Forest Ecology and Management 528 (2023) 120626

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Dogs trained to recognise a bark beetle pheromone locate recently attacked

spruces better than human experts
N. Vošvrdová a, A. Johansson b, c, M. Turčáni a, R. Jakuš a, D. Tyšer a, F. Schlyter a, b, 1,
R. Modlinger a, 1, *
a
Czech University of Life Sciences, Faculty of Forestry and Wood Sciences, 16500 Prague, Czech Republic
b
Chemical Ecology, Department of Plant Protection Biology, PO Box 102, Swedish University of Agricultural Sciences, Alnarp, Sweden
c
SnifferDogs Sweden, Bäckvägen 26, SE-342 93 Hjortsberga, Sweden

A R T I C L E I N F O A B S T R A C T

Keywords: One of the most promising techniques for rapid detection of bark beetle-infested trees is the use of specially
Detection dog trained dogs. Due to the novelty of using dogs in detecting bark beetle-infested trees, evaluation of success or
Forest pest management comparison with the traditional approaches is lacking. Spruces were pre-treated with a synthetic pheromone at
Ips typographus
several tree positions in six experimental forest stands of 4–12 ha. The tree positions were selected based on their
Norway spruce
arrangement in a random scheme or in patches considered suitable for bark beetle colonisation. Three dogs of
Green attack
different ages, sex, and levels of experience in detecting Ips typographus were compared with three experienced
human bark beetle specialists. We used GPS positioning of dog tracks (unleashed), handlers, human experts, and
detection points during the search under a blind-test procedure for tracking positions. The potential utility of the
search methods was estimated with three aspects: 1) search success: detection of infested trees, 2) search effort:
length of route, and 3) search efficiency: trees detected / unit time.
Dog-handler pairs were overall more successful in detecting trees attacked by bark beetles than human experts.
In particular, the success rate of dogs was higher in plots with random arrangement pre-baited trees and search
efficiency was four times higher than that of the human experts.
The most efficient time for the use of dogs for detection would be during the spring flight period, when
detection of first attacks and small hot spots could potentially prevent the development of larger infestations. The
main advantage of using the dog search method is to amplify the time-window from about one week to one
month from the detection to prompt removal of the infested trees from the forest.

1. Introduction
The Eurasian spruce bark beetle Ips typographus (L.) is an intensively
studied, native long-term pest of Norway spruce in the entirety of its
natural and planted distribution in the European forests (Christiansen &
Bakke 1988, Grégoire & Evans 2004). Climate change has induced an
unprecedented outbreak of I. typographus infestation in spruce trees in
recent years (Hlásny et al. 2019). The epicentre of the current bark
beetle outbreak is Central Europe, where the most affected regions are
now being deprived of older spruce stands (Hlásny et al. 2021a).
Drought stress has been the main driver of outbreaks in spruce forests
(Hlásny et al. 2021b). Climate change predictions show an increased
frequency of shorter or longer periods of precipitation and temperatures
that are outside the bioclimatic niche of Norway spruce, and this would
induce drought stress (Lindner et al. 2010). Considering these dramatic
changes, forest management should act quickly to contain the spread of
the spruce bark beetle.
Integrated pest management of spruce bark beetles traditionally in­
volves the implementation of preventive measures and treatment ac­
tions (Fettig & Hilszczanski 2015). Early detection and removal of bark
beetle-infested trees remain crucial aspects of bark beetle management
(Hlásny et al. 2019). However, the visual signs of infestation in the tree
crown are very difficult to observe with the human eye from a distance,
as the foliage remains green for weeks (Kautz et al. 2022). Substantial
progress in the identification of attacked trees was achieved with remote
sensing, where aerial, unmanned aerial vehicles, and satellite imagery

* Corresponding author.
E-mail address: modlinger@fld.czu.cz (R. Modlinger).
1
Authors claim shared seniority.

