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Quantitative Parameters of the Body Composition Influencing Host pathogens Article Quantitative Parameters of the Body Composition Influencing Host Seeking Behavior of Ixodes ricinus Adults Joanna Kulisz 1,* , Katarzyna Bartosik 1 , Zbigniew Zaj ˛ac 1 , Aneta Wo´zniak 1 and Szymon Kolasa 2 1 Chair and Department of Biology and Parasitology, Faculty of Health Sciences, Medical University of Lublin, Radziwiłłowska 11 St., 20-080 Lublin, Poland; [email protected] (K.B.); [email protected] (Z.Z.); [email protected] (A.W.) 2 Polesie National Park, Lubelska 3a St., 22-234 Urszulin, Poland; [email protected] * Correspondence: [email protected] Abstract: Ixodes ricinus, a hematophagous arthropod species with great medical importance in the northern hemisphere, is characterized by an ability to survive prolonged periods of starvation, a wide host spectrum, and high vector competence. The aim of the present study was to determine the quantitative parameters of questing I. ricinus ticks collected in eastern Poland during the spring peak of their activity. The study consisted in the determination of quantitative parameters characterizing I. ricinus females and males, i.e., fresh body mass, reduced body mass, lipid-free body mass, water mass, and lipid mass and calculation of the lipid index. A statistically significant difference was observed between the mean values of the lipid index in females collected during the first and last ten days of May, which indicates the progressive utilization of reserve materials in the activity period. Higher activity of I. ricinus female ticks was observed during the last ten days of May despite the Citation: Kulisz, J.; Bartosik, K.; less favorable weather conditions, indicating their strong determination in host-seeking behaviors Zaj ˛ac,Z.; Wo´zniak,A.; Kolasa, S. accompanying a decline in the lipid content and the use of the “now or never” strategy. Quantitative Parameters of the Body Composition Influencing Host Keywords: Ixodes ricinus; tick parameters; questing ticks; host-seeking behavior Seeking Behavior of Ixodes ricinus Adults. Pathogens 2021, 10, 706. https://doi.org/10.3390/ pathogens10060706 1. Introduction Ticks (Acari: Ixodida) are the most important vectors of pathogens among arthropods Academic Editors: Ladislav Šimo and occurring in the Western Palearctic [1,2]. Species representing the Ixodes ricinus complex Daniel Sonenshine have the greatest medical importance associated with their ability to transmit pathogens to humans and their role in the maintenance and circulation of tick-borne pathogens and Received: 2 April 2021 diseases in animals [3–6]. Accepted: 3 June 2021 Published: 5 June 2021 In Poland, Ixodes ricinus ticks have the greatest medical importance [7–12]. The species has been shown to transmit numerous harmful microorganisms, including spirochetes, Publisher’s Note: MDPI stays neutral rickettsiae, protozoa, and viruses [9,13,14]. The genetic material of many other microorgan- with regard to jurisdictional claims in isms has been detected in I. ricinus ticks as well. However, their pathogenicity to humans is published maps and institutional affil- still being investigated [9,15,16]. The most common direct effects of I. ricinus infestations in iations. humans are skin lesions, i.e., redness at the bite site [7,17,18]. Additionally, the components of tick saliva can cause local and systemic allergic reactions. The literature has also reported cases of allergy to red meat induced by IgE Ab against alpha-gal in patients infested by this tick species [19–22]. The ability of ticks to transmit pathogens is influenced by external factors regulating Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. their host-seeking activity in the environment and modifying the risk of attacks (i.e., temper- This article is an open access article ature, relative humidity, saturation deficit, photoperiod, presence of potential hosts) [23–25], distributed under the terms and and internal factors regulated at the level of genes and gene expression [26–28]. Labora- conditions of the Creative Commons tory studies have confirmed the effect of tick-borne pathogens and other microorganisms Attribution (CC BY) license (https:// present in the tick microbiome on metabolic processes occurring in the organism of these creativecommons.org/licenses/by/ arthropods [29–32]. It has been evidenced that a decrease in the quantities of reserve 4.0/). substances, e.g., lipids, is associated with an increase in the activity and aggressiveness of Pathogens 2021, 10, 706. https://doi.org/10.3390/pathogens10060706 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 706 2 of 18 hungry ticks. This increases the chance of finding a potential host and raises the potential risk of pathogen transmission [33,34]. Lipid substances present in tick bodies serve struc- tural, signaling, and energetic functions. They are also utilized by tick-borne pathogens and have an impact on their growth and development, evasion of the immune response of the target host, and severity of symptoms of tick-borne diseases [35–37]. The aim of the present study was to determine for the first-time quantitative pa- rameters that can affect ticks’ host-seeking behavior, i.e., fresh body mass, reduced body mass, water mass, lipid-free body mass, lipid mass, and lipid index, characterizing quest- ing I. ricinus ticks collected from vegetation during the spring peak of their activity in eastern Poland. 