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Detection dogs recognize pheromone from spruce bark beetle and follows it to source: A new tool from chemical ecology to forest protection

Conference Paper

Detection dogs recognize pheromone from spruce bark beetle and follows it to source: A new tool from chemical ecology to forest protection

Abstract and Figures

Chemical ecology has already provided tools for monitoring, mass-trapping, and relocation of forest insects, especially in conifer bark beetles. Here we demonstrate the use of detector dog to be effective for finding and locating spruces that has been recently infested by the European spruce bark beetle (Ips typographus L.), one of the most aggressive forest pests. For active beetle management, attacked trees must be promptly removed (weeks) but are difficult to spot. Humans, who rely on visual cues for target identification of recent tree kills (still green), need to approach within <1 m, dogs use primarily olfactory cues and can therefore locate remote targets that are not visually obvious. The ability to search for target odour and then go to its source makes dogs ideal for rapid target recognition in field settings. Dogs are trained on synthetic pheromone components, from both early and late stage attacks, on an educational platform (video) and later on trees before beetle swarming. Dog movement and detection distance data were collected during experiments with GPS. After beetle flight started, the dogs showed rapid and accurate orientation to single or groups of trees attacked, often over >50 m distance (video). We observed detection distances ranging from 0.5 m to 150 m. Attacks of different ages (day –weeks) and standing or wind-felled trees were all detected. Scents from synthetic pheromone blends or natural pheromone seemed equally detectable for the dog. Detection limits and training of groups of private non-search dogs with their owners will be discussed. Further applications may include detection of low-level attacks of alien or recently introduced pest insects.
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RESEARCH PAPER
Using synthetic semiochemicals to train canines to detect bark
beetleinfested trees
Annette Johansson
1,2
&Göran Birgersson
1
&Fredrik Schlyter
1,3
Received: 10 December 2018 /Accepted: 23 April 2019
#The Author(s) 2019
Abstract
&Key message The dog detection allows timely removal by sanitation logging of first beetle-attacked trees before offspring
emergence, preventing local beetle increases. Detection dogs rapidly learned responding to synthetic bark beetle phero-
mone components, with known chemical titres, allowing search training during winter in laboratory and field. Dogs
trained on synthetics detected naturally attacked trees in summer at a distance of > 100 m.
&Context An early detection of first beetle-attacked trees would allow timely sanitation felling before offspring emergence,
curbing local beetle increase.
&Aims We tested if detection dogs, trained off-season on synthetic pheromone components from Ips typographus, could locate
naturally bark beetleinfested spruce trees.
&Methods Indoor training allowed dogs to discriminate between the infestation odours (target) and natural odours (non-target)
from the forest. Odour stimuli were shown by chemical analysis to be bioactive at extremely low-levels released (< 10
4
ng/
15 min) in the laboratory.
&Results Detection dogs, trained to recognise four different synthetic pheromone compounds in the wintertime, were able to
detect naturally infested spruce trees unknown to humans the following summer. The dog-handler pairs were able to detect an
infested spruce tree from the first hours of beetle attack until several weeks after first attack, long before discolouration of the
crown. Trained sniffer dogs detected infested spruce trees out to 100 m, as measured by GPS-collar tracks.
&Conclusion Dog-handler pairs appear to be more efficient than humans alone in timely detecting bark beetle infestations due to
the canines ability to cover a greater area and detect by olfaction infestations from a far longer distance than can humans.
Keywords Ips typographus .Gas chromatographymass spectrometry extracted ion chromatograms .Detection dog .Sanitation
logging .Forest protection .Norway spruce
1 Introduction
Detection dogs are used to locate many objects including
humans, explosives, and illicit drugs (see Browne et al. 2006
and references therein; Lorenzo et al. 2003). Trained canines
have also been used to detect invasive organisms (Goodwin
et al. 2010; Hoyer-Tomiczek et al. 2016)aswellasendan-
gered species (reviewed by Beebe et al. 2016). Canines have
also been trained to detect small or cryptic insects such as
termites (Brooks et al. 2003), palm weevils (Nakash et al.
2000;Sumaetal.2014), bed bugs (Pfiester et al. 2008;
Vaidyanathan and Feldlaufer 2013), and endangered
Coleoptera (Mosconi et al. 2017). The key benefits of using
trained detection dogs are their keen sense of smell (Hepper
and Wells 2015) and their ability to cover large areas in a
shorter time when compared with humans (Mosconi et al.
Handling Editor: Aurélien Sallé
Contribution of the co-authors AJ and FS designed research; AJ and
GB collected data; AJ, GB, and FS analysed data; all authors contributed
to the writing process. All authors read and approved the submitted
version.
