
22.94
|
|
Uncertainty
|
1301
|
25.3
|
1818**
|
34.98
|
3119
|
29.27**
|
|
Aggression
|
808
|
15.1
|
368 -*
|
0.7
|
1176
|
11.2
|
|
Avoid
|
123*
|
2.3
|
648
|
1.24
|
771
|
7.2
|
|
Unclassified
|
403
|
7.26
|
136
|
0.26
|
539
|
5.03
|
|
TOTAL
|
5545
|
100
|
5092
|
100
|
10,637
|
99.91
|
Table 9: The frequency of each behavior in the 5 categories either performed by the initiator or as a response.
Note: *=significant at p>0.05; **=significant at p>0.01
Comparative Sociality in mammals measured from the frequency of their interactions
A comparative measure of the “sociability”, that is the frequency that a species communicates with its co specifics, has been neglected. This can be represented as the number of interactions per animal per hour observed. There were 1.89 interactions/elephant/hour, which is more than in horses: 1.01/horse/hour when the data was recorded and analyzed in the same way [85]. Whether other elephants are such frequent conversationalist, remains to be explored.
Protective responses
In many canids, felids and ungulates, the origin of some behaviours such as pulling the ears back, appears to be related to protection. This can be ritualized and become a signal indicating defensive threat. Ear withdrawal is particularly obvious and ritualized in species without horns such as canids, felids, equids and camelids. Here, the ears are drawn back and the orifices rotated towards the head [29]. The large aural orifices of elephants are not possible to protect in this way, but the ears themselves can be pulled back and flattened against the side of the head which may protect them from being torn in dangerous situations. Forty five different behaviours were elicited when an initiator put both his/her ears back, and it was often reciprocated (see Table 5) and accompanied by tail wagging, indicating uncertainty. The third most frequent response to ears back was to withdraw. The meaning of ear flattening is suggested below.
The use of the different sensory modalities in communication
The most frequent behaviours recorded in interactions were visual (97%). However many visual cues have inherent tactile, olfactory or gustatory involvement. This is the case for any trunk movements which inevitably involve the possibility of smell (and sometimes touch and taste) as well as visual positional messages. Olfactory and tactile communication is important in elephant communication, but they generally have a visual component and consequently also display a visual message. Vocal messages, audible to the human ear, or with visual indicators (for example trunk vibrations), were relatively rare in this group, although it is possible that seismic or infrasound messages were not picked up.
Olfactory communication
Although research attention has been placed on the production of pheromones from particular glands (see introduction) most of elephant’s olfaction may be to acquire diverse environmental and/or social information. With their well developed olfactory organs and areas for its analysis in the brain information can probably be gathered from the wind, changes in air humidity, smells of vegetation such as rising sap, potential fruiting or flowering and the recognition of individual plants, buds and leaves.
Information could be acquired in this way about both the past and the future from smells of seasonal changes. For example, Namibian elephants trek around 150km across the desert to baobab trees when they are fruiting, so they must know when this is happening perhaps partly by recognizing smells of seasonal changes. In social contexts, the age and sex of an individual can be recognized from urine or faces and elephants must be able to recognize individual elephants as well as other species by their smells. Indeed, elephants can been taught to discriminate between the smells of familiar and unfamiliar humans, and to track the smell of an individual.
To summarize, smell information will include where another individual has been, what s/he has been eating, who they are, what their sexual status and age is, who they have been with and so on. In effect, for elephants, the olfactory world could be “something like” reading a newspaper for humans, acquiring information about the past (on the wind, in the water, on the earth, from faeces and urine, from tracks and rubs on vegetation), and possible futures (e.g. oncoming oestrus or a possible birth, movements of groups and forth coming musth). Elephants may also be acquiring information concerning other individual elephants’ (and other animals’) moods (e.g. whether frightened, anxious, or relaxed from body odours such as sweat). Particularly interesting smells are also indicated visually by movements of the trunk.