https://doi.org/10.1016/j.foreco.2022.120626
Received 28 July 2022; Received in revised form 26 October 2022; Accepted 1 November 2022
Available online 14 November 2022
0378-1127/Published by Elsevier B.V.
N. Vošvrdová et al.
provided useful information on the extent of bark beetle damage
(Wulder et al. 2006, Näsi et al. 2015, Abdullah et al. 2019, Klouček et al.
2019). Still, the identification of infested trees is prone to errors due to
differing accuracy and the timeliness of detection (Huo et al. 2021,
Zabihi et al. 2021, Bárta et al. 2022). The most reliable method of
identifying bark beetle attack has been close visual inspection of the tree
trunk (Kautz et al. 2022). However, this method is time consuming, and
variability in weather conditions can complicate visual inspection
because the boring dust can be washed away by the rain (Hlásný et al.
2019). A novel method of detection is the use of specially trained dogs;
this is by far the most promising technique for the rapid detection of
bark beetle-infested trees and is already a technically proven concept for
praxis (Johansson et al. 2019).
Dogs have been widely used in the detection of humans, cadavers,
drugs, and explosives, (Hepper & Wells 2015). Recently, dogs have been
increasingly used to search for insects such as termites [Termitidae]
(Brooks et al. 2003), bugs [Cimicidae] (Pfiester et al. 2008), ants [For­
micidae] (Lin et al. 2011), palm weevils [Curculionidae] (Suma et al.
2014), and longhorn [Cerambycidae] or jewel beetles [Buprestidae]
(Hoyer-Tomiczek et al. 2016, Hoyer-Tomiczek & Hoch 2020). Some of
them are considered invasive species in particular areas. Dogs have been
used to detect xylobiont beetles that are protected by law (Mosconi et al.
2017, Apelqvist, 2022). Identification of these insect species by dogs is
made possible by previous knowledge of the pheromones and other
semiochemicals released during host colonization (Bakke et al. 1977),
and their quantitative changes (Birgersson et al. 1984). Dogs can detect
infested trees in the early stages of bark beetle attack, even before
physiological changes visually manifest in the tree crown (Kautz et al.
2022). Dogs trained to detect bark beetle pheromones can find an
infested tree up to a distance of 150 m (Johansson et al. 2019). Such
impressive detection ranges could be exploited for high sensitivity and
could be crucial in finding new bark beetle spots within forest stands,
which are more frequent and random during drought periods (Hlásný
et al. 2021b). However, due to the novelty of the dog-based detection
method, no evaluations or comparisons of this method with the tradi­
tional techniques have been made. Given the costs associated with long-
term training and maintenance of dogs for bark beetle detection (Esti­
mation for Czech conditions is 18 000 EUR, including eight months of
training, necessary materials, travelling to forests and personal costs
based on average gross nominal wage, excluding purchase price of the
dog and feeding), it is crucial to gauge the efficacy of this new approach
before adopting the method for forest pest management.
We hypothesise that dog-handler pairs would be more efficient
searchers than human experts in the early detection of beetle-attacked
trees in commercial forests. We measured three dependent variables:
1) search success: detection of recently attacked trees, 2) search effort:
search route length travelled / unit area, and 3) search efficiency:
infested trees detected / unit time.
2. Materials and methods
2.1. Dog-handler pairs and bark beetle specialists
The three dogs that participated in the experiment were Belgian
Shepherds (FCI 2002). Details about their ages, sex, and levels of
experience in detecting I. typographus are shown in Table S1. Two dogs
had five years’ experience with bark beetle detection, and the other dog
was a novice that had underwent six months of training in synthetic
compound detection and two months training in detecting infested trees.
The usual way to provide training odour stimuli is from natural material
for this type of study, which is cumbersome. Such biological material has
variable quality due to decay over time or low source material avail­
ability, for instance during winter or coming from protected species. In
contrast, training to detect semiochemicals of the Eurasian spruce bark
beetle is facilitated by the knowledge and year-round synthetic avail­