*Fredrik Schlyter
fredrik.schlyter@slu.se
1
Department of Plant Protection Biology, Swedish University of
Agricultural Sciences, PO Box 102, SE-230 53 Alnarp, Sweden
2
SnifferDogs Sweden, Bäckvägen 26, SE-342
93 Hjortsberga, Sweden
3
Present address: Excellent Team for Mitigation, Faculty of Forestry
& Wood Science, Czech University of Life Sciences Prague,
Kamycka 129, 16521 Prague 6, Czech Republic
Annals of Forest Science (2019) 76:58
https://doi.org/10.1007/s13595-019-0841-z
2017). In most cases, biological material is used for the train-
ing (Johnen et al. 2013).
The European spruce bark beetleIps typographus (L.)
is one of the mostdestructive forest pests in Europe (Grégoire
and Evans 2004). For forest protection, the rapid detection of
bark beetle infestations is required to successfully implement
a management strategy that relies upon removing recently
infested trees within 23 weeks of attack (Svensson 2007).
However, human detection generally requiresclose inspection
(1 m) of trees and is therefore time-consuming, costly, and
not always practical. Therefore, detection generally occurs 2
3 months after an infestation in north Europe, when tree crown
colour fades and bark falls off. By this time, most bark beetles
have left the infested tree and may attack other, non-infested
trees. Since a rapidly changing, but specific series of beetle
pheromone components and other semiochemicals are present
for several weeks after an initial attack, the use of detection
dogs may prove a better alternative than human inspection.
Upon attacking a tree, male bark beetles secret an aggregation
pheromone, consisting of a blend of 2-methyl-3-buten-2-ol
and cis-verbenol (Birgersson et al. 1984). A few days later,
an inhibitory signal (consisting mainly of ipsdienol) is emitted
when bark beetle females have begun laying eggs (Birgersson
et al. 1984; Schlyter et al. 1987). After the first week, an
additional chemical cue, indicating that the infested tree is
fully utilised and competition is high, is evident. This semio-
chemical, verbenone, is an oxygenation product by the beetle
and by the interaction of fungi and bacteria with damaged tree
phloem (Leufvén and Birgersson 1987; Schlyter et al. 1989).
In this proof of concept study, we tested if rapid laboratory
training of detection dogs on a series of synthetic semiochem-
icals associated with bark beetle infestations would allow
these trained dogs to later detect and locate bark beetle
infested trees of different ages in the field. Since the semio-
chemical profile of attacked trees changes rapidly in both the
quality and quantity of semiochemicals released over several
weeks (above), we chose to use four synthetic chemical com-
pounds as stimuli, representing the four major cues emitted
over the weeks of insect attack, in our canine training. We
hypothesised that dogs field-trained on this series of synthetic
pheromones in the winter months could later locate infested
trees from several weeks past in the summer months. Finally,
we tested the hypothesis that a trained dog can detect natural
infestations from distances further away than a human can (10
to 100 times).
2 Materials and methods
2.1 Canines
Two dogs, owned by SnifferDogs Sweden (Hjortsberga,
Sweden), were used in this study. Dog A was a 9-year-old
female German shepherd that previously trained as a search
and rescue dog for humans. Dog B was a 1-year-old female
Belgian shepherd (Malinois) that had only basic obedience
training and had no previous formal detection expertise.
2.2 Chemicals
Synthetic bark beetle pheromones used in this study included
methylbutenol (2-methyl-3-buten-2-ol; Acros Organics,
Gothenburg, Sweden), 4S-cis-verbenol (Borregard,
Sarpsborg, Norway), and ipsdienol (ICN/MP Biomedicals,
USA). Synthetic verbenone, a bark beetle pheromone and a
product of the host tree, was obtained from Fluka (Sigma-
Aldrich, Stockholm, Sweden). Other chemicals used in the
study were obtained from our chemical stocks (see
Andersson et al. 2012).
Each pheromone component was stored separately in sep-
arate jars of glass to avoid cross-contamination of odours. In
each jar of glass, a cotton pad (ICA Basic Bomullsrondeller,
Netherlands) was placed in the bottom and a small amount of
each semiochemical was dropped on to the cotton pad (10 μl
methylbutenol, 10 mg cis-verbenol, 1 μlipsdienol,or10μl
verbenone). The glass jars were then filled with cotton pads,
and so molecules in gas phase of each component passed
passively by aeration transfer in the closed jar via adsorption
of the odour to the pads placed above (Hudson-Holness and
Furton 2010). The glass jars were stored in a freezer (≈−
18 °C).