Gustatory communication
Observations with captive elephants confirm that they have a well developed sense of taste as they taste and smell different or new foodstuffs carefully before eating. One behaviour that was relatively common was placing the trunk in another’s mouth, here tactile, olfactory and taste messages as well as visual, and may be, emotional ones, will be acquired ( further discussion below).
Tactile communication
Despite the thick skin of elephants (5-15mm), they are extremely sensitive to gentle touch. In teaching experiments [58], gently stroking between the front and hind legs and on the shoulder acted as a positive rein forcer, and helps to calm anxious elephants. The multi-sensory trunk is used to discriminate objects by touch [53] and to gather information and communicate to others using all sensory capacities. But, other parts of the body are also used to touch or feel each other, for example, seismic vibrations are picked up through the feet [40,86,87]. The feet are used to search for and manipulate objects (e.g. branches, pieces of rock etc) and feel others. They are also used in violent interactions: To kick, stamp or squash irritants and frightening objects such as fences or other species, including humans. All other parts of the body can also be used to touch, rub, push or scratch another: The head, shoulders, belly, quarters and the ears; as well as the trunk. Eighteen percent of the behaviours in interactions had a tactile component. The common use of tactile communication in this young and predominantly male group may enhance amicable bonds, but further research in family groups is needed.
Auditory communication, audible to the human ear
This was used very little (0.5%) during the observations. In some vocalisations, such as trumpeting, the trunk is used as a vibratory chamber to increase the amplitude of the sound. Trumpeting has sound characteristics which facilitate dispersal and location over a large distance (high amplitude and alternating frequencies facilitating location using the two ears) and trumpets are individually different and recognizable [29], but there were no trumpets during the study. It is possible that the elephants were using infra sound or seismic vibrations, but visual signs of this would be likely and would have been picked up by the observers. Very little research on the occurrence and communicative significance of non vocal noises has been reported in elephants. In this study, “blow” and “puff” accounted for 1% of the behaviours used in social interactions; twice as much as vocalisations and “Blow” appears to have an important communicative value, since it was rarely ignored. Elephants moving around make a variety of noises: Breaking sticks, pushing over trees, pulling branches or grass, sighing, farting and so on, but these were not recorded in this study. When and where these noises are made with intent to communicate (e.g. to stay in touch with the rest of the group) requires further research. However, we know that elephants (and other species) can be aware of making such environmental noises because when they do not want to be found (when hunted or searched for) they can move extremely silently, (indicating there awareness of the noises they make), and stop them intentionally.
Visual communication
All the behaviours recorded and analyzed (with the exception of 0.5% vocal noises) were visual (97%), all be it that some also had olfactory, tactile, gustatory or auditory messages attached. Purely visual signals accounted for over half (58%), it is clear that visual signals are numerous and frequently used in close contact. Further discussion on the use of the trunk and the cause and function of the different visual messages follows.
The trunk, a multi-sensory communicative organ
The elephant’s unique trunk functions as a nose, hand, mouth/tongue, and vibrating chamber, called “synesthesis” [88], as it is used for conveying and receiving messages in all the sensory modalities (Table 4).
The trunk is also a manipulative organ, like humans, elephants are manipulators, humans with their hands, elephants with their trunks. All of their food is collected using the trunk, which sorts, selects, prepares and processes it [24,25,58] .The trunk has approximately 500 muscles controlling its movement [57]. Consequently, it can perform a great variety of movements such as:- Gripping, pushing, twisting, pulling, grabbing, touching. It can be turned and twisted into small places, used to investigate, to caress, push or slap other elephants and humans [59]. It is particularly used to investigate others’ body areas rich in smells, such as the mouth, ears, feet, temporal glands, anus and vulva. It can be used with great skill to lift, pick up, balance, carry, place and stack heavy objects and the tusks, head and trunk working together can act as a fore-loader. Adams [67], personal observations in India with timber elephants). It can also be used to find and lift objects under water (personal observations) and find small hidden objects (such as rings and buckles hidden in hay) and is skilled at sorting objects, even out of sight. It is used for breaking or pushing things over, such as trees or fences (including discriminating between electric and insulated lines, in order to lift posts our of the ground [89]. It is used to make and use tools [89,90] and can be used to manipulate objects in a mirror [91], which humans find difficult. The trunk is used as a resonating cavity for vocalisations, and used to learn to imitate human words [92] and invent new sounds (personal videos elephants in the [93].