ability of the pheromone components and the verbenone released during
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Forest Ecology and Management 528 (2023) 120626
their development (Bakke et al. 1977, Birgersson et al. 1984, Johansson
et al. 2019). All three dogs were trained using the method of Johansson
et al. (2019), which is based on the principle of positive reinforcement;
that is, dogs were rewarded immediately after a correct indication of the
target scent (Rebmann et al. 2000, Braun 2013). For scent detection,
three separate components of the I. typographus aggregation pheromone,
specifically 2-methyl-3-buten-2-ol, 4S-cis-verbenol, and ipsdienol, as
well as verbenone were used during the early stage of training (Bir­
gersson et al. 1984). An education scent platform was used to teach these
four odours. Dogs were exposed to various indoor training situations.
After this phase, the training lessons were moved to outdoor conditions.
Individual substances were replaced by a mixture of the compounds
during the advanced stage of training, and the search area was gradually
enlarged. The dogs were trained with actual bark beetle-attacked trees
in the last training phase. Three bark beetle specialists were included in
the experiment; the specialists had extensive experience in searching
bark beetle-infested trees in Central Europe.
2.2. Experimental set-up
All experimental plots were situated in the School Forest Enterprise
(SFE) Kostelec and Černými lesy (Czech University of Life Sciences),
near the small town of Stříbrná Skalice (Central Bohemia, Czech Re­
public; Fig. 1). The SFE is an upland area outside the natural Norway
spruce distribution, with suboptimal environmental conditions for the
tree species: a mean annual temperature of 7–8 ◦ C, and mean precipi­
tation of 550–600 mm / year (Tolasz et al. 2007). In 2018, when the
experiment was conducted, the outbreak of I. typographus was on a steep
rise in Central Bohemia (Hlásny et al. 2021b). Six experimental plots
were established in an 100–120-year-old Norway spruce-dominated
forest stand, where spruce trees constituted more than 95 % of the
tree cover. For better orientation of the dog handlers and human spe­
cialists, trees on the plot boundaries were marked using a coloured
paint.
For initialization of bark beetle attack, standard pheromone dis­
pensers IT Ecolure® (Fytofarm, Mělník, Czech Republic) were used. The
number of baited trees and plot areas are given in Table 1. Two types of
dispenser placements on the experimental plots were used: (a) random
spatial distributions (referred to as random plots) in any place of the
experimental area (e.g. a single tree in the middle of the forest), and (b)
places considered suitable for beetle attacks (referred to as suitable plots),
based on knowledge of bark beetle preferences (Wermelinger 2004,
Fahse & Heurich 2011). The suitable plots could be forest edges (Kautz
et al. 2013) with logging residuals (Stříbrská et al. 2022), stands around
trees damaged by wind (Göthlin et al. 2000), sunny parts of the forest, or
southern slopes of the hills ((Netherer and Nopp-Mayr, 2005) (Table 1;
Fig. 1).
Pheromone dispensers were placed on selected spruce trees at a
height of 3 m above the ground on 27, 28, and 30 June 2018. The lo­
cations of baited trees were recorded using GPS. After 4–8 days
(depending on appropriate weather conditions for beetles flight), the
dispensers were removed, and the trees were checked for infestation
status (to certify if attacks had started during the short period of baiting,
considering that the weather controlling beetle flight intensity was a
random factor). At 2–10 days after dispenser removal and two days
before the start of the experiment, the plots were again checked for the
presence of spontaneously attacked trees, which were also recorded
using GPS.
The search for attacked trees was performed using the double-blind
method (Moser & McCulloch 2010; Jendrny et al. 2020), where a bark
beetle expert/dog-handler pair was made to walk through the experi­
mental areas alone without knowledge of position of the infested trees.
The experiment was performed for eight days; dog-handler pairs were
allowed to search the forest for the first four days, followed by the
human experts for the remaining four days. The performing of the
experiment was realised under the prepared scheme, each dog searched
N. Vošvrdová et al. Forest Ecology and Management 528 (2023) 120626