For determination of release rates by GC-MS and corre-
sponding dog training response (Fig. 1; Table 1), we always
used the cotton pads from the top in each glass jar. The last
five cotton pads in the glass jars were never used but filled up
with new pads when needed. A cotton pad holding the semio-
chemical (Hudson-Holness and Furton 2010) was placed in a
stainless steel tin (5 cm dia.) with perforated lids (Ströare,
Biltema®, Helsingborg, Sweden). For release rates by GC-
MS and dog training response study, we prepared five steel
tins of each synthetic pheromone at the same time. These tins
were stored in room temperature (+ 20 °C). Release rates
were determined using odour collections similar to Zhang
et al. (2000). An inverted glass funnel (5 cm dia.) was placed
above the steel tin and air was drawn through a column packed
with Porapak ® Q (25 mg mesh 6080; in a Teflon tube 3 mm
i.d.) at 100 ml/min at 15 min intervals (Photos and text
ESM_0 in Johansson et al. (2019)). Compounds were eluted
from the column with 400 μl pentane (Sigma-Aldrich,
Steinheim, Germany) into a 400-μl insert placed in a 2-ml
screw-top vial (Agilent Technologies, Böblingen, Germany),
and 1 mg heptyl acetate was added as internal standard.
Aeration extracts were analysed by gas chromatography-
mass spectrometry (GC-MS; Agilent 6890-5975, Agilent
Technologies, Santa Clara, CA, USA) with techniques previ-
ously reported (Birgersson et al. 1984). Quantifications were
58 Page 2 of 10 Annals of Forest Science (2019) 76:58
based on extracted ion chromatograms of prominent frag-
ments for each tested compound and the internal quantifica-
tion standard, respectively. The limit of quantification (LOQ)
in the analytical procedure was < 0.1 ng/min.
2.3 Laboratory tests
Initially, dog A was introduced to the bark beetle phero-
mones using the synthetic odour from a commercial dis-
penser, ETOpheron ® (Pheronova AG, Switzerland),
which is used in bark beetle monitoring traps. Because of
the dispensersconstruction of fabric with a plastic shell, it
was not certain that the dog only learned the scent of the
pheromone components as the target odour, or if it learned
any other odour of the dispenser materials. One may inad-
vertently train a dog to detect an unexpected or impure
source when attempting to train to a pure compound. To
be sure that the dog learned the right odours, we subse-
quently trained the dog on pure synthetic semiochemicals
applied to cotton pads (above). Non-target odours that
could disturb search were also used in the training and
consisted of items found in a forest setting such as vegeta-
tion odours from spruce needles, cones, resin, bark, moss,
and animal odours (i.e. scent from feathers, fur, hoofs, and
faeces). All non-target (disturbance) odours were collected
in the forest or donated by local hunters (fur and hoofs
from moose, deer, and boar). Both target and non-target
odours were stored in jars of glass and transferred by aer-
ation to cotton pads to ensure that the background odour of
cotton was present in both target and disturbance odours.
The training platform used (Figure ESM_1 and video
in ESM_4_V1 from Johansson et al. (2019)) was devel-
opedbyStigMeierBergandGeirKojedal,Spesialsøk,
Selbu, Norway, based on an idea from Hundcampus,
Hällefors, Sweden (Fischer-Tenhagen et al. 2011). It is
designed to let the dog work independently, to minimise
the cues from the handler, and to be easily manoeuvred by
the handler creating a more effective learning situation
with a high rate of opportunities to reward the dog for
desired behaviour. Disturbance odours (non-target
scents) were presented together with one or several target
stimuli in a movable tray with seven positions (Figure A
in ESM_2 from Johansson et al. (2019)). To compare
different stimulus linear layouts, mixing target and non-
target scent, on the movable tray, the two dogs were tested
in three trials with each stimulus layout.
For evaluation of the dog detection performance with
decreasing amounts of odour molecules over time, nine
trials were conducted to evaluate the dogsidentification
performance with each synthetic semiochemical. For these
trials, we used four of the prepared five steel tins contain-
ing cotton pads with synthetic semiochemical. Since the
trials were conducted over several days (184hafterthe
cotton pads were placed in the tins and stored in room
temperature), we used a new tin every day. This was done
to make sure that the tins were not contaminated with any
other scents such as odour from the dogs. Every trial ses-
sion lasted for approximately 1 min (5070 s).
a
b
Fig. 1 Correct responses in relation to estimated stimuli evaporation
rates. aCorrect positive responses to stimuli (compounds) with estimated
release rates per 15 min over 3 days of testing. No effect of time for all
stimuli joined (r
2
0). bCorrect negative responses to stimuli with
known releases per 15 min over 3 days of testing. Weak effect of time
for all stimuli joined (r
2
= 0.18). Separately, MB shows the strongest
effect (r
2
= 0.85) followed by Vn (r
2
=0.48). Chemical data from
Table 1. The responses of the two dogs are pooled here, separate data in
Supplementary Table (ESM_3 from Johansson et al. 2019).
