Stutz et al. Ecological Processes
(2019) 8:25
https://doi.org/10.1186/s13717-019-0179-3
RESEARCH
Open Access
A mechanistic understanding of repellent
function against mammalian herbivores
Rebecca S. Stutz1* , Louisan Verschuur1,2, Olof Leimar1 and Ulrika A. Bergvall1,2
Abstract
Background: Browsing repellents are widely used to deter large herbivores from consuming plants of ecological,
economic and aesthetic importance. Understanding how these repellents function on a behavioural mechanistic
level is critical to predicting effectiveness. Here, we illustrate how these mechanisms can be tested, by exposing a
model mammalian herbivore, the fallow deer, to different concentrations of a commercial chemical repellent
(HaTe2) in two-choice feeding trials.
Results: The repellent acted as a defensive chemical for the food by both reducing visitation and the amount
consumed. Deer favoured the less defended feeders before ingesting any food, suggesting that the repellent
altered olfactory and/or visual cues. Deer also consumed less of the more defended food when choosing between
low and high repellent feeders than no and low repellent feeders, indicating that the repellent modified flavour
and/or sensation. Repellent effectiveness declined with increased exposure, suggesting that consumption had no
negative post-ingestive effects, and thus, deterrence was not caused by a conditioned aversion or irritation. Instead,
this pattern suggests that deer learned, through repeated sampling of repellent-treated food, that there was no
adverse physiological effect of ingesting it.
Conclusions: These results imply that HaTe2 repellent will not be effective over prolonged periods or in the
absence of alternative untreated food. Understanding the mechanisms driving repellent function using two-choice
trials could help practitioners decide whether a particular repellent is likely to be effective against mammalian
herbivory in their management scenario.
Keywords: Browse, Foraging decisions, Forestry, Ungulate, Wildlife damage
Background
Plants and herbivores interact in a complex and reciprocal manner: plants influence the health and distribution
of herbivores, while herbivory modifies the composition
and structure of plant communities (Augustine and McNaughton 1998). These interactions can have farreaching consequences for other plants and animals by
influencing the availability of resources (Nuttle et al.
2011; Pedersen et al. 2007; Stephan et al. 2017), the success of revegetation efforts (Austin et al. 1994; Stutz et
al. 2015) and productivity in agriculture and forestry
(Putman and Moore 1998). One method for reducing
damage by abundant mammalian herbivores is the application of chemical repellents to deter herbivores from
* Correspondence: rebecca.stutz@zoologi.su.se
1
Department of Zoology, Stockholm University, SE-106 91 Stockholm,
Sweden
Full list of author information is available at the end of the article
high-value plants such as those used in cropping, timber
production, restoration and gardening. While several
commercial wildlife repellents are available, and some
products have been tested for effectiveness (e.g. Conover
1984; El Hani and Conover 1998; Nolte 1998; Novellie
and Bigalke 1981), we have an incomplete understanding
of the behavioural mechanisms that underlie repellent
function (or malfunction) in deterring mammalian herbivores from consuming plants.
Repellents may deter herbivores via one or more
mechanisms that reduce the appeal of plants and thus
influence foraging decisions. Kimball et al. (2009) defined four ‘modes of action’ for mammalian herbivore
repellents: neophobia, irritation, flavour modification
and conditioned taste aversion. We propose an extension of this framework that disentangles the sensory cues
altered by repellents from the behavioural and physiological mechanisms that drive deterrence (Fig. 1).
© The Author(s). 2019 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 appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.
Stutz et al. Ecological Processes
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Fig. 1 Repellents alter the sensory cues of food and may deter herbivores via mechanisms both with and without realized physiological
consequences of ingestion. The dotted line indicates the relationship between conditioned aversion and aversion to a mimic (a repellent
mimicking cues associated with adverse physiological effects but without any adverse effects itself)
Repellents often change the smell and appearance of
food, and these cues are apparent before the food is
tasted. Once the animal takes a bite, it experiences the
flavour and feeling of the food in its mouth and this can
also be modified by a chemical repellent. The association, or not, of these cues with previous experiences
and adverse physiological effects determines how effectively the repellent deters herbivores from consuming
treated food (Kimball and Taylor 2010).
Repellents that do not cause any adverse physiological
effects rely on cues that induce innate or learned avoidance behaviours. For example, those based on neophobia
take advantage of the fear of novel stimuli (Cassini 1994;
Villalba and Provenza 2000). However, if a repellent only
consists of a novel taste, texture, smell or colour, without
any negative post-ingestive consequences, its effectiveness generally decreases with exposure time as animals
learn to incorporate it in their diet (Nolte 1999). This
is probably a consequence of post-ingestive learning
(Arnould and Signoret 1993; Provenza 1995), in combination with the continuous sampling behaviour of
mammalian herbivores (Provenza et al. 1998), with
the speed of learning depending on an animal’s nutritional status and the availability of alternative food
(Provenza 1995).