Fig. 1. Overview of the experimental plots in the School Forest Enterprise of Kostelec nad Černými lesy (Czech University of Life Sciences, Czech Republic) in Central
Bohemia and their location in the Czech Republic. Inside the experimental plots, the positions of bark beetle-infested trees are marked (pre-baited and spontaneously
attacked). See Table 1 and Table S1 for details of plots and search parties.

overall areas of search and the movement of the dogs to facilitate up­
Table 1
wind search, as detailed by Johansson et al. (2019). The dog handlers
Parameters of experimental plots.
were neither trained foresters nor entomologists, but were experts in dog
Plot Plot Attacked trees Arrangement behaviour and sniffer dog training; however they had the necessary
nr area of pre-baited
Artificially Number of Volume of knowledge and ample practical experience to allow them to ascertain
(ha) trees
pre-baited infested infested trees whether an indicated tree had been attacked by I. typographus. The
trees at start trees at end at end of
number of infested trees and the time taken for searching the given plot
of of experiment
experiment experiment (m3/ha)
was also recorded. At the end of each part of the experiment, all trees in
all the plots were visually inspected by the same independent person
1 10 10 44 5.3 Suitable*
from the team of authors, and the number of infested trees (pre-baited or
2 7.7 12 67 10.4 Suitable
3 4 5 9 2.7 Random not) and their GPS positions were recorded.
4 12 10 13 1.3 Random
5 12 11 14 1.4 Suitable
6 12 9 13 1.3 Random 2.3. Statistical analyses
*
Position of pre-baited trees (to become attacked) in patches of the plot that
we judged as ‘suitable’ for bark beetle colonisation of trees, as opposed to purely Statistical evaluation was performed using three dependent vari­
randomised tree positions for pre-baiting. ables, each in a separate regression model. The first dependent variable,
“Search success”, was the percentage of successfully detected beetle-
maximally-two plots per day, and to prevent tracking, only one dog was attacked trees in a plot. In dog-training terms, these were the “true
planned for each plot per day, except plot 5, where in the morning was positives”. The second variable “Length of search route” was measured
BB and afternoon Aska (the most experienced dog who does not follow a as the GPS track route length covered to search a plot (unit: km / ha). A
track on the ground but fully used wind blowing). Search routes of the third variable “Search efficiency” was calculated as the ratio of “Search
dog, the handler and bark beetle specialists were recorded using GPS success” and time spent on the plot (unit: trees detected/min.).
(Fig. 2). The handler track generally followed the dog track. Hence, only We analysed the three dependent variables using a generalised linear
the route of the dog in each dog-handler pair was evaluated. The dogs mixed model (GLMM). As the independent variables for GLMM, we used
moved faster and covered a larger search area because they were “Design”, which was the arrangement of the trees attacked by bark
directed by olfactory stimuli, whereas the handlers determined the beetles in the plot (random vs suitable) and “Searcher”, or who inspected
the plots (dog-handler pair vs human expert). Interactions of the

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N. Vošvrdová et al. Forest Ecology and Management 528 (2023) 120626

Fig. 2. Maps of two examples of GPS routes of human experts and dog-handler pairs searching for bark beetle-attacked trees in experimental plots. A) Plot 1 was
established in the “suitable” tree arrangement spatial design, and B) plot 6 in a “random” design (Table 1, Fig. 1). See the Materials and Methods for the definitions of
the spatial arrangements. Higher resolution track examples for all 6 plots can be found in Fig. S2.

independent variables were also included in all cases, but in two models
Table 3
they were found to be not significant according to the likelihood-ratio
GLMM contrast comparison the Search success of the “Searcher” on Suitable and
test (χ2) during the model building; hence, they were not included in
Random plots.
the final models shown in Tables 3–5. All variables were explored for
basic assumptions of regression type analysis, as described by Zuur et al. Design

(2010). Violation of the assumptions was found in relation to the inde­ Searcher Suitable Random
pendence of the observations, which were influenced by the evaluation Dog-handler pair vs Human expert 0.81182 0.000406 ***
of the same experimental plots. Therefore, using GLMM, a random
structure for each experimental plot was implemented in the model.
Model formulation and prediction were realised in the package Table 4
GLMM contrast comparison the Search success of Dog-handler pairs and Human
experts on different plot “Design” arrangements.
Table 2
Searcher
GLMM likelihood-ratio test for significance independent variables including Design Dog-handler pair Human expert
their interaction. Dependent variable attacked trees detected (%,), independent
Suitable vs Random 0.217012 5.82e-06 ***
variables “Searcher” and “Design”.
Df AIC LRT Pr(>Chi)

Searcher 1 5.4687 5.5938 0.0180 * glmmTMB following the procedures described by Brooks et al. (2017).
Design 1 8.0261 8.1513 0.0043 ** Because response variables were continuous, strictly positive, and
Searcher:Design 1 1.8748 5.0634 0.0244 * without zeroes, gamma distribution was used (Zuur et al. 2009). All

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Table 5 experts in suitable plots, where 66 % of infested trees were detected by