Semiochemical acronyms: MB, methylbutenol; cV, 4S-cis-verbenol; Id,
Ipsdienol; Vn, ()-verbenone
Annals of Forest Science (2019) 76:58 Page 3 of 10 58
2.4 Outdoor tests
To train the dogs to pinpoint the target odour source out-
doors, pieces of the cotton pads containing synthetic pher-
omone odours as those used for platform training were
hidden in cracks of the bark of several species of trees.
The cotton pieces were placed in the height of the nose
of the dogs and the dogs were shown where to sniff for
the target (video ESM_4_V2 from Johansson et al.
(2019)). When the dog found the cotton piece holding the
target odour, it was immediately rewarded by a clicker
sound and a piece of food delivered between its nose and
the odour source. Several pieces of cotton with either target
or non-target odours were put in cracks of the bark in a
small area (30 × 30 cm) to ensure the dogs did not use
visual cues for close-range target location. When the dog
understood the game, consistently (~ 100%) locating the
pads, the height of the placement was gradually increased
up to 1½ m aboveground and only cotton pads with target
odour were used. The dog was sent from longer distances
to locate the tree in which the cotton pad was put. Because
the cotton pads contain very low concentrations of the syn-
thetic substance and emit very little odour, the pads were
replaced with commercial dispensers as the dog became
more skilled for the task. The fresh dispensers used in traps
emit several orders of magnitude odour molecules than
pads and for a longer period of time. By using the dis-
pensers, the dog could recognise the target odour from a
greater distance and must practise its search technique
while working its way upwind in the vapour plume to-
wards the source.
Dogs were trained in the winter under a variety of weather
conditions (e.g. rain, snow, sun).
Training trials using synthetic odour were conducted on
average once a week during 2009 and 2010. The temperature
ranged from 2 to 28 °C. The handler determined the search
strategy to best cover the assigned area based on wind condi-
tions and terrain. These protocols were employed to simulate
future practical field survey conditions.
A first proof-of-concept test, evaluating the detection by
dogs of spruces that were known to be recently attacked by
bark beetles, was conducted at the Nature Reserve of Notteryd
(near Växjö, Småland, Sweden). The area consisted of wind-
felled trees and standing healthy spruces. In the spring of
2009, 95% of all spruces in the reserve were already killed
by bark beetles. The remaining spruces that were still alive
stood together in clusters of 1015trees. We felt these circum-
stances made this particular Nature Reserve an optimal area to
first try the dogs on natural attacks. Another series of tests
were conducted at a production-forest in Nottebäck, also near
Växjö, Småland, Sweden, with the permission of the owner of
the forest. The dog team consisted of one dog (dog A) work-
ing off-leash and one handler and searched three different
Table 1 Estimated release rates from cotton pad on days one to three
Compound/
stimuli
Molecular weight
(g/mol)
Vapour
pressure
(Pa,
25 °C)
a
Regression,
r
2
Regression,
n
Estimated
emission
(ng/15 min)
at end
of day 1
Estimated
emission
(ng/15 min) at end
of day 2
Estimated
emission (ng/
15 min) at
end of day 3
Estimated emission
(molecules/s) at
end of day 1
Estimated emission
(molecules/s)
at end of day 2
Estimated emission
(molecules/s)
at end of day 3
Methylbutenol,
new pad
86.1 3053 0.97 8 3.0E01 9.7E03 3.6E04 1.6E+17 5.8E+15 2.1E+14
Methylbutenol,
old pad
86.1 3053 0.81 11 1.3E02 2.9E05 6.6E08 7.9E+15 1.8E+13 0.0
cis-Verbenol 152.2 4.4 0.85 6 1.1E01 1.8E03 3.1E05 3.4E+16 6.0E+14 1.1E+13
Verbenone 150.2 10.3 0.35 5 1.8E+00 1.2E01 1.3E02 3.6E+17 4.0E+16 4.5E+15
Ipsdienol 152.2 1.3 0.98 3 1.6E05 3.7E11 0.0 5.6E+12 0.0 0.0
Based on calculations by exponential regression of vapour phase concentrations data over pads from aerial entrainment on Porapak ® Q on day one (Zhang et al. 2000)
IUPAC names: 2-Methyl-3-buten-2-ol, (4S)-4,6,6-trimethylbicyclo[3.1.1]hept-3-en-2-ol, (1S,5S)-4,6,6-trimethylbicyclo[3.1.1]hept-3-en-2-one, and 2-Methyl-6-methylene-2,7-octadien-4-ol
a
Vapour pressure at 25 °C derived from www.chemspider.com estimates
58 Page 4 of 10 Annals of Forest Science (2019) 76:58
areas in the production forest attacked by bark beetles in pre-
vious years. The handler had knowledge of the location of
former attacks, but no information on new attacks. The dog
and handler searched each area with no time limit. The han-
dlers determined their search strategy to best cover the
assigned area based on wind and terrain. These protocols were
employed to simulate expected future practical field survey
conditions.