Another category of repellents is based on herbivores’
innate fear of predation, often induced using odour cues
from predator urine and faeces, or sulphurous compounds associated with predation (Bean et al. 1997; Pfister et al. 1990; Sullivan et al. 1985; Woolhouse and
Morgan 1995). Much like the repellents based on novelty, those based on fear of predation are infrequently reinforced by experience; unless predation pressure is
high, there are relatively few opportunities to associate
the cue with the presence of a predator or a predation
event in the herd. Their effects can thus be short-lived,
particularly in the absence of alternative food (Murray et
al. 2006).
In contrast, repellents that cause pain or discomfort
on contact with the mouth, nose or eyes generally have
immediate deterrent effects (Beauchamp 1997; Mason
1998), possibly because these irritants mimic the compounds released during tissue damage (Clark 1997).
There is some evidence that repellents containing compounds that activate the trigeminal system, such as capsaicin, deter mammalian herbivores from consumption
when applied at high concentrations, but hunger appears
to reduce the deterrent effect (Andelt et al. 1992; Andelt
et al. 1994).
Animals experiencing sensory cues associated with
malaise or gastrointestinal distress, such as those indicating the presence of tannins or lithium chloride, can
develop conditioned aversions (Burritt and Provenza
1989; Provenza 1996; Provenza et al. 1990). The effects
of these repellents are typically long-lasting as repeated
sampling by herbivores reinforces the negative association between flavour and consequence. Conditioned
aversions may even extend to mimicking cues associated
with experiences of negative post-ingestive effects (Massei et al. 2007).
A single repellent may employ one or a combination
of sensory cues and behavioural mechanisms to deter
herbivores from consuming treated plants. A large number of repellents exist and have been tested for efficacy
in the field, but we currently do not have a mechanistic
understanding of how these repellents operate to deter
herbivores. This is important for predicting repellent effectiveness under variable field conditions and the factors that could lead to failure. Our objective was to
develop a simple behavioural experiment for determining
Stutz et al. Ecological Processes
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the mechanisms of deterrence and modes of action
employed by commercial repellents.
We used two-choice feeding trials to quantify the behavioural responses of a model mammalian herbivore, the fallow deer (Dama dama), to food varying in repellent
concentration. We chose the commercial repellent HaTe2
(Fluegel GmbH, Germany), a black viscous liquid comprised of ethanol, balsam resin and black pigment. Given
that the repellent altered the appearance, smell and possibly taste and texture of food, we hypothesised that the
mechanisms behind its deterrent function would be twofold: first by reducing the frequency with which animals
chose the food and second by reducing the amount of
food they ingested as a function of repellent concentration. For each sensory and behavioural mechanism that
could be involved in deterring food consumption, we specified the foraging behaviour that we would expect from
the deer (Table 1). Some modes of action are more robust
than others; thus, understanding how a chemical repellent
functions at the behavioural level is critical for predicting
its performance as a herbivore deterrent.
Methods
Experimental design
We used seven adult female fallow deer that were born
in 2000 and had been hand-reared, making them amenable to conducting individual paired-choice feeding trials. They were held in a 4-ha enclosure at Tovetorp
Research Station (Stockholm University, south-central
Sweden). The enclosure comprised a sloping meadow
with low-lying shallow waterbodies and a variety of trees
including spruce Picea abies, Scots pine, silver birch
Betula pendula, downy birch Betula pubescens, Norway
maple Acer platanoides, rowan Sorbus aucuparia, aspen
Populus tremula, alder Alnus glutinosa, hazel Corylus
avellana, oak Quercus robur and small-leaved lime Tilia
cordata. The deer had ad libitum access to water, minerals and a salt stone throughout the study period (26th of
January to 26th of February, 2016). The food consumed
during trials constituted more than their normal daily intake, so no additional food was provided on trial days.
