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Department of Physics, Chemistry and Biology
Master Thesis
Olfactory discrimination performance and
long-term odor memory in Asian elephants
(Elephas maximus)
Alisa Rizvanovic
LITH-IFM-A-Ex--12/2639--SE
Supervisor: Matthias Laska, Linköpings universitet
Examiner: Mats Amundin, Linköpings universitet
Department of Physics, Chemistry and Biology
Linköpings universitet
SE-581 83 Linköping, Sweden
Rapporttyp Report category
Examensarbete
D-uppsats
Språk/Language
Engelska/English
Titel/Title:
Olfactory discrimination performance and long-term odor memory in Asian elephants (Elephas maximus) Författare/Author:
Alisa Rizvanovic
Sammanfattning/Abstract:
Behavioral evidence suggests that Asian elephants strongly rely on their sense of smell in a variety of contexts including foraging and social communication. Using a food-rewarded two-alternative operant conditioning procedure, three female Asian elephants were tested on their olfactory discrimination ability with 1-aliphatic alcohols, n-aldehydes, 2-ketones, n-carboxylic acids and with a set of twelve enantiomeric odor pairs. When presented with pairs of structurally related aliphatic odorants, the discrimination performance of the elephants increased with decreasing structural similarity of the odorants. Nevertheless, the animals successfully discriminated between all aliphatic odorants even when these only differed by one carbon atom. The elephants were also able to discriminate between all twelve enantiomeric odor pairs tested. Additionally, the elephants showed an excellent long-term odor memory and remembered the reward value of previously learned odor pairs after three weeks and one year of recess. Compared to other species tested previously on the same sets of odorants, the Asian elephants performed at least as good as mice and clearly better than human subjects, South African fur seals, squirrel monkeys, pigtail macaques, and honeybees. Taken together, these results support the notion that the sense of smell may play an important role in regulating the behavior of Asian elephants.
ISBN
LITH-IFM-A-EX—12/2639—SE
__________________________________________________
ISRN
__________________________________________________
Serietitel och serienummer ISSN
Title of series, numbering
Handledare/Supervisor Matthias Laska
Ort/Location: Linköping
Nyckelord/Keyword:
Asian elephant; Elephas maximus; Behavioral testing; Olfactory discrimination; Olfactory memory
Datum/Date
2012-05-25
URL för elektronisk version
Institutionen för fysik, kemi och biologi
Department of Physics, Chemistry and
Biology
Contents
1 Abstract............................................................................................................... 1
2 Introduction ........................................................................................................ 1
3 Material and methods ......................................................................................... 3
3.1 Animals and management ............................................................................ 3
3.2 Odor stimuli.................................................................................................. 3
3.3 Experimental set-up ..................................................................................... 8
3.4 Training and testing procedure .................................................................. 10
3.5 Experimental design ................................................................................... 12
3.6 Statistics ..................................................................................................... 14
4 Results .............................................................................................................. 15
4.1 Experiment 1: Odor discrimination with structurally related aliphatic
odorants ............................................................................................................ 15
4.1.1 Aliphatic 2-ketones .............................................................................. 16
4.1.2 Aliphatic 1-alcohols ............................................................................. 17
4.1.3 Aliphatic n-aldehydes .......................................................................... 18
4.1.4 Aliphatic n-carboxylic acids ................................................................ 19
4.1.5 Comparison between odorant classes .................................................. 20
4.2 Experiment 2: Odor discrimination with enantiomers ............................... 21
4.3 Experiment 3: Long- term odor memory ................................................... 21
5 Discussion ........................................................................................................ 23
5.1 Odor discrimination with structurally related aliphatic odorants .............. 23
5.2 Odor discrimination with enantiomers ....................................................... 25
5.3 Long-term odor memory ............................................................................ 27
5.4 Theoretical explanations for the good odor discrimination in Asian
elephants ........................................................................................................... 28
5.5 Conclusions ................................................................................................ 29
6 Acknowledgements .......................................................................................... 30
7 References ........................................................................................................ 30
1
1 Abstract
Behavioral evidence suggests that Asian elephants strongly rely on their
sense of smell in a variety of contexts including foraging and social
communication. Using a food-rewarded two-alternative operant
conditioning procedure, three female Asian elephants were tested on their
olfactory discrimination ability with 1-aliphatic alcohols, n-aldehydes, 2-
ketones, n-carboxylic acids and with a set of twelve enantiomeric odor
pairs. When presented with pairs of structurally related aliphatic odorants,
the discrimination performance of the elephants increased with decreasing
structural similarity of the odorants. Nevertheless, the animals successfully
discriminated between all aliphatic odorants even when these only differed
by one carbon atom. The elephants were also able to discriminate between
all twelve enantiomeric odor pairs tested. Additionally, the elephants
showed an excellent long-term odor memory and remembered the reward
value of previously learned odor pairs after three weeks and one year of
recess. Compared to other species tested previously on the same sets of
odorants, the Asian elephants performed at least as good as mice and
clearly better than human subjects, South African fur seals, squirrel
monkeys, pigtail macaques, and honeybees. Taken together, these results
support the notion that the sense of smell may play an important role in
regulating the behavior of Asian elephants.
Keyword: Asian elephant; Elephas maximus; Behavioral testing; Olfactory
discrimination; Olfactory memory
2 Introduction
Some authors argue that brain size correlates with cognitive abilities.
However, the few studies so far that assessed cognitive abilities in Asian
elephants (Elephas maximus) showed mixed results depending on the type
of task and the sensory system involved (Cozzi et al., 2001; Hart and Hart
2007; Plotnik et al. 2011).
Behavioral evidence suggests that Asian elephants strongly rely on their
sense of smell in a variety of contexts including foraging and social
communication (Langbauer 2000; Rasmussen 2006; Rasmussen and
Krishnamurthy 2000; Santiapillai and Read, 2010; Scott and Rasmussen
2005; Sukumar 2003; Vidya and Sukumar 2005). The behavior of Asian
elephants has been studied in some detail and suggests that chemical
communication is an important part in their social interactions (Rasmussen
1999; Rasmussen 2006; Rasmussen 1998; Rasmussen and Krishnamurthy
2000; Rasmussen and Schulte 1998; Schulte et el. 2005). In fact, the
2
elephant is one of the few mammal species so far for which a sex
pheromone has been chemically identified and functionally verified
(Rasmussen et al. 1997, 2005). Anatomical evidence of well-developed
olfactory and vomeronasal systems (Göbbel et al. 2004; Johnson and
Rasmussen 2002; Koikegami et al. 1941; Shoshani et al. 2006) as well as
of specialized skin glands (Lamps et al. 2001; Wheeler et al. 1982) further
supports the idea that the sense of smell plays a crucial role in regulating
the behavior of elephants.
