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Article

Bark Gnawing by Rodents in Orchards during the Growing Season—Can We Detect Relation with Forest Damages?

1
Department of Zoology, Fisheries, Hydrobiology and Apiculture, Faculty of AgriSciences, Mendel University in Brno, Zemědělská 1, 613 00 Brno, Czech Republic
2
Research and Breeding Institute of Pomology Holovousy Ltd., Holovousy 129, 508 01 Holovousy, Czech Republic
3
Department of Forest Ecology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemědělská 3, 613 00 Brno, Czech Republic
*
Author to whom correspondence should be addressed.
Submission received: 20 December 2021 / Revised: 6 January 2022 / Accepted: 18 January 2022 / Published: 19 January 2022
(This article belongs to the Special Issue Rodents in Crop Production Agricultural Systems)

Abstract

:
Rodent bark gnawing is common during winter in times of low or unavailable food supply. During the growing season, it is a rare phenomenon, but can occur due to low food supply and/or poor food quality resulting from climatic influence. We evaluated this unusual damage of apple tree (Malus domestica) orchards by rodents in two localities in the Czech Republic. In 2019, 24% of trees in the orchard in Brno were gnawed by the common vole (Microtus arvalis) population. Damage in the Holovousy orchard by water vole (Arvicola amphibius) was inspected in 2020 and showed that 15% of trees were damaged with massive root gnawing. These findings were compared with gnawing in forest beech plantations in 2019, with up to 13% of trees damaged. Three rodent species (Microtus agrestis, M. arvalis and Clethrionomys glareolus) participated in the damage. Detailed description of the various vole species’ damage in vegetation period, which somehow differs from winter time damage, may help in the future in early recognition and early application of plant protection in times when this phenomenon may reappear.

1. Introduction

Rodent damage to both wild and domesticated tree species is common during winter in times of low or unavailable food supply. Fruit tree damage by rodents (Rodentia) is a debated issue in many European and North American countries [1,2,3,4]. Rodents are one of the most harmful and difficult-to-control agricultural pests (e.g., [3,5]). In the case of fruit trees, rodents feed on the bark and roots, injuring and killing the trees [6,7,8,9]. Damage is most frequent in the dormant season from late autumn to early spring, when other food sources are relatively scarce and of low quality and snow cover protects foraging voles from avian and mammalian predators [1,9,10,11]. The more severe the damage to the tree bark, the greater the negative effect on fertility and life expectancy of the tree. When a large amount of bark is removed and/or the conducting tissue is interrupted completely around the tree trunk (girdling), almost every tree dies [9,12].
Among rodents, the most important pests in the temperate zone of the northern hemisphere are various voles (Microtus spp., Arvicola spp.). Local vole species periodically increase their numbers [2,13,14,15,16,17], which may lead in some conditions to their damaging effect.
Producers of various fruits in the countries of Western and Southern Europe pay great attention to the damage of fruit trees, especially by voles [7,15,16,17]. In the middle of Europe, the common vole, Microtus arvalis (Pallas, 1788) is a significant pest for fruit trees and field crops, with a considerable economic impact on agricultural and horticultural production [3,4,9]. Common vole population dynamics are characterized by multi-annual cyclic fluctuations, with population peaks occurring every two to five years [18,19,20]. Some of their population cycles are characterized by extraordinary population peaks, both in terms of the number of voles and the damage caused. Such an outbreak was recorded in 2019 and affected a few countries in Central and Western Europe [21]. In the Czech Republic, the total damage was estimated at more than 1.65 billion CZK, or approximately 61 million Euros. The most affected areas were south and central Moravia in 2019 and Czechia in 2020 [22].
The unusual damage of the apple trees (Malus domestica) in orchards by rodents in two localities in the Czech Republic was evaluated and compared with forest plantation damage from the same district and period. We are aware that the data are limited as always from one locality and the year, but growing season rodent damage is a rare phenomenon, and thus worth publishing. We assume that the detailed description of the various vole species damage in vegetation period (which somehow differ from winter time damage) may help in future in early recognition and early application of plant protection in time when this phenomenon may reappear.