Fallow deer were offered a choice between food treated
with different concentrations of HaTe2 repellent. We
used Renfor pellets (manufacturer: Lantmännen, Nyköping), a product specifically designed for cervids that contains dried beet pulp and molasses, oats, wheat, malt
sprouts, distiller's grains, corn, rapeseed and sodium
chloride (crude protein = 100 g kg−1, energy = 11.2 MJ
kg−1). We used a hand-pressurized spray bottle to apply
the repellent to pellets at three wet-weight concentrations: high (70 g kg−1), low (7 g kg−1) and control (none
applied). Testing occurred with one individual at a time
led to the entrance of a triangular pen in a corner of
their enclosure. Animals were presented with two clay
bowls (feeders, 23 cm in diameter) at 20 cm apart, containing 200 g of food each in one of two repellent combinations: no and low, or low and high. We expected that
adding repellent would alter the food quality perceived
by deer by artificially increasing defence against herbivores. The level of defence was expected to be lowest in
feeders with no repellent and highest in feeders with
high repellent concentration; the defence of low
repellent feeders should then be relative to the alternative feeder offered. Both positive and negative simultaneous contrasts have been previously demonstrated in
fallow deer (Bergvall and Balogh 2009) and are potentially important when applying repellents in forests because this may create contrasts between treated and
untreated plants, with the untreated plants themselves
having variable levels of natural plant defences.
We randomly allocated treatments and the position of
the feeders (left/right). The trial endpoint was when the
animal had eaten all the food in one of the feeders. The
remaining feeder was then removed and food weighed.
During each trial, we also recorded at which feeder the
animal initiated feeding and the number of times they
switched feeders. The former indicates whether or not
deer used visual and/or olfactory cues at a distance to
Table 1 The expected foraging responses of fallow deer for each potential mechanism of repellent function. Deer were exposed to
two-choice food trials with no and low or low and high concentrations of repellent (more repellent = more defended)
Mechanisms
Expected foraging response
Sensory cues altered
Olfactory/visual
-Fewer trials involve consumption from more defended feeder in pair
-More likely to initiate consumption at less defended feeder in pair
Gustatory/somatosensory
-Shift between feeders more often when consumption initiated at more defended feeder in pair
-Consume more from less defended feeder in pair
-More selective for less defended feeder in more defended (low-high) pair
Adverse physiological effects
Yes
-More selective for less defended food with exposure
No
-Less selective for less defended food with exposure
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select feeders, while the latter suggests the level of indecision or satisfaction with their current choice. We
performed one two-choice trial per day with each of the
seven fallow deer for 10 days, except one individual (#7)
which only participated in seven trials (thus N = 67).
Deer were involved in trials for a maximum of four consecutive days, followed by a break of at least 5 days before trials recommenced.
Statistical analyses
We tested whether initial feeder choice was a function
of relative repellent concentration within two-choice
pairs (less or more), the type of two-choice pair (no-low
or low-high) and their interaction. We fitted a generalized linear model (GLM) specifying a binomial response
variable (initial feeder = 1, otherwise = 0, for each of the
two feeders in a trial) with logit link function. We could
not include trial day and animal identity as random effects because in this logistic model, each level of these
factors necessarily consisted of equal numbers of 0’s and
1’s (i.e. where one bowl was chosen first, the other was
not). A model that included these random effects as
interaction terms with relative defence failed to
converge.
To test if the first feeder chosen in a trial had any effect on the number of times each deer switched between
feeders, we fitted a generalized linear mixed effects
model (GLMM) specifying a Poisson response distribution with log link function. We included relative defence
and pair type as fixed effects, as in the previous model.
We also included trial day and animal identity as random effects, accounting for potential effects of uncontrollable conditions on a trial day (e.g. temperature,
cloud cover, environmental noise) and of consistent foraging behaviours by individual deer (Bergvall 2009).
We used a linear mixed effects model (LMM) to test
how relative defence and type of two-choice pair affected
food consumption, including trial day and animal identity as random effects. Here, we also included trial day
as a continuous fixed effect to determine whether the
amount consumed by deer in a trial changed over consecutive trials.
Repellents often become less effective at deterring herbivores with increasing exposure. We therefore tested
how selective deer were across the five replicates of the
two types of two-choice pair. We divided the amount
consumed from the less defended feeder in each pair (no
in no-low and low in low-high) by the total consumption
across both feeders in each trial. We then fitted a LMM
with the treatment replicate number as a continuous
fixed effect and animal identity as a random effect.
We performed all statistical analyses using the ‘lme4’
package (Bates et al. 2015) in R version 3.2.2 (R Core
Team 2016). We report the significance of the type II
Wald chi-square tests derived using the ‘car’ package
(Fox and Weisberg 2011). Quantile-quantile plots were
checked for approximation of normality.