Until recently, however, no behavioral test existed which would allow us to
systematically assess the olfactory capabilities in this species. Asian
elephants have successfully been trained in two-choice visual (Rensch
1957); Rensch and Altevogt 1955; Nissani et al. 2005), auditory (Heffner
and Heffner 1982) and tactile (Dehnhardt et al. 1997) discrimination tasks.
A previous study by Arvidsson et al. (2012) developed and successfully
applied an olfactory discrimination paradigm for Asian elephants and
collected first data on learning speed, olfactory memory and olfactory
discrimination performance. The paradigm is based on a food-rewarded
two-alternative operant conditioning procedure. The animals learned to
sniff at two odor ports and were food-rewarded when they performed an
operant response (placing the tip of the trunk at a certain position of the
experimental set-up) upon correctly identifying the rewarded odor. The
study showed that Asian elephants indeed have fast learning abilities and a
good olfactory memory.
Similar operant conditioning procedures to assess olfactory learning
capabilities and olfactory long-term memory have been employed with
other mammals such as squirrel monkeys (Laska and Hudson 1993), spider
monkeys (Laska et al. 2003), pigtail macaques (Hübener and Laska, 2001),
South African fur seals (Laska et al. 2008), mice (Bodyak and Slotnick
1999), rats (Slotnick et al. 1991), and dogs (Lubow et al. 1973). This
allows for direct comparisons of olfactory learning performance and
olfactory long-term memory performance between species.
Using aliphatic odorants and enantiomers that have previously been used
with humans (Laska and Teubner, 1998, 1999; Laska and Hübener 2001),
squirrel monkeys (Laska and Freyer 1997; Laska et al. 1999a,b; Laska et
al. 2005), Pigtail macaques (Laska et al. 2005), South African fur seals
(Laska et al., 2010), mice (Laska and Shepherd, 2007; Laska et al. 2008),
and honeybees (Laska and Galizia, 2001; Laska et al. 1999) in this study
allows for comparisons of olfactory discrimination performance between
species and assessment of the mechanisms underlying between-species
differences and similarities in this basic measure of chemosensory
capabilities.
3
The aims of the present study were to collect data on olfactory
discrimination performance for structurally related odorants in three female
Asian elephants, to collect data on olfactory long-term memory, to assess
odor structure-activity relationships, and to compare them to those of other
species tested previously on the same sets of odorants.
3 Material and methods
3.1 Animals and management
The study was conducted using three adult female Asian elephants
(Elephas maximus) housed at Kolmården Wildlife Park. Saonoi and Bua
were born 1996 and 1997, respectively in Thailand at work camps and have
been housed at the Swedish zoo since 2004. Saba (born 1968) was
transferred to Kolmården Wildlife Park from Zoo Le Pal, France, at the end
of 2007. The animals were kept as a group in two indoor rooms
(approximately 150 m2 and 250 m
2) but were allowed to be in an outdoor
enclosure (750 m2) or an outdoor exhibit (3000 m
2) at least once a day or
for a larger part of the day when the weather was appropriate. The
elephants were fed pellets in the morning and roughage and branches were
provided ad libitum. Environmental enrichment was provided at least once
a day in the form of scattered and hidden fruits and vegetables throughout
the enclosure. During the study no food-deprivation was required. The
elephants were kept in a hands-on system in which the keepers have full
access to the animals and they were therefore trained to follow commands
and perform certain motor patterns upon demands. The experiments
outlined here comply with the Guide for the Care and Use of Laboratory
Animals (National Institutes of Health Publication no. 86-23, revised 1985)
and with current Swedish laws.
3.2 Odor stimuli
For the assessment of odor discrimination with structurally related odorants
two sets of stimuli were used. The first set comprised four aliphatic ketones
(2-butanone, 2-pentanone, 2-hexanone, and 2-heptanone), four aliphatic
alcohols (1-butanol, 1-pentanol, 1-hexanol, and 1-heptanol), four aliphatic
aldehydes (n-butanal, n-pentanal, n-hexanal, n-heptanal), and four aliphatic
carboxylic acids (n-butanoic acid, n-pentanoic acid, n-hexanoic acid, n-
heptanoic acid) (see Figure 1). The second set comprised the enantiomers
of limonene, carvone, dihydrocarvone, dihydrocarveol, limonene oxide,
alpha-pinene, menthol, camphor, beta-citronellol, rose oxide, iso-pulegol
and fenchone (see Figure 2). When introducing new odorants to the
animals, n-amyl acetate and anethole were used by pairing one of these
4
odors with a new odorant. These two odorants were already highly familiar
to the animals and were therefore used as a “standard” task, in which the n-
amyl acetate was used as the rewarded odor and anethole as the
unrewarded odor. For the memory tests, ethyl butyrate was used as the
rewarded odor vs. 2-phenylethanol as the unrewarded odor and n-amyl
acetate was used as the rewarded odor vs. anethole as the unrewarded odor.
All substances were obtained from Sigma-Aldrich (St. Louis, MO) and had
a nominal purity of at least 99 %. They were diluted using near-odorless
diethyl phthalate (Sigma-Aldrich) as the solvent in such a way to provide
clearly detectable stimuli of equal subjective intensity. The concentrations
of the odorants are shown in table 1, 2 and 3.
5
2-ketones 1-alcohols
2-butanone 1-butanol
2-pentanone 1-pentanol
2-hexanone 1-hexanol
2-heptanone 1-heptanol
n-aldehydes n-carboxylic acid
n-butanal n-butanoic acid
n-pentanal n-pentanoic acid
n-hexanal n-hexanoic acid
n-heptanal n-heptanoic acid
Figure 1: The aliphatic odorants used and their molecular structures.
6
Enantiomers
Figure 2: The enantiomers used and their molecular structures modified from Laska (2004) and Laska and Galizia (2001). The black shade in the structures means that it is protruding towards the reader.
7
Table 1: The odorants used for training and long-term odor memory and their concentrations. CAS number is a unique numerical identifier for every chemical.
Odorant CAS number Dilution
n-amyl acetate 628-63-7 1:5 anethole
104-46-1 1:10
ethyl butyrate 105-54-4 1:3 2-phenylethanol 60-12-8 1:3
Table 2: The aliphatic odorants used and their concentrations. Chemical classes are given in italics.