The use of the trunk in communication accounted for 18% of all the behaviours in interactions. The 16 different trunk movements had meanings inall 4 of the batched behavioral categories. The trunk is also used of course, for self directed behaviours such as self grooming, smelling, rubbing, scratching, stroking, and essential for drinking, food selection and processing.
The trunk placed in the performer’s own mouth was frequent in training experiments [94], occurring when the individual was uncertain what to do, or confused. It occurs in the same situations in which children put their finger or thumb in their mouths which demonstrate uncertainty [95]. On several occasions when teaching elephants with unprotected contact, when they were frustrated or annoyed, they stamped one front leg. This is a similar behavior given in a similar situation by a child stamping a foot. Beating the trunk on the ground is another well known behaviour in captive elephants associated with frustration (e.g. awaiting food or to be unshackle [51], but was not observed during these observations.
One of the most interesting movements is the trunk placed in another’s mouth, a relatively common behaviour (performed 121x’s by an initiator and by a recipient 54x’s: Total 175x’s). Here the performer acquires information about the recipient and it also demonstrates “trust/confidence/amicability” as biting the other’s trunk would be easy. This action has frequently been observed to have a calming influence on the recipient (observations & videos). Some handlers imitate this action by stroking the tongue of an elephant when greeting. The establishment of predictability in behaviour, “trust” or “confidence in each other” has been widely used by good animal handlers for generations [85,96-98] and is now considered to be one of the most important components in establishing good cooperative animal handling and teaching [58].
The hand/nose/tongue trunk is used in almost every type of situation to manipulate the world, to communicate with others and to read intentions and emotional states of others. Without being aware that his trunk is HIS, the elephant would be unable to do these things, indicating his self awareness of his trunk and his ability to control what, where and when it moves. (Further discussion below).
The indication of parallel experiences between the elephant trunk and human hand underlines the importance of taking a conditional anthropomorphic approach to further comprehend elephant epistemology and mental aptitudes [68,69,71,82].
The meanings of the different behaviours
Communication in elephants, like the rest of their behaviour is flexible and adaptable [24,25,81]. One of the problems is to assess which behaviours (other than vocalisations) are performed with intent to communicate, and which are coincidental and have no communicative significance.
The meanings of many behaviours are self evident; that is, they are “explicit” and can be batched into two categories (i) aggression and avoidance / withdrawing all of which will tend to split the group. (ii) Affiliation and interest in the other, which will encourage group cohesive or sticking. The third category contains behaviours frequently used in communication, which have an “implicit” (inherent, hidden) meaning. Many visual signals are in this category. Further discussion follows.
“Uncertainty”. Behaviours indicative of approach avoidance conflict and frustration, convey a message of indecision
Tail wagging, head shaking and ear flapping are widely used in communication throughout large mammals [26,29,30]. They often occur in approach-avoidance conflict or when frustrated: Where the ability to perform a desired behaviour is inhibited. At such times, often an irrelevant and or less urgent behavior is performed. These have been called “transitional” or “displacement activities” and their original cause related to cutaneous irritation or frustrated movement [26,76,99-101]. Sometimes these behaviours are ritualized for communication (exaggerated and emancipated from their original cause/s) to carry a specific message [76,77,100]. However, highly ritualized displays (which are common in birds), are relatively rare in large herbivores [26], perhaps because the meaning is clearer. For example, behaviours related to skin irritation occur frequently in communication associated with approach-avoidance conflict and frustration [26,78,99,102] and are characterized by some arousal [103]. Behaviours originally associated with cutaneous irritation are tail wagging, ear flapping and head shaking or nodding. Tail wagging was the most frequent; the most common responses were to ignore, or to reciprocate. Ear flapping and head shaking were also frequently ignored or reciprocated. But, since neither head shaking nor ear flapping resulted in aggression, avoidance or withdrawal, they do not indicate any threat, but rather that the communicant is slightly aroused and indecisive/ uncertain what to do.