GLMM likelihood-ration test for length of search route (km/ha, dependent dog-handler pairs and 63 % by human experts (GLMM p = 0.81; Table 3;
variable). “Searcher” and “Design” are independent variables. Fig. 3A). Significant difference in detection levels between human ex­
Df AIC LRT Pr(>Chi) perts and dog-handler pairs was observed in the random plots, where the
Searcher 1 1.0119 6.7232 0.0095 **
bark beetle-infested trees were at unexpected locations and mostly
Design 1 − 5.3748 0.3365 0.5619 encountered fewer attacks. Dog-handler pairs found 51 % of attacked
Searcher:Design 1 − 3.7113 0.1699 0.6801 trees, while human experts found only 23 % (GLMM p < 0.001; Table 3).
In contrast, the search success on the suitable plots was similar between
dog-handler pairs and human experts (Fig. 3A). The search success of the
GLMM analyses were performed using the R 4.0.2 environment (R Core
Human expert was significantly different between the variant arrange­
Team 2020).
ments (63 % vs 23 %; GLMM p < 0.001), whereas the Dog-handler pair
success cannot be considered different (66 % vs 51 %; GLMM p = 0.81;
3. Results
Table 4). These statistical conclusions are well illustrated by the example
of the best human expert, who was more successful than dog-handler
3.1. Search success
pairs in all the suitable plots (Fig. 3A).

The experiment was performed a week after the first bark beetle
attack. Therefore, the infested trees did not yet show any visible changes
in the crown; they could only be detected by the presence of boring dust
that had settled at the base of the tree trunk. Overall, dog-handler pairs
were more successful than human experts in the detection of trees
attacked by bark beetles (GLMM p < 0.05; Table 2). On average, 58 % of
bark beetle-infested trees were detected by dog-handler teams and 43 %
by bark beetle human experts (Table S2). The experimental tree
arrangement factor provided clear differences between dog and human
searchers.
A higher proportion (64 %) of attacked trees were found in the
suitable plots. Plots with pre-baited trees in random positions were much
less detected (37 %), indicating a significant difference between spac­
ings (GLMM p < 0.01; Table 2; Fig. 3). From the factors interaction point
of view, there was no difference between dog-handler pairs and human
3.2. Search effort
During search for infested trees, dog-handler pairs covered an
average distance of 2 km longer than that of human experts. The average
distance covered by dog-handler pairs was 0.55 km/ha, while human
experts walked 0.36 km/ha (Supplementary Table S2). Plot type had a
no effect on length GLMM p = 0.56; Table 5). There was a significant
difference in the length of the route between dog-handler pairs and
human experts (p < 0.01, Table 5; Fig. 4). Dog-handler pairs on average
walked a greater distance than did human experts. However, if we
exclude the data of the young dog in training (“BB”; Supplementary
Table S1), which took the longest route in all the plots, the difference
between dog-handler pairs and human experts was minimal (upper red
dot in Fig. 4). The route length did not show significant interaction
between searcher type and tree arrangement (GLMM p = 0.68; Table 5).

Fig. 3. Search success – the successfully identified attacked trees found by dog-handler pair (red) and human expert (blue) searchers in two types of spacing of
experimental tree arrangement: A)‘Suitable’ arrangement in patches considered ‘suitable’ for beetle attacks and B) ‘Random’ with a randomised spatial distribution.
The bigger dot in the middle is a posterior mean value and whiskers represent the 95 % CI of the prediction. Smaller dots are original values. (For interpretation of the
references to colour in this figure legend, the reader is referred to the web version of this article.)

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N. Vošvrdová et al. Forest Ecology and Management 528 (2023) 120626

Fig. 4. Search efforts: Length of search route in km/ha by dog-handler pair (red) and human expert (blue) searchers in two types of spacing of experimental tree
arrangement: A)‘Suitable’ arrangement in patches considered ‘suitable’ for beetle attacks and B) ‘Random’ with a randomised spatial distribution. Bigger dots in the
middle represent posterior mean values and whiskers represent 95% CIs of the predictions. Smaller dots are original values. (For interpretation of the references to
colour in this figure legend, the reader is referred to the web version of this article.)