Odorant CAS number Carbon chain length Dilution
1-alcohols
1-butanol 71-36-3 4 1:10
1-pentanol 71-41-0 5 1:10
1-hexanol 111-27-3 6 1:3
1-heptanol 111-70-6 7 1:3
n-aldehydes
n-butanal 123-72-8 4 1:10
n-pentanal 110-62-3 5 1:10
n-hexanal 66-25-1 6 1:10
n-heptanal 111-71-7 7 1:5
2-ketones
2-butanone 78-93-3 4 1:10
2-pentanone 107-87-9 5 1:10 2-hexanone 591-78-6 6 1:3 2-heptanone 110-43-0 7 1:3
n-carboxylic acids n-butanoic acid 67-43-6 4 1:100 n-pentanoic acid 109-52-4 5 1:100 n-hexanoic acid 142-62-1 6 1:100 n-heptanoic acid 111-14-8 7 1:20
8
Table 3: The enantiomers used and their concentrations.
Odorant CAS number Dilution
(S)-(+)-carvone 2244-16-8 1:3
(R)-(–)-carvone
6485-40-1 1:3
(R)-(+)-limonene 5989-27-5 1:3
(S)-(–)-limonene
5989-54-8 1:3
(+)-fenchone 4695-62-9 1:3
(–)-fenchone
7787-20-4 1:3
(+)-dihydrocarvone 5524-05-0 1:2
(–)-dihydrocarvone
7764-50-3 1:2
(+)-dihydrocarveol 22567-21-1 1:2
(–)-dihydrocarveol
20549-47-7 1:2
(R)-(+)-beta-citronellol 1117-61-9 1:3
(S)-(–)-beta-citronellol
7540-51-4 1:3
(1R)-(+)-camphor 464-49-3 1:10
(1S)-(–)-camphor
464-48-2 1:10
(+)-rose oxide 16409-43-1 1:3
(–)-rose oxide
5258-11-7 1:3
(+)-limonene oxide 1195-92-2 1:3
(–)-limonene oxide
42477-94-1 1:3
(+)-iso-pulegol 104870-56-6 1:5
(–)-iso-pulegol
89-79-2 1:5
(1S,2R,5S)-(+)-menthol 15356-60-2 1:10
(1R,2S,5R)-(–)-menthol
2216-51-5 1:10
(+)-alpha-pinene 7785-70-8 1:5
(–)-alpha-pinene 7785-26-4 1:5
3.3 Experimental set-up
To present the odorants two high density polyethylene (HDPE) boxes with
removable lids (Rubbermaid Cooling Bags, 35 cm high x 35 cm wide x 20
cm deep) were used. The tight fitting lid of each container was equipped
with a ventilator (6 cm in diameter) powered by a lead accumulator (Clas
Ohlson, power: 12V, 1.3Ah). The ventilator provided an ingoing airflow of
approximately 0.58 m3 min
-1. A total of 130 holes of 3 mm diameter were
placed in intervals of even distance to form a filled circle with a diameter
9
of 7.5 cm. These holes were drilled in an exact pattern in the middle of one
of the front sides of each odor box, serving as an outlet for the airflow
provided by the ventilator.
For the presentation of the odorant, a circular filter paper of 9 cm diameter
(Grycksbo Pappersbruk AB) was placed into an open Petri dish and 1 ml of
the odorant was pipetted onto it and put in an odor box. After each session
the odor boxes were cleansed with warm water and perfume-free detergent.
The testing was carried out in the indoor quarters, in a separate room in
which the animals could be trained individually. The experimenter was
situated in a hayloft on the second floor where an opening in the wall was
fitted with a service door (106 cm high x 90 cm wide x 5 cm deep) made of
steel (see Figure 3). This door was modified to hold a window (45 cm high
and 75 cm wide) in its upper part which was covered with a steel grid (with
a mesh width of 4 x 4 cm). This grid separated the experimenter from the
animals while allowing the experimenter to observe and interact with the
animals and to present the food-reward. The grid also served as a barrier
that kept the elephants from reaching and grabbing the odor boxes. The
location of the door allowed the experimenter to observe the animals while
the animals had a very limited opportunity to see the experimenter.
The service door was located approximately 3 meters above the ground of
the test room and it was divided by a vertical bar in the middle into a left
and a right section. Each section contained an odor port (a round opening
with a diameter of 21 cm) at the lower half part of the door. Above the odor
ports was the rectangular grid-covered window through which the reward
could be given to the animals. A wooden platform inside the
experimenter’s room ensured that the odor boxes were placed with their
outlets congruent with the odor ports of the experimental set-up.
10
Figure 3: The experimental set-up from the experimenter’s side. The odor boxes were manually placed in front of the test grid with its odor ports at each test trial, then removed after the reward was given, to be randomly shifted for the next trial. The experimenter was separated from the elephant by a service door covered with a grid but was still able to present the odorants and the reward.
3.4 Training and testing procedure
The training and testing took place between the 6th
of September 2011 and
the 3th of February 2012. All training and testing was carried out in the
indoor quarters, in a room which the animals could be separated. The
elephant to be tested was brought individually, in a predetermined and
fixed order (with some exceptions), into the test room by the keepers. Once
the elephant was brought into the test room, the keepers locked the door
and left the room. The animals had no visual contact with each other during
testing but were within auditory range.
The sessions took place five days a week twice a day (with some
exceptions). The time of day varied from 8.00 am to 15:00 pm. During
each session 30 trials were completed. Each animal participated in a total
number of 168 sessions.
11
Each session started with the removal of a wooden board covering the
experimenter’s side of the experimental set-up. This made the animals
voluntarily approach the set-up. Each trial started with the experimenter
presenting the odor boxes with their outlets facing the odor ports. After a
verbal command – the loudly spoken word “now” – the elephants were
allowed to sample the odor ports and to indicate their decision by putting
the tip of their trunk onto the grid above the corresponding odor port (see
Figure 4). As the animals were not restrained they could always explore the
set-up with their trunks but any exploring of the set-up before the verbal
command was ignored. Only decisions made after the odor boxes were in
place and the command had been given were considered as valid decisions.
The rewarded and unrewarded odorants were presented in an order that was
pseudo- randomized either to the right or to the left. However, the same
side for the odorants was not used more than three times in a row. Since
one session had 30 trials, left side was the correct decision in 15/30 trials
and the right side was the correct decision in the other 15/30 trials. The
decision (correct or incorrect) of the animals was recorded after each trial.
Correct decisions were rewarded with a bridge (a whistle) followed by a
food-reward (a carrot). When an animal made an incorrect decision, the
odor boxes were simply removed and no reward was given.
When the elephants had completed the 30 trials comprising a session, the
end of the session was signalled by a verbal command – the loudly spoken
words “now you’re done” - followed by a few carrots being distributed
through the grid into the room. This made the animals move away from the
experimental set-up and the wooden board was again placed to cover the
inside of the set-up. The elephant was then led out from the test room by
the keepers.