2. Materials and Methods

Inspected were 901 of young fruiting apple trees (Malus domestica) in Brno (Moravia) and 593 in Holovousy (Bohemia). These were compared with inspection of 500 young trees of beech (Fagus sylvatica) close to Brno in 2019.

2.1. Experimental Plots

Orchard Brno (Moravia) (N49°9′, E016°33′): The fruit growing farm on 4.5 ha is situated in an area with other orchards of various fruit trees around three sides and a small grove on one side. We inspected part of the orchard with the Sampion variety of apple trees. The trees were in 23 rows, and each row consisted of about 70 to 80 (mean 75) trees. We selected every second row to check to get about 52% of the trees to be inspected (901 tree controlled).
This orchard was under ecological management with plant composition for flower beds between the rows of trees and then with homogenous cover: Onobrychis viciifolia, Medicago lupulina, Trifolium repens, Trifolium incarnatum, Securigera varia, Anthyllis vulneraria, Lotus corniculatus, Phacelia tanacetifolia, Sinapis alba, Camelina sativa, Festuca ovina, Festuca rubra, Malva verticillata, Daucus carota, Plantago lanceolata, and Fagopyrum esculentum. The flower beds were regularly mowed in late summer to enable long flowering period for insects.
By our preliminary inspection, damages to apple trees were spread mostly evenly in the orchard, indicating large revenue losses. By orchard farmer information on the crop losses, 20% of the trees were completely damaged by the common vole and should be removed. This counting of damage by the owner is close to our findings as, by our investigation, 24% of trees were damaged to some extent (Table 1). Rodenticides were not applied. Net protection was installed around the apple tree trunks to prevent damage by hares.
Orchard Holovousy (Bohemia) (N50°23′, E015°34′): The orchard is situated in a large area with other orchards of various fruit trees surrounding it (1 ha—4000 fruit trees). Agriculture fields are in the far distance. We inspected part of the orchard with the Gala variety of apple trees. The trees were in 13 rows, each consisted of about 40 to 50 trees (mean 45). We inspected each tree in each row counting 593 trees.
Wilting trees were easily pulled out of soil, enabling further measurement of root damages. By farmer information, all girdled and root damaged trees were removed. A two times a year-mowed grassy belt was between the tree rows. The trees were protected by underground mechanical application of rodenticides in the grassy belts. After the damage of trees by the water vole, rodenticides such as Stutox II (Agrochema Studenec: Studenec, Czech Republic) and Polytanol (Chemische Fabrik Wülfel GmbH & Co. KG: Hannover, Lower Saxony, Germany) were applied to the burrows. Tree trunks were protected by nets against hares. Differences in damage in the vegetation period were in tree trunk damage, as this species gnaw only roots, but in winter.
Hostěnice location (close to Brno, Moravia) (N49°14′, E016°46′): The 10 small sized clearings (up to 0.25 ha) were regularly inspected. Trees in beech plantations were always in rows. Fifty samples were taken from each of the plots. As to have homogenous and characteristic samples, these were chosen equally from the edges and in a quarter, one half and three quarters of plot every time 10 trees to be checked. From this locality altogether 500 of the beech trees were inspected.
Beech plantations were with various naturally grown forest plants between the rows (grasses, Juncus sp., Carex sp., Luzula sp. Rubus sp., Senecio sp., Urtica dioica and bracken being the most common). The abundance of voles and the vole species identification was assessed using snap-trapping during years of this study in each of the 10 plots [12]. A detailed description of damage on the trees was recorded, as three vole species participated. The most important difference and distinguishability of the damage was in bank vole (Clethrionomys glareolus), feeding on sap and phloem higher on tree trunks, which was obtainable only in the vegetation period.

2.2. Data Collecting

During the damage recording, the stem basal diameter d (in cm) of each sapling was recorded as: vertical length l (in cm) and horizontal extent h (in% of perimeter). The extent of gnawed bark on the sapling S (in cm2) was calculated by formula: S = π * d * h * l. The damage caused by the genus Microtus and the bank vole can be distinguished by the specific character of their gnawing: Microtus sp. gnaw deep into the stem, leaving the wood visible, while the bank voles only gnaw bark along the stems surface and leaves pieces of the darker phloem and cambium layers visible. These different gnawing strategies are related to differing digestive tract physiologies in the respective species. Voles of the genus Microtus usually gnaw bark up to 20 cm above the ground, while the bank vole also gnaws above 20 cm from the ground. Therefore, we also measured the height of gnawing above the surrounding ground to verify this imaginary border line between these two genera. By contrast, the persistent gnawing of bark and phloem by voles, especially around the whole perimeter of the sapling base (girdling), resulted frequently in the drying of the sapling and its death. Water vole, as a more fossorial species, is known to damage tree roots, but at this time, the bark on the base of tree stems was also damaged, and then its extension was measured as well as the damaged roots (after pulling the trees out of soil).