Results
All the deer consumed food from at least one feeder in
each trial. In no-low pairs (N = 33 trials), deer consumed
food from both feeders in 70% of trials, exclusively from
no-repellent feeders in 27% of trials and exclusively from
low-repellent feeders in 3% of trials. In low-high pairs
(N = 34 trials), deer consumed from both feeders in 59%
of trials, exclusively low-repellent feeders in 35% of trials
and exclusively high-repellent feeders in 6% of trials.
First feeder selected
When presented with a choice between two feeders with
no and low, or low and high concentrations of HaTe2
repellent, fallow deer were more likely to initiate trials at
the less defended feeder in the two-choice pair (relative
defence, χ21 = 5.07, P = 0.024; Fig. 2). There was no interaction between relative defence and pair type (χ21 = 0.24,
P = 0.621); pair type itself was not of interest as probabilities of selection within pairs were equal to 1 (χ21 = 0,
P = 1).
Number of feeder shifts
Deer changed feeders more often when they started the
trial at the more defended feeder (relative defence of first
feeder, χ21 = 7.84, P = 0.005; Fig. 3). The pair type and its
interaction with relative defence of first feeder were not
significant (pair, χ21 = 0.10, P = 0.752; interaction, χ21 =
0.91, P = 0.339).
Amount consumed
There was a significant interactive effect of relative defence and pair type on the amount consumed by deer:
consumption from the more defended feeder was greater
Fig. 2 The probability of fallow deer initiating consumption at each
feeder within two-choice pairs (± SE)
Stutz et al. Ecological Processes
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Fig. 3 The number of times fallow deer shifted between feeders as
a function of initial feeder selected (± SE)
in no-low pairs than in low-high pairs, while consumption from the less defended feeder was greater in lowhigh pairs than in no-low pairs (interaction, χ21 = 7.30,
P = 0.007; Fig. 4). Overall, deer ate more from the less
defended feeders in each pair (relative defence, χ21 =
44.42, P < 0.0001). Pair type and the number of trials that
deer completed had no significant effect on the total
amount of food consumed by deer in a trial (pair, χ21 =
2.66, P = 0.103; trial day, χ21 = 1.44, P = 0.230).
Selectivity as a function of exposure
The proportion of consumption comprising lower
repellent food was greater in low-high than no-low
repellent pairs (pair, χ21 = 5.71, P = 0.017; Fig. 5). Selectivity for the lower repellent food decreased with the
number of trials each deer was exposed to in both types
of two-choice pairs (replicate, χ21 = 5.79, P = 0.016). The
rate at which selectivity decreased over time was not significantly different between pair types (interaction, χ21 =
0.70, P = 0.402).
Fig. 4 The amount of food that fallow deer consumed from each
feeder. Bars indicate arithmetic means ± SE, with less defended
feeders in each pair indicated in white and more defended feeders
in grey
Fig. 5 The consumption per treatment replicate of the lower
repellent food (no in no-low and low in low-high) as a proportion of
total consumption. Shading indicates 95% confidence limits
Discussion
Browsing by large herbivores can cause significant damage to plants that are important in forestry, agriculture
and restoration, yet chemical repellents to deter browsing are not well understood from a behavioural perspective. Using simple two-choice trials with captive fallow
deer, we demonstrated the mechanisms of deterrence
operating behind a commercial herbivore repellent,
HaTe2. We found evidence of both reduced visitation to
more defended (higher repellent) feeders and reduced
consumption while there. The patterns of consumption
from differentially defended pairs of feeders supported a
mechanism that included pre-ingestive cues (olfactory
and/or visual) and lacked adverse physiological consequences post-ingestion. The two-choice tests therefore
provided critical information about the contexts in
which the repellent is likely to be effective.
In the majority of trials, the deer consumed food from
both feeders but, consistent with our predictions, they
chose the higher repellent (more defended) food less
often and very rarely consumed the higher repellent food
exclusively. Deer were more likely to initiate consumption at the lower repellent (less defended) feeder, showing some ability to differentiate between more and less
defended feeders prior to tasting. They may have used
visual or olfactory cues coupled to food quality to select
the first feeder in a trial. Fallow deer are known to be
able to use colour to discriminate between visual stimuli
(Birgersson et al. 2001). In addition, there is mounting
evidence that colour and odour are important cues used
to detect and assess palatable food plants by mammalian
herbivores that consume green vegetation, not just for
those consuming fruits and fungi (Schmitt et al. 2018;
Stutz et al. 2016; Stutz et al. 2017).
Stutz et al. Ecological Processes
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When deer did initiate feeding at the more defended
feeder, they were more indecisive, switching more often
between feeders. This behaviour is consistent with that
observed when applying compounds extracted from
birch bark (Betula spp.) to food; in a two-choice experiment consisting of test and control feeders, fallow deer
switched feeders more often when test feeders contained
higher concentrations of the extract (Bergvall et al.