12
Figure 4: The experimental set-up. The picture on the left shows an elephant exploring one of the two round odor ports, and the picture on the right shows an elephant performing the operant response, that is, placing the tip of its trunk onto one of the two rectangular grids to obtain a food reward. The vertical bar in the middle serves as a divider to make the animal’s choice behavior unequivocal.
3.5 Experimental design
A total of 3 experiments were conducted (see table 4). Experiment 1 was
conducted to assess the ability of the animals to discriminate between
aliphatic odors that are structurally related to each other (only differ in
carbon chain length). Experiment 2 was conducted to assess the ability of
the animals to discriminate between enantiomeric odor pairs which are
structurally identical except for chirality. Finally, Experiment 3 was
conducted to evaluate the long-term odor memory of the animals for a
given odor combination after a recess in training for three weeks and one
year.
13
Table 4: Experimental design. The table shows the different odor combinations used. Chemical classes are given in italics.
Experiment Rewarded odor Unrewarded odor
1. Odor discrimination with structurally related odorants
1-alcohols C7 vs. C4 C7 vs. C5 C7 vs. C6
1-heptanol 1-heptanol 1-heptanol
vs. vs. vs.
1-butanol 1-pentanol 1-hexanol
n-aldehydes C7 vs. C4 C7 vs. C5 C7 vs. C6
n-heptanal n-heptanal n-heptanal
vs. vs. vs.
n-butanal n-pentanal n-hexanal
2-ketones C7 vs. C4 C7 vs. C5 C7 vs. C6
2-heptanone 2-heptanone 2-heptanone
vs. vs. vs.
2-butanone 2-pentanone 2-hexanone
n-carboxylic acids C7 vs. C4 C7 vs. C5 C7 vs. C6
n-heptanoic acid n-heptanoic acid n-heptanoic acid
vs. vs. vs.
n-butanoic acid n-pentanoic acid n-hexanoic acid
2. Odor discrimination with enantiomers
(R)-(–)-carvone
vs.
(S)-(+)-carvone
(R)-(+)-limonene vs. (S)-(–)-limonene (+)-fenchone vs. (–)-fenchone (+)-dihydrocarvone vs. (–)-dihydrocarvone (+)-dihydrocarveol vs. (–)-dihydrocarveol (S)-(–)-beta-citronellol vs. (R)-(+)-beta-citronellol (1S)-(–)-camphor vs. (1R)-(+)-camphor (+)-rose oxide vs. (–)-rose oxide (+)-limonene oxide vs. (–)-limonene oxide (–)-iso-pulegol vs. (+)-iso-pulegol (1S,2R,5S)-(+)-menthol vs. (1R,2S,5R)-(–)-menthol (+)-alpha-pinene vs. (–)-alpha-pinene
3. Odor memory Three week recess
n-amyl acetate
vs.
anethole
One year recess ethyl butyrate vs. 2-phenylethanol
14
Experiment 1 was performed to assess the discrimination ability of the
animals with structurally related odorants. One of the odorants (with 7
carbons, from here on named C7) from each of the four chemical classes
was chosen as the rewarded odor and during the initial phase the animals
were allowed to become familiar with this rewarded odor. This was done
by using anethole as the unrewarded odor for 2-4 days (4-8 sessions). Once
familiarized with the rewarded odor the anethole was exchanged for one of
the other odorants of the same chemical class and each of the critical
stimulus combinations (C7 vs. C6, C7 vs. C5, and C7 vs. C4) was
presented for two consecutive sessions. The animals were assigned to
different treatments to avoid a possible order effect. One elephant was
assigned C4 as the first unrewarded odor, followed by C5 and C6 as the
second and third unrewarded odor while the second elephant was assigned
C6 as the first unrewarded odor (followed by C4 and C5). Thus the third
elephant was assigned C5 as the first unrewarded odor (followed by C6 and
C4). Between the different test combinations, up to two sessions with
anethole as the unrewarded odor was implemented if needed in order to
boost the animal’s confidence and to refresh its memory for the reward
value of the rewarded odor.
Experiment 2 was conducted to assess the discrimination ability of the
animals with enantiomers (that is, pairs of odorants that are mirror images
of each other). With each of the enantiomeric odor pairs one of the forms,
(+) or (-), was chosen as the rewarded odor and in an initial phase each
animal was allowed to become familiar with its rewarded odor by using
anethole as the already familiar unrewarded odor. Then, each rewarded
odor of a given enantiomeric odor pair was tested for two sessions against
its other form.
Experiment 3 was performed to assess the long-term odor memory of the
animals by using odor pairs that the animals have learned in a previous
study. The elephants were presented with these pairs of stimuli for two
sessions each after three weeks of recess for the n-amyl acetate vs. anethole
and one year recess for ethyl butyrate vs. 2-phenylethanol.
3.6 Statistics
In the method described here, the animal had two options: (1) to correctly
respond to the positive stimulus (hit), and (2) to falsely respond to the
negative stimulus (false alarm). The percentage of correct decisions was
used as the measure of performance.
15
In all tasks, the criterion of individual performance was set at either 70%
hits in one session of 30 decisions (corresponding to p < 0.05, two-tailed
binomial test), or at 80% hits in one session (corresponding to p < 0.01,
two-tailed binomial test). The rationale for choosing these criteria is that
the same criteria have been used in previous studies on olfactory learning
and discrimination performance with other species that data is being
compared to. First session was used when analyzing only one session and
first and second session was used when analyzing the combined sessions.
Correlations between discrimination performance and structural similarity
of odorants in terms of differences in carbon chain length were evaluated
using the Spearman rank correlation coefficient. Comparisons of
performance across individuals were made using the Mann-Whitney U-test
for independent samples.
4 Results
4.1 Experiment 1: Odor discrimination with structurally related
aliphatic odorants
The three elephants were presented with aliphatic ketones, aliphatic
alcohols and aliphatic aldehydes. Two elephants were presented with
aliphatic carboxylic acids (Saba did not participate in this task). Each group
of odorants allowed for three combinations that were tested with each
elephant (see table 4). The rewarded odors in this experiment were always
kept constant while the unrewarded odors were altered.