Dog and handler movements were recorded using glob-
al positioning systems (GPS) in 5-s intervals in all field
trials. These data allowed identification of the point at
which the dogs lifted their nose up in the air and made
a sudden change in direction of travel and moved directly
towards an infested spruce (video of search using GPS;
ESM_4_V3 from Johansson et al. (2019)). The GPS units
used in the study were Garmin Astro® 220 Nordic hand-
set and Garmin DC30 dog collar (Garmin Corporation,
Taiwan). The map used in the handset was Garmin
Friluftskartan Pro V2 Götaland. The data from the
GPS unit were transferred to a PC with Garminssoftware
MapSource. Using the measuring tool, we could measure
the distance from where a track from the dog changed
direction to the waypoint where the dog alerted on an
infested spruce.
2.5 Field trialdetection distance from natural
sources
We used 20 different areas, whereof 10 were located in
naturereservesand10inproductionforests,withpermis-
sion of the owners and from The Swedish Forest Agency in
Växjö in 2010. All areas were 24haandtestsweredone
in three different set-ups: (a) 10 search areas with location
of infestations known by handler, (b) 5 areas with location
of infestations known by the forest manager, and (c) 5
areas with location of infestations unknown, but were con-
sidered as risk areas with bark beetlesinfestations on pre-
vious seasons.
To design the best search strategy for long distance
detection, based on wind, terrain, and the location of the
attacks, the dog handler had prior knowledge of attacks in
the 10 first areas. To estimate if the dog handler might
involuntarily cue the dog to an odour source (an infested
tree), the dog handler was not allowed prior knowledge of
attacks in the 10 latter areas.
3 Results
3.1 Laboratory training
The two dogs were successfully trained to recognise the four
different synthetic semiochemical compounds on the
educational scent platform (video ESM_4_V1 from
Johansson et al. (2019)). Both dogs learned to recognise a
new target scent in just one training trial, similar to Johnston
(1999). In that time, the dogs managed to sample the tins for
target odour about 30 times on average. Occasionally, the dogs
reacted with an increased interest when a new non-target dis-
turbance odour was presented. When this happened, the handler
stood silent and just waited until the dog stopped investigating
the new non-target odour and, if the dog did not continue to
search by itself, gave the dog a new command to start sampling
the other tins again. After a few encounters with the new non-
target odour, the dogsinterest decreased since they learned that
there would not be any reward for that particular odour. Even
though the dogs were interested in new disturbance odours
(mostly edible items like cookies and chips or scents from other
animals), the handler did not record such behaviour as an alert.
When alerting on a target odour, both dogs stopped sampling,
and waited for their reward, in contrast to increased sampling a
tin in order to investigate a disturbance odour.
3.2 Chemical stimulus strength
Chemical quantification by odour collection and GC-MS was
at start routine with a limit of quantification (LOQ) of <
0.1 ng/min. However, 2 days later, we found that most stimuli
titres, still well biologically active, decreased to below the
LOQ. Using estimates based upon linear regression, chemical
data indicates that by the third day, some compounds were
very close to zero (Table 1).
The dogs responded to estimated doses of 10
4
ng/15 min
releases or less. The four different semiochemicals were
learned equally well, and responses to these sub-picogram
release rates of stimuli aged up to 3.5 days remained stable
(Table in ESM_3 from Johansson et al. 2019).
3.3 Biological responses
The responses of both dogs to target odours are
summarised per target scent in the Supplementary
Table (ESM_3 from Johansson et al. (2019)). The dogs
achieved a mean of 99% correct indications; 1% of the
incorrect indications were either false positive (alerting to
a non-target odour; dog A) or false negatives at the begin-
ning of a trial session (dog B). None of the dogs sampled
all tins in every repetition. In each repetition, four tins were
presented, but the trainer could never know where the dog
would start searching or in which direction it would con-
tinue its search. The only dispenser tin always sampled was
the tin holding the target scent. This explains the high
success rate of 99% for correct positives for the target scent
(at which tin the search will stop), but the much lower rate,
55% for the correct negatives with direct sampling of emp-
ty tins before finding the target scent.
Annals of Forest Science (2019) 76:58 Page 5 of 10 58
To increase the dogs sampling of all presented tins, we tried
the dogs in different kinds of stimulus layouts with zero to
three different target odours presented in the same trial
(Figure A in ESM_2 from Johansson et al. (2019)). The only
clear effect was for the layout with no target scent, where
response decreased with time (Figure B in ESM_2 from
Johansson et al. (2019)). Other sample set-ups and target
scents had correct positives close to 100% (Table 2).