2. Results In total, 102 adult I. ricinus ticks (64 females and 38 males) were collected during field sampling. The highest number of ticks was collected in the last ten days of May (second sampling day), at a temperature of 22.1 ◦C and 57.57% relative humidity (Table1). Table 1. Weather parameters in the study area and the number of collected Ixodes ricinus ticks. StDf Number of Active Ticks Sampling T[◦C] RH [%] [mmHg] FM 1st sampling day 18.10 54.00 20.47 25 9 Mean for 7 previous days 17.47 56.43 22.10 - - 2nd sampling day 22.1 48.00 57.25 39 29 Mean for 7 previous days 19.50 57.57 32.47 - - T—temperature; RH—relative humidity; StDf—saturation deficit; F—females; M—males. The fresh body mass (FBM) ranged from 0.53 to 1.99 mg in the group of females and from 0.27 to 0.81 mg in the group of males (Tables A1 and A2). The reduced body mass (RBM) of I. ricinus females and males ranged from 0.40 to 1.19 mg and from 0.21 to 0.52 mg, respectively (Tables A1 and A2, Figures1 and2). A statistically significant difference was found in the RBM between the groups of females collected on the first and second sampling days (Table2, Figure1). The water mass (WM) of the I. ricinus females and males ranged from 0.05 to 1.00 mg and from 0.01 to 0.38 mg, respectively (Tables A1 and A2, Figures1 and2 ). A statistically significant difference was found in the WM of males collected on the first and second sampling days (Table2, Figure2). Table 2. The results of statistical analysis. t Value p Value r Value RBM of females collected on the 1st and 2nd sampling days 2.3067 0.0244 - WM of males collected on the 1st and 2nd sampling days −2.5079 0.0168 - LFBM of females and males 15.6765 <0.0001 - Mean LM between females and males −2.1839 0.0157 - LM between females collected on the 1st and 2nd sampling days 3.9965 0.0001 - LM of males collected on the 1st and the 2nd sampling days 2.8045 0.0040 - Correlation between the RBM and LM of females - 0.0112 r(62) = 0.3153 Correlation between the RBM and LM of males - 0.0245 r(36) = 0.3644 LI values between females and males −6.1192 <0.0001 - LI values between females collected on the 1st and the 2nd sampling days 3.7796 0.0002 - LI of females and males collected on 1st sampling day −2.8502 0.0038 - RBM—reduced body mass; WM—water mass; LFBM—lipid-free body mass; LM—lipids mass; LI—lipid index; the value of p < 0.05 was considered statistically significant. Pathogens 2021, 10, 706 3 of 18 Pathogens 2021, 10, x FOR PEER REVIEW 3 of 19 FigureFigure 1. 1.A A quantitative quantitative comparisoncomparison of of the the body body components components of ofIxodesIxodes ricinus ricinus females.females. Box-plot Box-plot di- agram without outliers: Min-minimum; Max-maximum; SD-standard deviation; FBM-fresh body diagram without outliers: Min-minimum; Max-maximum; SD-standard deviation; FBM-fresh body mass; RBM-reduced body mass; LFBM-lipid-free body mass; WM-water mass; LM-lipids mass. mass; RBM-reduced body mass; LFBM-lipid-free body mass; WM-water mass; LM-lipids mass. Pathogens 2021, 10, 706 4 of 18 Pathogens 2021, 10, x FOR PEER REVIEW 4 of 19 FigureFigure 2. 2.A A quantitativequantitative comparison of of the the body body components components of ofcollected collected IxodesIxodes ricinus ricinus males.males. Box Box-- plot diagram without outliers: Min-minimum; Max-maximum; SD-standard deviation; FBM-fresh plot diagram without outliers: Min-minimum; Max-maximum; SD-standard deviation; FBM-fresh body mass; RBM-reduced body mass; LFBM-lipid-free body mass; WM-water mass; LM-lipids mass. Pathogens 2021, 10, 706 5 of 18 The lipid-free body mass (LFBM) of the I. ricinus females and males ranged from 0.39 to 0.96 mg and from 0.18 to 0.43 mg, respectively (Tables A1 and A2, Figures1 and2). A statistically significant difference was found in the LFBM of females and males (Table2). The lipid mass (LM) of the I. ricinus females and males reached values ranging from 0.00 to 0.49 mg and from 0.00 to 0.21 mg, respectively (Tables A1 and A2, Figures1 and2 ).
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