16
4.1.1 Aliphatic 2-ketones
Figure 5 shows the performance of the elephants in discriminating between
aliphatic 2-ketones. The left panel shows the elephants’ performance in the
first session and the right panel shows their performance in the first and
second sessions combined. The rewarded odor, 2-heptanone (C7) was
structurally most similar to 2-hexanone (C6), and differed from the
unrewarded odor by only one carbon atom, ΔC1. 2-heptanone (C7) was
least structurally similar to 2-butanone (C4), and differed from the
unrewarded odor by three carbon atoms, ΔC3. All three elephants
performed above criterion level (70%) in both the first session alone and in
the two sessions combined. A positive correlation between discrimination
performance and structural similarity of the odorants in terms of
differences in carbon chain length was found both for the first session alone
(r=+0.58, p=0.099) and a significant positive correlation for the two
sessions combined (r=+0.72, p=0.043).
Figure 5: Olfactory discrimination performance of the three elephants Saba (diamond), Saonoi (square), and Bua (triangle) with 2-ketones. Each data point represents the percentage of correct decisions from a total of 30 decisions (first session, left panel) or from a total of 60 decisions (first and second session combined, right panel). ΔC1 corresponds to the discrimination of 2-ketones which differ by only one carbon atom, and ΔC2 and ΔC3 to the discrimination of 2-ketones which differ by two and three carbon atoms, respectively. The horizontal dotted lines represent chance level (at 50%) and the criterion level (at 70%, two-tailed binomial test, p<0.05)
17
4.1.2 Aliphatic 1-alcohols
Figure 6 shows the performance of the elephants in discriminating between
aliphatic1-alcohols. The left panel shows the elephants’ performance in the
first session and the right panel shows their performance in the first and
second sessions combined. The rewarded odor, 2-heptanone (C7) was
structurally most similar to 2-hexanone (C6), and differed from the
unrewarded odor by only one carbon atom, ΔC1. 2-heptanone (C7) was
least structurally similar to 2-butanone (C4), and differed from the
unrewarded odor by three carbon atoms, ΔC3. All three elephants
performed above criterion level (70%) in both the first session alone and in
the two sessions combined. A positive correlation between discrimination
performance and structural similarity of the odorants in terms of
differences in carbon chain length was found both for the first session alone
(r=+0.35, p=0.320) and for the two sessions combined (r=+0.35, p=0.322).
Figure 6: Olfactory discrimination performance of the three elephants Saba (diamond), Saonoi (square), and Bua (triangle) with 1-alcohols. Each data point represents the percentage of correct decisions from a total of 30 decisions (first session, left panel) or from a total of 60 decisions (first and second session combined, right panel). ΔC1 corresponds to the discrimination of 1-alcohols which differ by only one carbon atom, and ΔC2 and ΔC3 to the discrimination of 1-alcohols which differ by two and three carbon atoms, respectively. The horizontal dotted lines represent chance level (at 50%) and the criterion level (at 70%, two-tailed binomial test, p<0.05).
18
4.1.3 Aliphatic n-aldehydes
Figure 7 shows the performance of the elephants in discriminating between
aliphatic n-aldehydes. The left panel shows the elephants’ performance in
the first session and the right panel shows their performance in the first and
second sessions combined. The rewarded odor, n-heptanal (C7) was
structurally most similar to n-hexanal (C6), and differed from the
unrewarded odor by only one carbon atom, ΔC1. N-heptanal (C7) was least
structurally similar to n-butanal (C4), and differed from the unrewarded
odor by three carbon atoms, ΔC3. All three elephants performed above
criterion level (70%) in both the first session alone and in the two sessions
combined. A positive correlation between discrimination performance and
structural similarity of the odorants in terms of differences in carbon chain
length was found both for the first session alone (r=+0.29, p=0.412) and for
the two sessions combined (r=+0.29, p=0.412).
Figure 7: Olfactory discrimination performance of the three elephants Saba (diamond), Saonoi (square), and Bua (triangle) with n-aldehydes. Each data point represents the percentage of correct decisions from a total of 30 decisions (first session, left panel) or from a total of 60 decisions (first and second session combined, right panel). ΔC1 corresponds to the discrimination of n-aldehydes which differ by only one carbon atom, and ΔC2 and ΔC3 to the discrimination of n-aldehydes which differ by two and three carbon atoms, respectively. The horizontal dotted lines represent chance level (at 50%) and the criterion level (at 70%, two-tailed binomial test, p<0.05).
19
4.1.4 Aliphatic n-carboxylic acids
Figure 8 shows the performance of the two elephants in discriminating
between aliphatic n-carboxylic acids. Saba did not participate in this task.
The left panel shows the elephants’ performance in the first session and the
right panel shows their performance in the first and second sessions
combined. The rewarded odor, n-heptanoic acid (C7) was structurally most
similar to n-hexanoic acid (C6), and differed from the unrewarded odor by
only one carbon atom, ΔC1. N-heptanoic acid (C7) was least structurally
similar to n-butanoic acid (C4), and differed from the unrewarded odor by
three carbon atoms, ΔC3. Both elephants performed above criterion level
(70%) in both the first session alone and in the two sessions combined. A
positive correlation between discrimination performance and structural
similarity of the odorants in terms of differences in carbon chain length was
found both for the first session alone (r=+0.37, p=0.409) and significant
positive correlation for the two sessions combined (r=+0.89, p=0.047).
Figure 8: Olfactory discrimination performance of the two elephants Saonoi (square), and Bua (triangle) with n-carboxylic acids. Each data point represents the percentage of correct decisions from a total of 30 decisions (first session, left panel) or from a total of 60 decisions (first and second session combined, right panel). ΔC1 corresponds to the discrimination of n-carboxylic acids which differ by only one carbon atom, and ΔC2 and ΔC3 to the discrimination of n-carboxylic acids which differ by two and three carbon atoms, respectively. The horizontal dotted lines represent chance level (at 50%) and criterion level (at 70%, two-tailed binomial test, p<0.05).
20
4.1.5 Comparison between odorant classes
In all eight cases for which a correlation between discrimination
performance and structural similarity of the odorants was calculated, this
correlation was positive. In two out of eight cases the correlation was
statistically significant. Saonoi scored a higher percentage of correct
discriminations with odors which differed by three carbons (C7 vs. C4)
than with odors which differed by only one carbon (C7 vs. C6) in all eight
cases. Similarly, Bua scored a higher percentage of correct discriminations
with odors which differed by three carbons (C7 vs. C4) than with odors
which differed by only one carbon (C7 vs. C6) in six out of eight cases. For
the remaining two cases Bua had equally good results for C7 vs. C4 and C7
vs. C6 that is 100% correct decisions on both. Saba scored a higher
percentage of correct discriminations with odors which differed by three
carbons (C7 vs. C4) than with odors which differed by only one carbon (C7
vs. C6) in three out of six cases. In the remaining cases she had better
results on C7 vs. C6 than C7 vs. C4. This may be due to a so-called “order
effect” since Saba always started with the odor combination in the critical
tests which supposedly was the “easiest” combination and then improved in
performance in the subsequent tasks. A comparison of performance across
individuals showed a significant difference between Saba and Saonoi
(p=0.0003) with Saonoi performing better than Saba. The comparison of
performance across individuals also showed significant differences
between Saba and Bua (p=0.0001) with Bua performing better than Saba.