2.3. Data Analysis

To compare damaged trunk areas between forest and orchard from Moravia, the Wilcoxon rank sum test was used. The Wilcoxon test was used because the data followed extreme value distribution given by a high proportion of zero values and because the data did not meet the homogeneity of variance. This test is a sufficiently robust statistical method to analyze this kind of data. The data were analyzed in the R software (4.0.1., R Core Team: Auckland, New Zealand) [23].

3. Results

In two localities of apple tree orchards, damage to bark was inspected during the vegetation period and presented. In Table 1, details were described to show differences between orchards. In Brno, damage was done by the common vole in 2019. The area of above ground gnawed bark per tree in Brno orchard was μ = 62.126 cm2. The other orchard was situated in Holovousy, and the damage was done by a water vole (Arvicola amphibius) in 2020. The above ground bark gnawed area per tree was μ = 10.826 cm2. Further inspection found massive damage to the root system of the trees in Holovousy, which is typical for the water vole (Table 1). The area of gnawed bark on roots per tree was high (μ = 12.994 cm2).
During the vegetation period in 2019, research was also concentrated on the rodent gnawing in beech forest plantations in Moravia closed to Brno, which was compared with damage in Brno orchard. The results showed fewer damaged trees in forests (2019—W = 226,190, p < 0.0001; Figure 1), and the area of gnawed bark per tree was significantly higher in orchard in 2019 (W = 1509.5, p < 0.0001) (Figure 2).