An interesting behaviour in the same category is placing the trunk in his own mouth. Children may also place their fingers in their moths when in indecisive situations [26,29,58,95], another similarity to humans.
Anselme & Gurturkun [104], in a recent paper shows that “uncertainty” magnifies food searching behavior in birds which then increases exploration and survival. This “uncertainty principle” could equally be applied in communication to reduce potentially emotionally inflammatory situations, encourage group cohesion which in turn will encourage social exploration and curiosity, leading to the acquisition of more environmental and social knowledge.
Ignoring directed behaviours
Ignoring a directed behaviour accounted for 30% of the recipients responses. The reasons for ignoring could be that the directed behaviour had no meaning, or, that the recipient had not seen it. Since all the performed behaviours were responded to on other occasions, ignoring cannot be the result of it having no meaning. Since the initiators behavior was only recorded when it was clearly directed at another, it is unlikely that the recipient was not aware of it as elephants are visual aware as we have shown (Table 2).
Therefore, the most likely explanation is that the recipient chose to ignore that behaviour directed at him/her. Detailed investigation of what behaviours were ignored indicates that some of the most frequently ignored demonstrated “uncertainty” (e.g. tail wag, head nod, flap ears, swing trunk and head shake). The message of “uncertainty” or indecision had been received, but, because there was no threat to social cohesion, there was no need for a response. Ignoring in this situation may help to deflate any emotional conflict.
It is less clear why social behaviours, such as approach and contact make, turn body towards, turn head towards, tail up (indicating a rise in excitement), trunk up, and tusking another’s body are so frequently ignored. But this may indicate that ignoring a situation in which conflicts might otherwise arise and grow, will aid group cohesion.
Behaviours that are less ignored will have strong messages. These include putting the trunk in the mouth of another, which shows interest, familiarity, confidence or “trust”. “Blow” and trunk extended sniffing were also rarely ignored both indicating something like” take heed, there is something interesting around”. Drawing both ears back against the head was also infrequently ignored; which may have a message something like “I am slightly concerned about the situation” and the recipient reciprocating message will mean: “I have seen you and am therefore also slightly concern” .
Do as you have been done by/ reciprocity or imitation
Another puzzle is that reciprocity/ imitative / ‘do as you have been done by’/‘be done by as you did’ [105], is much more frequent than expected overall and for particular behaviours. This is relevant to discussions concerning mirror neurons [106,107], which have now been demonstrated to be widely distributed in different species rather than restricted to humans.
Reciprocity and its role in fostering bonding and cooperation has been discussed in some animals [108], but has not previously been reported in elephants. Sixteen of the most commonly recorded behaviours all of which demonstrated affection/sticking behaviour or uncertainty, were very significantly imitated by the recipient. These were those involving orientation movements and postures (ears prick or turn head towards the other,) investigation (trunk up & smelling), interest in another (approach and contact make). They included those indicating an increase in arousal and preparation for action such “tail up” [26]. Behaviours indicating “uncertainty”/ indecision, were also significantly reciprocated (such as tail wag, head nod, swing trunk, head shake and trunk to own mouth).