No significant difference in performance was found between Bua and
Saonoi (P=0.8555).
21
4.2 Experiment 2: Odor discrimination with enantiomers
Figure 9 shows the performance of the elephants in discriminating between
enantiomeric odor pairs. All three elephants performed above criterion
level (70%) in all 12 discrimination tasks and thus were clearly able to
discriminate between all enantiomeric odor pairs presented. This was true
not only when the data of the two sessions performed per odor pair were
combined (as depicted in figure 9), but also for the first of two sessions
alone, suggesting a fast learning of the discrimination tasks.
A comparison of performance across individuals showed a significant
difference between Saba and Saonoi (p=0.0001) with Saonoi performing
better than Saba. The comparison of performance across individuals also
showed significant differences between Saba and Bua (p=0.0001) with Bua
performing better than Saba. No significant difference in performance was
found between Bua and Saonoi (p=0.3183).
Figure 9: Olfactory discrimination performance of the three elephants Saba (diamond), Saonoi (square), and Bua (triangle) with enantiomers. Each data point represents the percentage of correct decisions from a total of 60 trials (first and second session combined). The black vertical lines separate the data points for the different enantiomers. The horizontal dotted lines represent chance level (at 50%) and the criterion level (at 70%, two-tailed binomial test, p<0.05).
4.3 Experiment 3: Long- term odor memory
The three elephants were tested on their long- term odor memory by using
two different odor combinations that they had learned previously (see
Figure 10). The testing was carried out after a period of recess. For n-amyl
22
acetate vs. anethole the period that had passed was three weeks and for
ethyl butyrate vs. 2-phenylethanol it was one year.
All three animals performed at least as good in the two sessions after the
three-week recess compared to the two last sessions with n-amyl acetate vs.
anethole before the recess. On the very first 10 decisions after the recess all
three elephants scored 10 out of 10 correct decisions. Similarly, all three
animals performed at least as good in the two sessions after the 1-year
recess compared to the two last sessions with ethyl butyrate vs. 2-
phenylethanol before the recess. Here, too, on the very first 10 decisions
after the recess all three elephants scored 10 out of 10 correct decisions.
This clearly demonstrates that the animals did not quickly re-learn the
reward values of the rewarded and the unrewarded odor, but that they
indeed remembered them over these periods of time.
Figure 10: Long-term odor memory performance of the three elephants Saba (diamond) Saonoi (square) and Bua (triangle). The figure shows the performance of the animals in the two last sessions before the recess in testing, followed by the performance in the first two sessions after three weeks and one year of recess, respectively, for the given odor combination. The black vertical line separates the two tasks. The horizontal dotted lines represent chance level (at 50%) and the criterion level (at 70%, two-tailed binomial test, p<0.05).
23
5 Discussion
5.1 Odor discrimination with structurally related aliphatic odorants
The results of the present study show that Asian elephants are able to
discriminate between structurally related aliphatic ketones, alcohols,
aldehydes and carboxylic acids. Further, the results show a positive
correlation between discrimination performance and structural similarity of
the odorants in terms of differences in carbon chain length.
The same odorants have previously been tested with humans (Laska and
Teubner, 1998, 1999; Laska and Hübener 2001), squirrel monkeys (Laska
et al. 1999a), South African fur seals (Laska et al., 2010), mice (Laska et
al. 2007; Laska et al. 2008), and honeybees (Laska et al. 1999). This
allows for direct comparisons of olfactory discrimination performance
between species.
Humans have well-developed olfactory discrimination ability when it
comes to aliphatic alcohols, aldehydes, ketones and carboxylic acids. The
human subjects succeeded in discriminating between all odor pairs that
were also tested with the elephants (Laska and Teubner 1998; Laska and
Teubner 1999; Laska and Hübener 2001). Similar to the elephants, a
positive correlation between human discrimination performance and
structural similarity of the odorants in terms of differences in carbon chain
length was found. This means that the human subjects indeed had more
difficulties to discriminate odor pairs that differed by only one carbon atom
than those that differed by two or three carbon atoms (Laska and Teubner
1999).
Squirrel monkeys have been tested with aliphatic alcohols, aldehydes,
ketones and carboxylic acids in previous studies (Laska and Teubner 1998;
Laska et al. 1999a). The squirrel monkeys managed to discriminate above
chance level between all odor pairs tested for the aliphatic alcohols,
aldehydes, ketones and carboxylic acids, which were also tested with the
elephants. With all four classes that were tested, a significantly positive
correlation was found between discrimination performance and structural
similarity of the odorants in terms of differences in carbon chain length.
South African fur seals have been tested with aliphatic alcohols, aldehydes,
ketones and carboxylic acids in a previous study (Laska et al., 2010). The
South African fur seals were able to discriminate between all odor pairs
tested for aliphatic alcohols, aldehydes, ketones and carboxylic acids that
were also tested with the elephants, suggesting that South African fur seals
have a well-developed ability to discriminate between structurally related
aliphatic odorants. There was no statistically significant correlation
24
between discrimination performance and structural similarity of the
odorants in terms of differences in carbon chain length. Only a
nonsignificant trend was observed towards a positive correlation with the
alcohols.
CD-1 mice have been tested with aliphatic alcohols, aldehydes, ketones and
carboxylic acids (Laska et al. 2007; Laska et al. 2008). All mice managed
to significantly discriminate between all odor pairs tested. A significant
positive correlation was found between discrimination performance and
structural similarity of the odorants in terms of differences in carbon chain
length in aliphatic ketones but not with alcohols, carboxylic acids and
aldehydes (Laska et al. 2008) which is not the same as for the Asian
elephant. In the study only addressing aldehydes (Laska et al. 2007) a
significant positive correlation was found between discrimination
performance and structural similarity of the odorants in terms of
differences in carbon chain length. These two studies suggest that CD-1
mice have well-developed discrimination ability for aliphatic odorants.
Honeybees have been tested with aliphatic alcohols, aldehydes and ketones
in a previous study (Laska et al. 1999). The results show that there is a
significant positive correlation between discrimination performance and
structural similarity of the odorants in terms of differences in carbon chain
length with all three classes tested. The odor pairs that differed by only one
carbon atom were significantly more difficult to discriminate than odor
pairs that differed by two or three carbon atoms which is in agreement with
the Asian elephants.