2013). We suggest that repellent residue on the tongue
may have made subsequent comparisons with the other
feeder in the pair more difficult.
The absolute amount that deer consumed during trials
did not differ significantly between no-low and low-high
pairs. However, the repellent had the effect of suppressing intake of the more defended food, with deer eating a
greater amount from the less defended feeder in both
treatment pairs (no in no-low and low in low-high pairs)
. This is consistent with the idea that repellents are more
effective when there are alternative (better) food options
available (Kimball et al. 2002; Provenza 1995). Consumption of the more defended food was higher in no-low
than low-high pairs, suggesting that the repellent modified flavour (odour, taste and texture) and that flavour
intensity played a role in food selection (Villalba and
Provenza 2000).
The effectiveness of the repellent declined over time in
both two-choice pairs, with deer becoming less selective
for the less defended feeder in each pair as trials progressed. This suggests that consumption of HaTe2
repellent in food did not have significant post-ingestive
consequences for fallow deer (Kimball et al. 2009). Alternatively, the effects of toxins or digestibility-reducing
compounds in the repellent may have been partly negated by the high nutritional value of the food compared
to natural forage. Detoxification, deactivation or elimination of toxic and anti-nutritional compounds require
nutrients and water and thus can be achieved more
quickly when food is nutrient-rich (Illius and Jessop
1995; Provenza et al. 2003). The deer may therefore have
learned over successive trials that the cost of ingesting
the more defended food was not very high; as a result,
they may have reduced their effort in selecting between
feeders and instead attempted to maximize total intake
or rate of intake. This could have implications for the
use of repellents near supplementary feeding stations;
animals feeding from stations would have enhanced detoxification abilities, decreasing the effectiveness of repellents applied to surrounding trees (Provenza et al.
2003; Timmons et al. 2010).
Conclusions
Our study provides evidence that HaTe2 repellent altered both pre- and post-ingestive cues perceived by
deer and suggests that these cues were not coupled with
significant physiological consequences. This has implications for the effectiveness of the repellent both temporally and spatially: herbivore deterrence is likely to
decrease with prolonged exposure to the repellent and
with lower availability of alternative feeding options
nearby. As a result, the repellent may not be appropriate
in some contexts or require application patterns to be
modified by, for example, using rotations of different repellents to maintain novelty, leaving some plants untreated as sacrificial feed or providing supplementary
feed.
Decisions about applying herbivore-repelling chemicals to plants over large areas, such as in forestry and
agricultural operations, should be informed by the behavioural mechanisms responsible for the deterrent effects. We demonstrated how simple two-choice feeding
trials can be used to understand herbivore responses to
repellents. The characteristics of the herbivores and
plants in an area will influence these responses and thus
the effectiveness of a repellent. For example, the effectiveness of a repellent will likely be lower where the nutritive value of the plant is high relative to other
available food, there is little alternative food or the herbivore density is high. We therefore suggest that this type
of experimentation could be used to select effective
mechanisms of plant protection for particular management scenarios and reduce the risk of repellent failure in
large-scale field applications.
Abbreviations
GLMM: Generalized linear mixed effects model; LMM: Linear mixed effects
model
Acknowledgements
We thank Sven Jakobsson, Thomas Giegold, Nils Andbjer and Susanna
Gustavsson for facilitating the fieldwork at Tovetorp Research Station and
Benjamin Croak for building experimental pens.
Authors’ contributions
UAB conceived and designed the experiment. LV and RSS performed the
experiment. RSS analysed the data and wrote the manuscript; all other
authors provided editorial advice. All authors approved the final version of
the manuscript.
Funding
The Swedish Research Council FORMAS awarded to UAB. The funding body
had no role in any part of the study.
Availability of data and materials
The datasets generated and/or analysed during the current study will be
available in the Mendeley Data repository (https://doi.org/10.17632/
ycdr6yr3dx.1).
Ethics approval and consent to participate
Research procedures were approved by the Swedish National Board for
Laboratory Animals (Dnr 14–14).
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Stutz et al. Ecological Processes
(2019) 8:25
Author details
1
Department of Zoology, Stockholm University, SE-106 91 Stockholm,
Sweden. 2Grimsӧ Wildlife Research Station, Department of Ecology, Swedish
University of Agricultural Sciences, SE-730 91 Riddarhyttan, Sweden.
Received: 23 November 2018 Accepted: 29 May 2019
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