4. Discussion

In recent years, central Europe has been affected by an intense dry period [24]. It affected population dynamics of vole species [21] and their interactions in ecosystems. Based on an observation of bark gnawing in the summers of 2019 in forests [12], this team focused on the hitherto unstudied phenomenon of bark gnawing during growing season in orchards. According to Suchomel et al. [12], bark gnawing during growing season in forests was caused by the joint influence of high rodent population density and the low quality of plant biomass as their food supply.
The greatest damage by bark gnawing in the growing season was significantly associated with the below-average precipitation in the winter of 2018/2019. Due to the lack of moisture, plant biomass contained more fiber and less nitrogen; therefore, it contained less concentrated nutrients. For this reason, a higher number of the vole species had to use tree bark, phloem or sap as an emergency food source [12]. During the monitored period in forests (2018–2020), the average annual temperatures were about 2 °C higher than the long-term average of the locality. The extremely dry period, which had lasted since 2014, was interrupted in the last year of monitoring (2020). The annual precipitation during the whole dry period was average or below-average; in 2018, the precipitation was the lowest since 1961 [12]. The climatic trends in both localities under study do not differ either from each other or from the situation in the Czech Republic, or almost the whole of central Europe [25]. The long-term combination of higher temperatures and average or below-average precipitation means an increase in potential evapotranspiration and a prolonged growing season [24], which results in less water in the landscape and reduced water availability. For all ecosystems, this means long-term stress which can lead to a number of unusual phenomena, such as changes in seed years, changes in the quantity and quality of the biomass production, and, in some cases, even in a complete change of an ecosystem (for example, destruction of the tree layer and temporary replacement by herbs, grasses and shrubs) [26]. Populations of the rodent species are influenced by the climate in different ways, both directly (survival because of winter conditions) and indirectly (via the quality and availability of food and the suitability of the environment) [27]. The resulting changes in the abundance and dominance of individual rodent species also determine the type and extent of damage [28].
The years 2018, 2019 and 2020 were exceptional for many reasons. The first is climate (mild and dry winters and springs with higher temperatures). Consequently, the lower quantity and quality of food supply and population outbreaks of rodents (field and forest species) led to exceptionally great damages during the vegetation period (in open land as well as in forests) (Figure 3a,b) [12].
Water voles usually exhibit eight- to ten-year population cycles, which operate independently from the dominant Microtus sp. and bank vole cycles (for example, in northern Europe [29,30]), but in 2019 and 2020 synchronization with the common vole population was found.
During the year of our investigation (especially in 2019), great damage by bark gnawing in orchards was recorded, especially in southern Moravia. For example, in four farms of apricot trees, damage by the common vole was evaluated to be over ten million CZK. In most of the trees, bark was girdled in the trunk base, causing the tree death. According to expert opinion, all these trees should be removed, as the trees were immediately infested with fungal diseases [personal communication and expert opinion, [7]]. In the future, climate variability may influence stability and prosperity, especially of fruit growers [12].
The occurrence of voles can also be influenced by the species composition of the herbal layer between rows in orchards. Sometimes the use of living mulch in ecologically managed (organic) orchards may influence the presence of rodents [8,31]. In our case in Brno, ecological management and various plant species (flower beds, see Materials and Methods) between the rows attracted the common vole population to invade the orchard. However, after the plant cover was completely consumed, the overcrowded population turned to the only food presented—the bark of apple trees. As the orchard was under ecological management, no chemical repellent was used against the rodents, leading to serious damage (personal information by the owner). Compared to other locality (Holovousy), grass cover, which was regularly mowed, was grown between the tree rows. Overcrowded water voles, having a low food supply, concentrated their feeding activity on roots, similar to what is usually seen in winters [32]. Plant protection in the form of chemical repellents were applied before and after the damage occurred (see Materials and Methods). It may be the case that the repellents intended for common voles were not effective enough against the water voles [33].
In upland regions of Europe, water vole (Arvicola amphibius) populations widely fluctuate, and periodic outbreaks move in waves from epicenters, devastating orchards, grasslands and young tree plantations [34]. Population cycles last six to seven years [35] with alternating phases of low-density and outbreaks, the latter of which can last two to four years [36], causing severe damage and economic losses [37]. According to Giradoux et al. [34], land use and landscape management could be a way to control water vole outbreaks. Cultivation practices strongly affected voles’ presence, especially in orchards [38].
Orchards are part of structurally simple, open agricultural landscapes with low autoregulation activities compared to forests. Therefore, they are directly affected by the overgrowth of rodents in agricultural crops. In addition, they are a suitable habitat for various species of voles [39,40].
It is very important to distinguish differences between the specific damage of the particular rodent species [33,41,42]. This is why we described damages of rodents in detail in Table 1 so they can be compared. Some differences between the marks of the vole species are already known [33,41]. In orchards, moles often contribute to water voles’ colonization success because they use its underground system to expand [37]. Therefore, we have to pay attention to all rodent species at the locality under study.
The natural food of the common vole is vegetative parts of various plants, but they will also feed on many agricultural crops within secondary habitats if available, which leads to faster reproduction than in primary habitats [43]. Their feeding activities and preferences are concentrated on aboveground green vegetation during the vegetation period. Bark as a food is not a preferred food for the common vole if enough green plant biomass is in the food supply [4,12].
The European water vole is especially known to damage young trees in orchards. Their diet throughout the year is diverse, as they feed on the green part of plants, but will also consume fruits, bulbs, twigs or buds. In the winter, their food contains rhizomes and roots of various plants if available, also damaging fruit tree roots. If there was a low food supply and its quality was poor, as in our case, roots were the main diet during the vegetation period [14,32]. In our case, it was not only the roots, but also the bark on the trunks of trees (Figure 3b).
In both of the orchards, net protection around the apple tree trunks was installed. Differences were found between the heights of bark damage on the trunk in both localities. These were caused by the common voles’ ability to go much higher by the help of nets (up to 51 cm) in some cases, because of their lower body mass compared to water voles (own observation).
Three species of rodents may participate in the damage to forest beech plantations. It is difficult to distinguish harmful activities of the voles (common vole and field vole). Bank vole is the only species that climbs, and therefore damages higher on the trunk are attributed to this species [12].
Exceptionally high damages to orchards during the vegetation period by rodents are not yet known in detail. That is why our information is so important.