When comparing the Asian elephants with other species tested previously
on the same aliphatic odor pairs, the results show that Asian elephants are
at least as good at discriminating aliphatic alcohols, aldehydes, ketones and
carboxylic acids as other animals. This is not surprising since they strongly
rely on their sense of smell (Greenwood et al., 2005; Langbauer 2000;
Rasmussen 2006; Rasmussen and Krishnamurthy 2000; Scott and
Rasmussen 2005; Schulte and Rasmussen 1999; Sukumar 2003). All
aliphatic odorants tested here are found in nature and are likely to be a part
of the Asian elephant’s chemical environment. Some of the aldehydes,
ketones, alcohols or carboxylic acids have also been reported in the
temporal gland secretions of male elephants in musth and in the urine of
females (Rasmussen et al. 1990; Rasmussen, et al. 1997; Rasmussen, 1998;
Rasmussen and Krishnamurthy 2001; Rasmussen and Wittemyer 2002;
Rasmussen et al. 2005).
25
5.2 Odor discrimination with enantiomers
The results of the present study show that Asian elephants are able to
discriminate between all enantiomeric odor pairs tested.
The same odorants have previously been tested with humans (Laska and
Teubner 1999), squirrel monkeys (Laska et al. 1999b; Laska et al. 2005),
pigtail macaques (Laska et al. 2005), South African fur seals (Kim 2012),
mice (Laska and Shepherd 2007), honeybees (Laska and Galizia 2001;
Laska et al. 1999) and SD/LE rats (Linster et al. 2001; Rubin and Katz
2001). This allows for direct comparisons of olfactory discrimination
performance between species.
Table 5 shows an across-species comparison of discrimination performance
with enantiomers. Table 5: Across-species comparison of discrimination performance with enantiomers. The “+”-symbol stands for a species being able to discriminate between the enantiomeric pair, the “-“-symbol stands for a species not being able to discriminate between the enantiomeric pair and the empty space means that the enantiomeric pair was not tested with this species. The numbers in brackets show how many out of the total number of animals tested with each species succeeded in discriminating between the given enantiomers.
Asian elephant
South African fur seal
CD-1 mice
Human subjects
Squirrel monkeys
Pigtail macaques
Honey bees
SD/LE rats
limonene +
(3/3)
-
(0/3)
+
(8/8)
+
(18/20)
+
(6/6)
+
(3/3)
+
(6/6)
+
(11/11)
carvone +
(3/3)
+
(3/4)
+
(8/8)
+
(17/20)
+
(5/6)
+
(3/3)
+
(5/6)
+
(6/6)
dihydrocarvone +
(3/3)
+
(3/4)
+
(8/8)
+
(16/20)
+
(4/4)
+
(3/3)
dihydrocarveol +
(3/3)
+
(4/4)
+
(8/8)
+
(18/20)
+
(4/4)
+
(3/3)
isopulegol +
(3/3)
-
(1/3)
+
(8/8)
-
(3/20)
-
(0/4)
+
(3/3)
limonene oxide +
(3/3)
+
(3/3)
+
(8/8)
-
(4/20)
-
(0/4)
-
(0/3)
camphor +
(3/3)
-
(1/4)
+
(8/8)
-
(4/20)
-
(0/6) -
(1/6)
fenchone +
(3/3)
+
(4/4)
+
(8/8)
-
(5/20)
+
(5/6) -
(0/6)
+
(6/6)
rose oxide +
(3/3)
-
(0/4)
+
(7/8)
-
(2/20)
-
(0/6) -
(0/6)
menthol +
(3/3)
+
(3/3)
+
(8/8)
-
(5/20)
-
(3/6) +
(6/6)
beta-citronellol +
(3/3)
-
(2/4)
+
(8/8)
-
(8/20)
-
(3/6) +
(6/6)
alpha-pinene +
(3/3)
+
(3/3) +
(18/20)
+
(6/6) +
(6/6)
26
The Asian elephants were able to discriminate all enantiomeric pairs tested
(12/12) which is as good as the CD-1 mice, who also managed to
discriminate all enantiomeric pairs tested for this species (11/11).
The South African fur seal managed to discriminate seven out of twelve
enantiomeric pairs showing that they are not as capable of discriminating
enantiomers as the Asian elephants and mice. The SD/LE rats managed to
discriminate all three enantiomeric pairs tested with this species which
suggests well-developed olfactory discrimination ability. Human subjects
discriminated five out of twelve enantiomeric pairs while squirrel monkeys
discriminated six out of twelve enantiomeric pairs. These two species are
able to discriminate the same enantiomeric pairs except fenchone. The
results for humans and squirrel monkeys demonstrate a very similar pattern
of discrimination performance. This is not surprising since these two
species are phylogenetically closely related and are likely to share many
molecular odor receptors (Rouquier et al. 2000). Pigtail macaques
discriminated five out of six enantiomeric pairs also showing a high degree
of similarity of discrimination performance to humans and squirrel
monkeys. Honeybees discriminated five out of eight enantiomeric pairs.
Several insect pheromones are single enantiomers making it important for
insects to be able to discriminate between certain enantiomers (Laska and
Galizia 2001).
Asian elephants and CD-1 mice are able to discriminate all enantiomeric
odor pairs tested here. This supports the idea that these animals strongly
rely on their sense of smell and thus have a highly evolved olfaction
system.
Elephants use their trunk to be able to detect both enantiomeric forms of
the pheromone frontalin. A study showed that Asian elephants release the
(+)- and the (-)-form of frontalin in a specific ratio that depends on the
elephant’s stage in musth and its age (Greenwood et al. 2005). The
reactions to frontalin from both male and female conspecifics were
different depending on its ratio, proposing that Asian elephants are able to
detect molecular chirality and use it for social communication.
Several of the enantiomeric pairs tested here such as carvone, limonene and
alpha-pinene are found in a variety of food plants (König et al. 1990;
Mosandl et al 1990) which may explain why a plant eating species as the
elephant is able to recognize and discriminate them. Enantiomers such as
rose oxide, for which only one of the two forms has been found in nature,
in contrast, are almost never found in essential oils (König et al. 1990;
Mosandl et al 1990). This is also shown by the discrimination performance
where several species had difficulties discriminating it.
27
5.3 Long-term odor memory
The results of the present study show that Asian elephants can remember
the reward value of odorants after recesses of three weeks and one year.
The Asian elephants showed no sign of forgetting, supporting the idea that
they do have a very good long-term memory for odors. Arvidsson et al
(2012) was the first to test the long-term odor memory in Asian elephants
with two-, four-, eight- and 16 week recesses in which the animals showed
a remarkably good long-term memory.