It may be that reciprocal behaviour is more common than has been previously reported in many species. Randle & Kiley-Worthington showed that inter-species imitation (the animal imitating a novel action of the human teacher) is frequent in teaching situations and, as in children, can be used as a teaching aid. The function may be to indicate to another; something like “I am also feeling the same way”, that is emotional contagion [65,66], which is another way of indicating awareness of others’ feelings and intentions. It is interesting that elephants can also be taught to imitate humans speech which is suggested helps them to bond with humans [92].
Kingsley [105], maintains that both “do as you would be done by “that is be nice to each other, and “be done by as you did” (if nasty, it will be returned) are moral rules which children should obey. Following on from this, reciprocating with aggressive behaviours when aggressed would ensure that the social contract is adhered to and those who do not adher can leave the society, so the society can continue. Reciprocity of behaviour (and its accompanying emotions) that might threaten the group stability and the social contract: “Be done by as you did”, would then discourage further contravention of the social contract.
Context dependent and context independent meanings
Context dependent meanings for some communication in elephants (and other species) has been demonstrated for many vocalizations [27], and head and tail movements in ungulates and carnivores [26,30].
One of the particularly interesting consequences of context dependent messaging is that, because a particular behaviour acts as an analogue system to convey a message about the general level of excitement or arousal of the individual, many behaviours are used in a variety of situations. The specific meaning, that is why the elephant is aroused, can only be gathered from the context, thus whether s/he is frightened, worried, feeling slightly aggressive or sexy will only be gathered from the context. As a result, each individual must be acutely aware of the environment and the intent of others or he will not be able to interpret accurately the meaning of the message. Any witness will have to have an understanding of the situation and be aware of others’ intentions that are his emotions, desires and needs to interpret the message. Such a reading of intentions of others has been labeled having a “theory of mind”: Defined as “attributing perceptual, epistemic, and volitional states to others and themselves” [109-117]. Therefore, animals that use context dependent communication must have a ‘theory of mind’ [71,110] or they would not be able to communicate, have a social contract and a social organization.
By contrast, to understand the meaning of context independent messages (such as human language), it is not always necessary to have an awareness of others intentions, desires and needs because the meaning of the message is constant, whatever the situation, emotions and intentions of the communicant which is what allows human language to be understood out of the present context: On the computer or telephone. This is because context independent communication conveys complex, symbolic non-emotional messages entirely divorced from the context and, consequently, can be understood without having any theory of mind of the communicator and his intentions.
Context dependent communication therefore presents a different complex cognitive assessment of the world from context independent language. But, judgments concerning mental development and complexity, are usually made only by comparison to humans, often because of the overruling importance of context independent language in which humans both speak and think most of the time which acts as a cognitive handicap when attempting to understanding the ontology and epistemology of species who use context dependent communication and who, to understand the message clearly, must be acutely aware of the social and physical environment around them and the feelings and intentions of others [66,71]. Without an awareness of others feelings and intentions, such communication will not function and without communications, there could be no social contract, recognition of other individuality, and their knowledge or roles, that is no “social networking” [11].
Rethinking elephants social contract and their epistemology related to these results
It may be that unless there is a need for constant competition within a group, (such as access to food, shelter or other scarce resources to ensure survival), the basis of any social grouping in mammals is emotional attachments [81,118,119], rather than competition for resources. This ontologically starts with the mother/infant attachment [120], controlled initially hormonally but as a result of learning, often reinforced and continuing into adulthood. Thus, it is reasonable to consider that positive emotional bonds become the social cement of some societies [121], rather than socially negative or competitive behaviours which will tend to disperse or split the group and “dominance hierarchies” evolved to reduce competition and injury to group members. The “dominance hierarchy” gives priority of access to resources in all situations to certain individuals. But, the explanation of elephant society in terms of “dominance hierarchies” [73,74,122], has obscured the importance of less melodramatic, non competitive behaviours including those that could help to de flame potentially inflammatory situations and split the group, such as ignoring or indecisive behaviours.