3.3. Search efficiency efficiency indicated an overall higher performance by dog-handler pairs.

Dog-handler pairs were overall more efficient, as they showed a 4. Discussion

higher number of trees detected / unit time than human experts (GLMM
p < 0.001; Table 6; Fig. 5). The mean number of trees detected per unit
time by dog-handler pairs was more than double compared to that by
human experts (dog-handler pair 2.3 trees/10 min, human expert 1.1
trees/10 min., Supplementary Table S2). The ‘suitable’ tree arrange­
ments of the pre-baited plots were less demanding for human experts,
the difference in the dog-handler pairs was relatively smaller (<1.9
times) (Supplementary Table S2).
Among the two tree arrangements, the number of trees detected /
unit time was generally lower for the random arrangement (Fig. 5B).
There was a significant difference for tree arrangement (averaged over
searcher type, p < 0.01; Table 6). In the random arrangement of pre-
baited trees, the human experts were less efficient and the efficiency
of the dog-handler pairs during the search was greater than 4 × higher
(dog-handler pair 1 tree/min, human expert 0.25 tree/min; Supple­
mentary Table S2). According to the statistical model the interaction
searcher with the tree arrangement factor was not significant (GLMM p
= 0.07; Table 6). Thus, our estimates for the three aspects of search
Table 6
GLMM likelihood-ration test for efficiency of detection (trees/10 min of search,
dependent variable). “Searcher” and “Design” are independent variables.
Df AIC LRT Pr(>Chi)
Searcher 1 96.2060 20.7422 0.0000
Design 1 82.4010 6.9376 0.0084
Searcher:Design 1 77.4630 3.2172 0.0729
For descriptive statistics of the input dependent variables, see Table S2.
To our knowledge, this is the first field comparison of the efficiency
of sniffer dogs and foresters (human experts) in the detection of bark
beetle-infested trees, using known positions of true positive cases in
experimental forest stands. False negatives did not occur because the
handler in the team verified the authenticity of the trees identified by
the dogs. Similarly, the experts used in this study were not expected to
give “false positives”, but “false negatives” may have occurred in the
event of fresh attacks where frass was washed away by rain. The field
experiences show that the dog finds almost no false positives. Perhaps 10
for the whole season. Usually, those trees have 1 or 2 bark beetle
entrance holes. The attack can develop into an infestation, or the tree
can defend itself. Both options are possible in the field. Known positions
allow a higher precision during evaluation, and the two types of ar­
rangements of pre-baited trees, random and suitable, helps to better
relate to a variety of real-life praxis conditions.
We found that dog-handler pairs found 51 % of attacked trees
whereas the human experts found 23 % in the case of random spatial
spacing of pre-baited trees (Supplementary Table S2). Such spatial
patterns of bark beetle attacks occur naturally during large outbreaks,
where the predisposition of trees play a lesser role in bark beetle infes­
tation, and the trees are colonised rather randomly (Fahse & Heurich
2011) or in other patterns, for example presence of Armillaria root rot
(Jakuš 1998). Similarly, we observed such patterns during 2018, when
bark beetle spots appeared inside a seemingly homogenous spruce stand
***
** with no visible predispositions. For the initialization of the bark beetle
. attack, local water availability for trees could be an important factor
(Netherer et al. 2021), which may occur irregularly at the level of