Interestingly, over the > 3 days of testing combined with
chemical sampling, the correct responses remained consis-
tently high irrespective of compound (Table in ESM_3
from Johansson et al. (2019)). The positive responses
showed no decline with estimated chemical stimulus levels
(Fig. 1a), indicating that stimulus levels were above the
animal detection limit for the whole duration of the testing
period. The correct negative responses (no alert to tins with
disturbance odours) declined with the estimated stimulus
strength, likely since the dogs learned that these odours
were not going to be rewarded (Fig. 1b).
3.4 Outdoor tests
During off-season training, dogs were introduced to cotton
pads initially placed at nose height in the cracks of the bark
in different kinds of trees (Video ESM_4_V2 from Johansson
et al. (2019)). Dog A, previouslytrained as a search and rescue
dog, just needed to come into contact with one of the newly
learned target odours to expect a reward, hence follow it to the
source and pinpoint it to its handler. Dog A also alerted the
found target source by barking. This was the trained alert
when locating a hidden human as a search and rescue dog.
Dog B, however, which had no previous search training, had
to learn how to follow the odour plume to the source. Dog B
was not trained to perform any other alert than pinpointing the
source of the target odour. This dog did not know any other
way to receive its reward but putting its nose on the target
source. The target source became a button to push to get its
reward.
Bark beetle activity began at the end of April, when the
temperature increased to over 20 °C, allowing us to test the
dogsability to detect natural pheromone from attacking
spruce bark beetles. Dog A successfully found the first spruce
that was under attack, on the first day. The spruce in question
showed no signs of the attack at first sight, but further inspec-
tion at close range revealed that the first bark beetles were
drilling their way into the spruce bark and the sound of their
drilling could also be heard. This finding was crucial in dem-
onstratingthat it is possible to train a dog ona synthetic odour
and subsequently showing that it will alert to the natural odour
under field conditions. All training of beetle detection in the
Nature Reserve was terminated at the end of May when so
many spruces were under various phases of bark beetle attack
that the smell from the attacked trees became obvious even for
the human nose.
Table 2 Evaluation of correct indications in different sample set ups with stimuli and blanks
Dog ID Sample set-up
1
Target scent Response type Stimuli age Correct indications
(n/trial) 1 h 6 h 36 h n% Mean
both dogsNumber of indications
A 1 Methylbutenol CPa (16) 16 16 16 48 100
CN (48) 32 28 31 91 63
B CP(16) 131616 459497%
CN (48) 30 27 29 86 60 61%
A 2a Methylbutenol and cis-verbenol CP (12 + 12) 24 20 23 67 93
CN (40) 23 18 17 58 48
B CP (12 + 12) 23 21 22 66 92 92%
CN (40) 17 14 22 53 44 46%
A 2b Ipsdienol and verbenone CP (8 + 8) 16 16 16 48 100
CN (48) 47 44 36 127 88
B CP (8 + 8) 16 16 16 48 100 100%
CN (48) 43 28 31 102 71 80%
A3 cis-Verbenol, ipsdienol, and verbenone CP (4 + 16 + 4) 23 22 24 69 96
CN (40) 37 40 33 110 92
B CP(4+16+4)242224 709797%
CN (40) 31 36 32 99 83 87%
1
Arrangement of positive (target) and disturbance (non-target) stimuli, see Figure A in ESM_2 (Johansson et al. (2019))
CP, correct positive; CN, correct negative
58 Page 6 of 10 Annals of Forest Science (2019) 76:58
Both dogs were also successful in locating sparser attacks
in production forest stands, where attacks were known neither
to the dog handler nor to the forest manager. In the first area
searched, dog A detected and alerted to a single, wind-felled
spruce that had been infested by bark beetles. In the second
area searched, the same dog found seven infested standing
spruces. Five of them stood together in a cluster among old
attacks. Two were located in a felling edge.
In the third area, the dog detected five infested spruces,
both standing and wind-felled. In this area, all the spruces
were located near a felling edge by a clear-felled area where
felled trap-trees were placed. The dog started its search with
detecting and alerting on the synthetic pheromones from the
trap-trees. When sent to continue its search, the dog detected,
recognised, followed, and alerted on the natural pheromones
emitted from the bark beetles in standing trees (as shown in
video ESM_4_V4 from Johansson et al. (2019)).
Quantitatively, the handler measured by GPS that a major-
ity of successfully located sources of natural pheromone were
detected within 50 m, but both dogs located sources in a be-
havioural sequence over a range of 50100 m (Fig. 2a). No
differences in detection distance by GPS could be seen among
areas with attacks (10) known or unknown (10) to the handler.
Later analysis of the GPS tracks showed seven cases where
the more experienced dog A changed direction and was able
to detect the pheromones from bark beetleattacked trees at a
distance of over 100 m (Fig. 2b). In the 20 areas visited, the
dogs found in total 193 trees infested by bark beetles in 77
different groups of attacked trees.