In addition in species such as large herbivours where resources are usually widespread and available for all or none, there is little need for constant competition within the group. Individuals have different personalities and consequently different placings in the different behavioural hierarchies, that is some are more aggressive than others, some more affiliative. Some more submissive, and some more socially involved [85]. But, there is not one individual who is top of the aggressive hierarchy and low in the avoidance hierarchy as there would be if there was a “dominance hierarchy” controlling access to resources. The organization of this society is more complex with individuals having a variety of different roles.
In large free living herbivors since there is no need for constant competition for resources, behaviours and their accompanying emotions which encourage group cohesion would be likely to be common and selected for such as those demonstrating interest and affiliation to keep the group together. Demonstrations of indecision that is “uncertainty”, “reciprocity” and ignoring directed behaviour may also help to here the group by reducing negative emotions and possible group splitting.
The question remains why group cohesion is so important. To grow, survive and reproduce, each individual must become a natural botanist, zoologist, ethologist, meteologist, geologist and geographer that is s/he must become a good “natural ecologist” [81,123]. There is an enormous amount of information to acquire by each infant in order to survive, so perhaps, the most important reason for group living is to enable the acquisition of such necessary knowledge by facilitating observational, social learning and imitation, which aid in a rapid and less risky accumulation of knowledge than learning everything by trial and error. However, it is necessary to know who to learn from: To know what knowledge other individual have. Thus an awareness of the age, personality, role [124] and knowledge of each group member will be crucial. Thus, older animal’s greater knowledge is recognized so they often become decision makers or “matriarchs” [25,71]. Strong, askilled manipulators will have a role of helping infants out of mud holes [125,126].
If the society is to prosper and reproduce, the society’s rules, that is, the social contract must be obeyed. Such rules as “do not attack infants”, ”recognize others roles” or “do not perform socially negative behavior unless another breaks the rules”. If an individual does break the rules, then action must be taken. This would account for the frequency of reciprocal behaviours: “If you are nice to me, I will be nice to you; if you are nasty, I will return it in kind”.
There are “other ways of seeing” outlined by Goethe [127], which may be imperative when considering other species epistemology. One idea that is becoming increasingly apparent and may be one of the most significant and important developments for life, is the recognition of how wide spread symbiosis is, both between and within species [128-130]. The importance of symbiosis in the social world of different species [131,132] and different strategies to encourage this in the social contract is another way forward to an understanding of that species epistemology [66,71, 81,82].
The question remains why, what would appear to be a relatively small evolutionary step, that of associating a particular movement posture or call with a particular message, has not always been taken. But, different cognitive maps are held by different individuals and species, for example blind humans become more sensitive to wind, smells and touch than normal humans, and other “handicaps” in humans also point out different cognitive maps. For different species, an emphasis on olfaction may require a different concept of space and time from that of humans [81]. A different world view will be acquired by two simultaneous large monocular visual fields, compared to a large binocular visual field and poor peripheral monocular vision characteristic of humans. The different world view implicated by context dependent communication also illustrates a different world view since when using context dependent communication, the recipient has to be aware of the “perceptual epistemic, volitional states of the other” to receive the correct message and must “socially network”.
There is much evidence that non-human mammals do recognize other living “beings”; that is they recognize the body/mind/moods/emotions/intentions/knowledge/roles of others, both inter- and intra-species, and discriminate between the living and the dead [25]. Such communication requires an awareness of others body/mind being that context independent communication does not always need. Thus, awareness that the other has a mind is a necessary attribute for context dependent communication.
Many even naïve/wild mammals have an ability to read others feelings and intentions, including those of other mammals, humans. Even naïve rhinos, horses, dogs, cattle, elephants, lions, tigers respond rapidly to humans moods, although some humans may need experience before they are able to read the intentions of an animal [58]. Having an awareness of others and their intentions is a necessary mental attribute for context dependent language users without which they could not have a social ontology, social organizations or a social network. Whether such animals have “reflective self-knowledge” [133-138], is not the same question.
Figure 1: Visual gestures as three elephants begin to walk down a path.