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N. Vošvrdová et al.
Fig. 5. Efficiency of search (correctly detected trees/10 min) by dog-handler pairs (red) and human experts (blue) under two types of experimental spatial tree
distributions: A)‘Suitable’ arrangement in patches considered ‘suitable’ for beetle attacks and B) ‘Random’ with a randomised spatial distribution. Bigger dot in the
middle is a posterior mean value and whiskers represent 95 % CI of the prediction. Smaller dots are original values. (For interpretation of the references to colour in
this figure legend, the reader is referred to the web version of this article.)
individual trees. Such random occurrence corresponded to our experi­
mental design, where prior knowledge about the preference of bark
beetles was not used for selecting trees in our random plots. Our results
showed that dogs were generally successful in detection of infested trees
in random plots, likely due to their ability to detect pheromones over
long distances, typically over 100 m (Johansson et al. 2019). Notably,
the dog-handler pairs did not move in any ‘random walk’ when
searching. Instead, the handlers followed direct search routes to cover
plots in a structured way (Fig. 2, Supplementary Fig. S1).
Human experts searched the experimental areas for approximately
twice as long as dog-handler pairs, regardless of the plot design (Sup­
plementary Table S2). Random plots were searched slightly faster than
suitable plots possibly due to the relatively lower number of attacked
trees / hectare (Supplementary Table S2). Completing the search was
entirely up to the discretion of the searcher. Dog-handler pairs could
finish the search of an area sooner due to the ability of dogs to detect
attacked trees from a distance that was approximately-two orders of
magnitude longer than that of a human – 100 m vs 1 m (Johansson et al.
2019). The shorter time to find an infested tree during the early stages of
infestation allows control of a larger endangered forest area at the start
of a beetle flight. One of the main reasons for failure to contain a bark
beetle outbreak is the lack of human resources during beetle flight pe­
riods (Hlásný et al. 2021a). Higher search success in a shorter amount of
time favours the use of sniffer dogs over humans for the timely detection
of infested trees.
We expected a longer search route for the human experts due to the
need for close-range inspection of the trunk. The contrasting results
could be caused by: (i) use of a young dog still in training, and (ii) the
confidence of the forest experts in their knowledge. Regarding the first
point, this study used a relatively inexperienced dog-handler pair
(Supplementary Table S1), who was trained on real infested trees for
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Forest Ecology and Management 528 (2023) 120626
only two months before the experiment. The search route of the inex­
perienced pair was the longest of all pairs, except in one case. Data
excluding the inexperienced pair indicate the search route of dog-
handler pairs would be similar to that of the human experts (0.35 vs
0.36 km/ha). Regardless, the novice dog-handler pair, still found more
infested trees than human experts with many years of experience.
Furthermore, the relatively short search route of the human experts was
due to their reliance on the visible markings in the attacked trees
(different shades of green, resin flow under the tree crown) or their
knowledge of suitable areas for bark beetles. Such a strategy was rela­
tively successful in plots with places judged as suitable, but frustrating in
the case of plots with random arrangement of pre-baited trees. Human
experts stopped searching on random plots earlier due to lack of direc­
tion in exploring attacked trees and the practical difficulty of visiting
each tree.
There have not been enough studies comparing the efficiency of dog-
handler pairs with other techniques. For detecting mammals was the
higher success of dogs, also found by Long et al. (2007) and Cristescu
et al. (2015). Unfortunately, here are no studies that evaluate the reli­
ability of humans (foresters) in detecting trees attacked by bark beetles.
A field survey of infested trees by foresters is considered a reliable
detection method (Bárta et al. 2022) but it is demanding both in terms of
time and workforce. In our experiment, the success of foresters and dog-
handler pairs in finding trees attacked in random plots differed sub­
stantially, with success rates of 23 and 63 %, respectively. In suitable
plots, the success rates were more similar, but still lower for humans
(Fig. 3A).
An impressive success rate with respect to dog-handler pairs was
observed, even though a week had passed between the field survey of
dogs and humans; more infested trees developed more visible signals
(mainly boring dust) during this time, which could be easier to detect for
N. Vošvrdová et al.
human experts. Moreover, according to Johansson et al. (2019), dogs
can detect infested trees from the first hours after the attack, which
agrees with the chemically determined rate of pheromone production
(Birgersson et al. 1984). In a recent comparison between human expert
and aerial hyperspectral detection methods, bark beetle-infested trees
were detected 23 days later via remote sensing compared to human
detection (Bárta et al. 2022). This shows the problem of timeliness with
remote sensing owing to reflectance of the crown; see also Kautz et al.
(2022).
Managing bark beetle population levels in most forests is realised by
sanitation felling (Hlásny et al., 2021a). The first and most important
rule formulated by Wermelinger (2004) for efficient sanitation felling is
that “trees must be found and cut before the new beetle generation
emerges”, optimally before parental adult females leave the tree for the
sister-brood establishment (Davídková & Doležal 2017). A critical
element of this rule is the early detection of infested trees. The sooner
the infested trees are found, the greater the chances of timely prevention