Other species such as spider monkeys (Laska et al. 2003), squirrel monkey
(Laska and Hudson 1993), pigtailed macaques (Hübener and Laska 1998;
Hübener and Laska 2001) and South African fur seals (Laska et al. 2008)
have also been shown to have a good long-term odor memory although
only recesses up to 15 weeks were tested.
Elephants are able to recognize members of their family by taking a sample
of the urine and transfer it from the trunk tip to the vomeronasal organ,
which is located at the roof of the mouth (Rasmussen and Munger, 1996).
This allows the elephant to evaluate and detect the chemical signals in the
urine. Since elephants are long-lived it is near at hand to assume that they
should also have a good long-term memory to be able to survive in nature.
They have to travel over long distances and should benefit from
remembering details of the environment, e. g. water and food resources
(Hart and Hart 2007; Hart et al. 2008) but they should also be able to
recognize individuals from the social group. There are even suggestions
that individuals can recognize their own mother by the smell of her urine
even if they have been separated from her up to 27 years (Bates et al.
2008b).
There are only a few studies that have tested the long-term memory in
elephants with other senses (Irie and Hasegawa 2009). Elephants
demonstrated a good long-term memory in visual discrimination tasks with
symbols, after one year of recess (Rensch, 1957). Markowitz et al (1975)
retested a captive Asian elephant in a visual discrimination task after eight
years of recess and the animal showed very good memory. She needed only
six minutes to reach the criterion of making 20 correct decisions in a row,
with only two errors made, showing that she did not have any problems
remembering what she had learned many years ago. Auditory memory of
elephants has been shown by McComb et al. (2000) to be very good.
Members of a family group of wild African elephants were able to
recognize the calls of group members that had been absent for two to
twelve years. The elephants responded in the same way when hearing the
calls from these absent members as for the present group members. The
family group showed no such response to sounds from unknown elephants
28
or from unrelated family groups. This finding suggests that elephants do
have an outstanding long-term auditory memory.
The results of the long-term odor memory tests in this present study
support the notion that elephants do have an excellent long-term memory.
5.4 Theoretical explanations for the good odor discrimination in Asian
elephants
Asian elephants have been shown to have very good olfactory
discrimination ability for both aliphatic odorants and enantiomeric odor
pairs. There are three different theoretical explanations for this.
The first explanation involves the functional genes coding for olfactory
receptors. Some authors suggest that the higher the number of functional
genes one has for olfactory receptors, the better one can distinguish
between different odorants. Humans, for example, have around 390
functional genes coding for olfactory receptors (Glusman et al. 2001).
Squirrel monkeys have about 900, rats about 1200, mice about 1000 and
pigtail macaques have around 700 (Rouquier et al. 2000; Gilad et al. 2004;
Godfrey et al. 2004) functional genes. Studies have indicated that the
number of receptor types may correlate with discrimination performance
(Laska and Shepherd 2007). Honeybees have been shown to have only 160
(Robertson and Wanner 2006) although they also were able to distinguish
between aliphatic aldehydes, alcohols, ketones and some enantiomers
(Laska and Galizia 2001; Laska et al. 1999). This suggests that the number
of functional genes may not be the only factor important for discrimination
performance. For the Asian elephant the number of functional genes for
olfactory receptors has yet not been determined. However, the African
elephant has recently been shown to have around 1500 functional genes
coding for olfactory receptors (Suwa et al. 2011) which is more than in the
mouse, honeybee, human and squirrel monkey. Since phylogenetically
closely related species usually have a similar number of functional genes
for olfactory receptors (Nei et al. 2008) this suggests that the Asian
elephant may also have a similarly high number of functional olfactory
receptor genes.
The second theoretical explanation for very good olfactory discrimination
ability is that it may correlate with the size of the olfactory brain or
olfactory bulbs.
Humans, squirrel monkeys and pigtail macaques differ in the relative size
of their olfactory structures of the brain. Squirrel monkeys have the largest
29
relative size of the olfactory bulbs followed by pigtail macaques and
humans (Stephan et al. 1988).
A recent study found that the olfactory bulbs of the African elephant have
an unusual feature in that their glomerular layer is composed of two to four
layers of glomeruli while the typical olfactory bulbs from mammals have
one to two layers of glomeruli. This suggests an unusually high
connectivity between the secondary neurons such as tufted and mitral cells
and the olfactory receptors (Ngweny et al. 2011).
The third theoretical explanation for very good olfactory discrimination
ability has to do with the behavioral relevance of the sense of smell. It is
near at hand to assume that species that rely to a high degree on their sense
of smell should also have a very good sense of smell. Humans, for
example, do not rely on their sense of smell as much as, for example, Asian
elephants. For the Asian elephant a well-developed sense of smell is
important in foraging, but is also used in a social context. Chemical
communication has been studied in elephants and is considered as a vital
mechanism in regulating the behavior of elephants (Rasmussen 1998;
Rasmussen 1999; Rasmussen and Krishnamurthy 2000). The complex
society of the Asian elephant requires a well-functioning communication
system to be able to identify potential mates and to be able to keep group
cohesion. This is all done by chemical signals and vocalization (Langbauer
2000, Sukumar 2003). The Asian elephant releases chemical signals
through secretions from different glands but also in urine and breath
(Rasmussen and Krishnamurthy 2000) and these are processed by the
vomeronasal and olfactory systems by other individuals. The signals are
important in recognizing individuals but they also tell the receiver about the
social status of the emitter (Schulte and Rasmussen 1999; Greenwood et al.
2005).
5.5 Conclusions
The present study shows that these three Asian elephants are able to
discriminate between all structurally related aliphatic odorants and all
enantiomeric odor pairs tested. The discrimination performance of the
elephants concerning structurally related aliphatic odorants increased with
decreasing structural similarity of the odorants. The Asian elephants are at
least as good, or better, at discriminating among aliphatic odorants and
among enantiomeric odor pairs as other species. The long-term odor
memory of the Asian elephant was shown to be outstanding as the animals
successfully remembered the reward value of a previously learned odor
30
pair after one year of recess. The next logical step would be to assess the
olfactory sensitivity in the Asian elephant.
6 Acknowledgements
I would like to thank my supervisor, Professor Matthias Laska for great
help and support throughout this thesis project. I would also like to thank
the elephant caretakers, Stefan Aspegren, Andreas Levestam, Tommy
Karlsson, Stefan Mattson and Erik Andersson at Kolmården Wildlife Park
for the invaluable help that made this work possible.
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