5. Conclusions

Orchards are part of open agricultural landscapes, which are structurally simple and, compared to forests, are under much more plant protection activities, resulting in lower autoregulation. However, damage to young trees by various rodents during growing season occurred in both orchards and forests, even though damage was seen to a lesser extent in forests.
Our recommendation to future research on rodent damage monitoring and its prediction should be based not only on rodent density monitoring, but also on its diet supply quality, influenced by weather conditions. In the future, climate variability may influence stability and prosperity, especially of fruit growers.

Author Contributions

Conceptualization, M.H. and J.S.; methodology, J.S., M.H., J.Š., J.O. and M.S.; formal analysis, J.Š.; writing—original draft preparation, J.S. and M.H.; writing—review and editing, J.Š., J.O. and M.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Ministry of Agriculture of the Czech Republic, grant number RO1521 and grant number QK1820091.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Proportion of damaged trees in studied forests and orchard in 2019.
Figure 1. Proportion of damaged trees in studied forests and orchard in 2019.
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Figure 2. Average damage by gnawed bark area (cm2) in studied forests and orchard in 2019.
Figure 2. Average damage by gnawed bark area (cm2) in studied forests and orchard in 2019.
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Figure 3. Damage of trees in orchards by bark gnawing in 2019–2020: (a) Damage of trunk, and rootstocks by common vole (Microtus arvalis) (Brno, 2019); (b) damage of trunk and roots by water vole (Arvicola amphibius) (Holovousy, 2020). © Josef Suchomel.
Figure 3. Damage of trees in orchards by bark gnawing in 2019–2020: (a) Damage of trunk, and rootstocks by common vole (Microtus arvalis) (Brno, 2019); (b) damage of trunk and roots by water vole (Arvicola amphibius) (Holovousy, 2020). © Josef Suchomel.
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Table 1. Collected data on young trees and damage by rodents.
Table 1. Collected data on young trees and damage by rodents.
LocalityYearSpecies of Treen TreesAge (Year)Basal Diameter (cm)Apple VarietyRootstock
Brno (A)2019Malus domestica90162.6 to 12 (mean 6.53; SD 1.09)SampionP14
Holovousy (B)2020Malus domestica59351.9 to 6 (mean 3.63; SD 0.93)GalaM106
Hostěnice (C)2019Fagus sylvatica5007 to 101.2 to 8.5 (mean 2.88; SD 0.82)
Tree Trunk Damage
Localityn/%Girdled/%Vertical Length of Damage (cm)Horizontal Extent % of Damage
A218/24131/151 to 51 (mean 14.88; SD 8.71)3 to 100 (mean 76.5; SD 31.41)
B91/1548/8.12 to 24 (mean 9.27; SD 4.03)20 to 100 (mean 64.89; SD 25.67)
C63/136/1.21 to 90 (mean 14.46; SD 17.68)1 to 100 (mean 30.44; SD 26.71)
Tree Root Damage
L.Depth (cm)Horizontal Extent % of DamageManagementHarmful Rodent
A51 rootstock and basePresent/absent dataecologicalMicrotus arvalis
B11 to 42 (mean 30.73; SD 6.28)50 to 100 (mean 94.76; SD 18.42)conventionalArvicola amphibius
Cnot measurednot measuredconventionalM. arvalis, M. agrestis
C. glareolus
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Suchomel, J.; Šipoš, J.; Ouředníčková, J.; Skalský, M.; Heroldová, M. Bark Gnawing by Rodents in Orchards during the Growing Season—Can We Detect Relation with Forest Damages? Agronomy 2022, 12, 251. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12020251

AMA Style

Suchomel J, Šipoš J, Ouředníčková J, Skalský M, Heroldová M. Bark Gnawing by Rodents in Orchards during the Growing Season—Can We Detect Relation with Forest Damages? Agronomy. 2022; 12(2):251. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12020251

Chicago/Turabian Style

Suchomel, Josef, Jan Šipoš, Jana Ouředníčková, Michal Skalský, and Marta Heroldová. 2022. "Bark Gnawing by Rodents in Orchards during the Growing Season—Can We Detect Relation with Forest Damages?" Agronomy 12, no. 2: 251. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12020251

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