4 Discussion
Training canines to detect bark beetleinfested trees poses
some important limitations, including the relatively short sea-
son available for using trees at various stages of attack, as well
as the risk of inducing a full-blown tree attack by placing
pheromone for training purpose on a host tree during the ac-
tual beetle flight period. While it is probably possible to train a
detection dog to locate spruces that have been attacked by
bark beetles by just letting the dog sniff an attacked spruce
and reward the dog, such a naturalmethod will not teach a
dog to recognise the different kinds of semiochemicals the
bark beetle releases over the course of an attack. Therefore,
we chose to train the dogs to recognise a series of synthetic
pheromone compounds using an indoor training platform. In
this study, we demonstrate that canines trained on synthetic
bark beetle pheromone compounds at low (sub-picogram)
levels, indoors, can later recognise naturally produced phero-
mone over long distances, outdoors. Additionally, by using
synthetic sources of the bark beetle pheromone in the labora-
tory, it is possible to train dogs off-season long before the bark
beetles start their flight period in the field, and the dog handler
has control over which odours the dog learns, one at a time
and at very low concentrations. The indoor training of canines
also has the benefit in that other environmental distractions are
minimised, thereby allowing the dogs to concentrate on and
learn the target odours.
In the field, detection dogs thatwork over largeareas (off-
leash) can often be seen lifting their nose up in the air and
then make a sudden change in direction of travel. This likely
occurs when the dog enters an area with a detectable odour (a
plume) that the dog identifies as its trained target odour, while
the odour plume structure in a field setting, where the plume
shape, size, and persistence are highly dynamic, cannot be
easily delineated by chemical means due to the very low titres
present in open air (Murlis et al. 2000; Riffell et al. 2008). It
can, however, be indirectly observed through olfactory-
behavioural responses of animals to target odour plumes. In
our study, a trained detection dog could detect an infested
spruce tree from a distance of 150 m, which is farther away
than that estimated for bark beetles (Ips typographus)
responding to beetle pheromone dispensers (Schlyter 1992).
In training dogs to detect bed bugs (Cimex lectularius L.),
the dog usually searches (either on-leashor off-leash)the
entire roomoften several timesbefore alerting on a bed
bug. In this case, the dog handler interaction is paramount
owing to the vastly different scales of indoor room searches
(110 m) compared with free-ranging forest searches (10
500 m). Issues surrounding a close interaction between dog
and handler have been reported (Lit et al. 2011), though dur-
ing our large-scale forest searches,these issues would be min-
imal, at best. In a study of canines involved in bed bug detec-
tion, a high degree of both false positives and low true posi-
tives were found (Cooper et al. 2014).
Little, if any, studies can be found using pure, known syn-
thetic samples for canine detection purposes (Johnen et al.
2013). However, it is clear that canines can show a dose-
response to relatively low (but quantitatively unknown) doses
(Krestel et al. 1984;Polgáretal.2016; Walker et al. 2006).
Our levels of correct positives (sensitivity) and correct nega-
tives (specificity) appear high, compared to the seven studies
recently reviewed that provided such data (Johnen et al. 2013).
Hitherto, no quantitative data exist on chemical strength dur-
ing dog training in the open literature in spite of some early
attempts (Krestel et al. 1984; Walker et al. 2006). No doubt,
the dearth of chemical data is due to low thresholds for dog
response tovolatiles. While our dataare novel, we must admit
that our empirical data spans only a part of the tested range of
stimuli diminution over time, mainly the 1-day-old dispenser
material, and we had to rely on estimates from linear regres-
sion for the older material with lower releases. Still, our esti-
mates appear to be the best so far documented.
The search-and-pickmethod of detection and removal
by sanitation cuttingof bark beetleinfested trees within
23 weeks of attack (Svensson 2007) often fail because of
Annals of Forest Science (2019) 76:58 Page 7 of 10 58
the short time frame involved. Trees were often not cut and
removed from the forest until weeks or months later by
salvage cutting(Långström and Björklund 2010), long
after beetles had moved to attack other trees. Finding
spruces in an early stage of attack is also significant for
the timber value, due to a blue stain fungi the beetle intro-
duces into the newly attacked trees (Kirisits 2004).
Since the pheromone blends used by the bark beetles for
intraspecific communication vary in strength and compo-
sition over time, we importantly observed that the dogs
could detect all of the substances on which they were
trained; therefore, it makes no difference which semio-
chemical composition the bark beetles in an infested tree
is currently emitting. Thus, a trained dog will detect and
follow any of the odours, alone or in blends, to the source
and alert the dog handler. While the dog may learn addi-
tional odours that may occur when a spruce is under attack
(Birgersson and Bergström 1989; Schiebe et al. 2012), any
conclusions to this effect would be speculation on our part.