of bark beetle infestation spread. The use of sniffer dogs brings a new
dimension where early and rapid detection of infested trees, immedi­
ately after occupancy by bark beetles, is achieved.
If intensive detection and processing management are carried out
immediately at the beginning of the first bark beetle attack activity, the
spread of later bark beetle outbreak can be prevented. Under warm and
dry conditions, serious landscape scale outbreaks can arise from the first
few spring bark beetle attack hotspots (tree groups). The use of dogs for
bark beetle detection is very effective and time-efficient, as they can find
small starting points (Johansson et al. 2019); in other words, they can
locate a single tree within the forest. Detection of infested trees in the
forest using classical visual methods can be challenging in areas with a
lower occurrence of bark beetles or in newly infested areas. Conversely,
in areas with larger, more continuous beetle disturbances, the benefit of
dog-handler pairs is less meaningful. These include larger areas with
ongoing bark beetle outbreaks, such as newly created forest edges, that
are usually easily traceable by visual methods alone.
The practical use of dogs for identifying bark beetle infested trees is
limited by the number of handlers, number of trained dogs, and time
necessary for dog training; however, in this study, the success of a young
dog trained only for a short time to detect infested trees is promising.
The most efficient time for use of dogs is almost certainly in the spring
flight period, when dog-handler pairs can detect initial attacks and small
hot spots (single or a few trees) and stop the development of incipient
larger infestations. Later, when larger bark beetle infestation spots
occur, dog-handler pairs could delineate foci of infestation hot spots,
narrowing down the area for forestry experts to focus the search activity
for new attacks, rather than searching the whole forest again.
Using dogs as searchers is crucial for active forest management at the
beginning of an outbreak. The main advantage of using the dogs is to
amplify the time-window for detection and timely removal of the trees
from forest, and/or their felling and debarking. Faster identification of
infested trees within the longer period (from the 1st day after attack to
9th week after attack, as opposed to when clear symptoms are visible, i.
e. in the 4–6th weeks) could be a key factor in bark beetle management
in the initial phase of outbreak. According to our experience, in both
Central Europe and Scandinavia, the forestry staff in the period of late
April to the first half of May are heavily stressed by other work, mainly
with artificial afforestation. This can result in relatively lower prioriti­
sation to identify and cut infested trees. Thus, the use of sniffer dogs is a
convenient way to effectively complement the work of foresters during
the demanding spring season.
In particular, the present global climate change is increasing the
effect of temperature on forest health (Hartmann et al. 2022) and has
made spruce forests more vulnerable. Observations over the past few
decades have indicated an increase in the number of I. typographus
generations from one to two in Scandinavia (Jönsson et al. 2011) and
three in Central Europe (Hlásný et al. 2011), which necessitates a strong
reduction of the bark beetle population in the spring period. The use of
8
Forest Ecology and Management 528 (2023) 120626
the most effective methods for the protection of forest stands from bark
beetles is currently an important mitigation measure that forest man­
agement must address to preserve carbon storage in spruce forests in the
coming decades (IPCC 2022).
5. Conclusion
Dog-handler pairs showed an overall higher efficiency in fulfilling
the demands in the three aspects of search potency: higher detection
success, lower search effort, and a resulting higher efficiency. Plots with
the two arrangements of briefly pre-baited tree positions, random and
suitable, differed strongly: the random pattern was difficult to search for
both dog-handler pairs and humans alone, but more so for humans. Our
results show that dog-handler pairs were four times more efficient in
detection within random plots, probably because they orient to single-
tree sources of pheromones over long distances. The shorter time to
find an early bark beetle-attacked tree allows proactive management of
a larger endangered forest area at the start of beetle flight. The use of
sniffer dogs brings a new, larger window of very early and rapid
detection and further management of infested trees, even immediately
after the first occupancy by bark beetles.
CRediT authorship contribution statement
N. Vošvrdová: Investigation, Data curation, Funding acquisition,
Writing – original draft. A. Johansson: Investigation, Writing – original
draft. M. Turčáni: Funding acquisition, Resources, Writing – original
draft. R. Jakuš: Investigation, Writing – original draft. D. Tyšer: Visu­
alization. F. Schlyter: Conceptualization, Supervision, Validation,
Funding acquisition, Writing – original draft. R. Modlinger: Method­
ology, Conceptualization, Investigation, Visualization, Funding acqui­
sition, Data curation, Writing - original draft, Writing - review & editing.
Declaration of Competing Interest
Authors declare to doń t have a competing interest.
Data availability
Data will be made available on request.
Acknowledgements
This research was supported by the EU project “EXTEMIT-K”, No.
CZ.02.1.01/0.0/0.0/15_003/0000433 financed by OP RDE and NAZV
QK1920435 funded by Ministry of Agriculture. It was also supported by
the Internal Grant Agency Czech University of Life Sciences, Prague,
Faculty of Forestry and Wood Sciences, Kamýcká 129, Praha 6 - Suchdol,
165 00, Czech Republic - projects GA FLD CZU A_19_10. AJ and FS were
partly supported by Swedish Research Council FORMAS grant 2013-
01583.
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.foreco.2022.120626.
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