In our study, searches would often be conducted in
colder and wetter periods, in-between the short warm-
weather swarming periods of the beetle. It would be in-
teresting and of practical relevance to know more precise-
ly how different weather conditions may affect the dogs
ability to search a larger area (Soroker et al. 2017).
Another question of considerable practical importance,
but not tested in this first study, is if endemic vs. epidemic
contexts would affect the detection accuracy of dog-
handler pairs. Later experiences by us indicate that such
pairs are able to orient in stands very heavily attacked as
Wind Change of
Direction
Attacked
Spruces Dog
Trac k Handler
Track
0
2
4
6
8
10
12
14
16
0-25 26-50 51-75 76-100 101-125 126-150 >150
Number of locaons with infested trees
Detecon distance (m)
Dog A
Dog B
a
b
Fig. 2 Field GPS tracks and dog
detection distances. aTracks from
an example of handler and search
dog finding a small group of
unknown mass-attacked trees.
GPS unit track shown with
Google Earth background satellite
image over the area. Distance
from Change of Direction to the
attacked trees =158 m (distance
and tracks by BaseCamp,ver.
4.7.0, Garmin Ltd). Maps, aerial
photos/satellite images:
Copyright/Lantmäteriet, Sweden,
consent #: I2011/0096 (see dog
search and GPS unit tracking in
video ESM_4_V3 from
Johansson et al. (2019)). b
Detection distances (distance
from Change of Direction to the
attack) recorded from GPS tracks
(as above) when locating natural
bark beetle mass attacks unknown
to handler
58 Page 8 of 10 Annals of Forest Science (2019) 76:58
well as to find single-attacked trees (Johansson et al.
unpubl.). Dogs may as well in practical search orient to
pheromone in traps. For the dog, both a trap and an
attacked tree are trained target sources and are corre-
spondingly correct positive responses. The dog does not
distinguish between the two. For the dog, it is just a source
that means reward from the handler. Similarly, one may ask
what amount of stand surface that could be inspected per day,
but this cannot be quantified from the present data. Detection
of attacks higher up on the trunk is another challenge; we have
observed that a motivated and experienced dog can handle
such situations. A direct comparison to detection by humans
alone is difficult to do here, as high attacks are seen only very
late when the crown fades.
In view of the large number of pheromones identified to
date from moths, beetles, and other pests (> 1000) (El-Sayed
2019), it would seem feasible to start training detection dogs
for many pest management systems.
5 Conclusion
This is the first report of using synthetic pheromone com-
pounds at known titres to train detection dogs to detect and
locate living animals in the field. Dogs could detect and locate
the source of pest insect infestations at a distance of over
100 m or more. The use of detection dogs for early detection
of bark beetle infestations could contribute to better forest
protection by timely sanitation felling. We suggest that, in
general, use of stimuli that are biochemically well-defined in
both quality and quantity appears to hold promise for both
better practise and science in detection dog training to biolog-
ical objects, such as cryptic woodborer pests.
Acknowledgments WethankDrs.M.AnderssonandA.Bonaventura,
and Prof. O. Anderbrant, as well as Drs. Veronique Martel and Krista
Ryall, and Mr. T. Gustafsson for valuable comments on earlier ver-
sions. Special thanks to go to Dr. M. Feldlaufer (USDA, Beltsville)
for extensive suggestions on content and language. The authors thank
A. Holmström at The Swedish Forest Agency, Växjö, and the private
foresters for granting us access to field trial and search areas in nature
reserves and production forests.
Funding information This research was funded by two grants from The
Södra Foundation for Research, Development and Education,Växjö,
Sweden, to AJ. FS and GB was supported by the Linnaeus programme
Insect Chemical Ecology, Ethology and Evolution(IC-E
3
, #217-2006-
1750) at SLU and later to FS (Rapid olfactory detection of insect and
fungal damage in forests, #2013-1583) both from The Swedish
Research Council Formas. FS was further supported by EXTEMIT-K
project financed by OP RDE at Czech University of Life Sciences Prague
(CZ.02.1.01/0.0/0.0/15-003/0000433).
Data availability The datasets generated and/or analysed during the
current study are available in the Zenodo repository (Johansson
et al. 2019)athttps://doi.org/10.5281/zenodo.2605357.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflicts of
interest.
Statement on ethical approval All applicable Swedish ethic guidelines
for the care and use of animals were followed. Both dogs participating in
this study were privately owned working dogs and handled by their owners.
Disclaimer Funding sources were not involved in study design, data
collection/interpretation, or writing/submission of this report.
Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give appro-
priate credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
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58 Page 10 of 10 Annals of Forest Science (2019) 76:58
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