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Effects of parasites and predators on nociception: decreases analgesia reduces overwinter survival in root voles (Rodentia: Cricetidae)

ABSTRACT

Growing evidence suggests that parasite-infected prey is more vulnerable to predation. However, the mechanism underlying this phenomenon is obscure. In small mammals, analgesia induced by environmental stressors is a fundamental component of the defensive repertoire, promoting defensive responses. Thus, the reduced analgesia may impair the defensive ability of prey and increase their predation risk. This study aimed to determine whether coccidia infection increases the vulnerability to predation in root voles, Microtus oeconomus (Pallas, 1776), by decreased analgesia. Herein, a predator stimulus and parasitic infection were simulated in the laboratory via a two-level factorial experiment, then, the vole nociceptive responses to an aversive thermal stimulus were evaluated. Further, a field experiment was performed to determine the overwinter survival of voles with different nociceptive responses via repeated live trapping. The coccidia-infected voles demonstrated reduced predator-induced analgesia following exposure to predator odor. Meanwhile, pain-sensitive voles had lower overwinter survival than pain-inhibited voles in enclosed populations throughout the duration of the experiment. Our findings suggest that coccidia infection attenuates predator-induced analgesia, resulting in an increased vulnerability to predation.

KEY WORDS:
Analgesic response; coccidian infection; predation effect; small mammal

INTRODUCTION

In nature, predators and parasites constitute the two primary extrinsic population regulators and play important roles in prey/host population dynamics (Sundell 2006Sundell J (2006) Experimental tests of the role of predation in the population dynamics of voles and lemmings. Mammal Review 36(2): 107-141. https://doi.org/10.1111/j.1365-2907.2006.00083.x
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). Predation can increase parasite infection by changing the phenotypic traits of the prey (i.e., morphological and physio logic traits) (Duffy et al. 2011Duffy MA, Housley JM, Penczykowski RM, Caceres CE, Hall SR (2011) Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Functional Ecology 25(5): 945-953. https://doi.org/10.1111/j.1365-2435.2011.01872.x
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, Caetano et al. 2014Caetano JVO, Maia MR, Manica LT, Macedo RH (2014) Immune-related effects from predation risk in Neotropical blue-black grassquits (Volatinia jacarina). Behavioural Processes 109: 58-63. https://doi.org/10.1016/j.beproc.2014.07.003
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,Shang et al. 2019Shang GZ, Zhu YH, Wu Y, Cao YF, Bian JH (2019) Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia 191: 83-96. https://doi.org/10.1007/s00442-019-04455-4
https://doi.org/10.1007/s00442-019-04455...
). In turn, increased parasite infection results in hosts vulnerability to predation (Carreon and Faulkes 2014Carreon N, Faulkes Z (2014) Position of larval tapeworms, Polypocephalus sp., in the ganglia of shrimp, Litopenaeus setiferus. Integrative and Comparative Biology 54(2): 143-148.https://doi.org/10.1093/icb/icu043
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, Shang et al. 2019Shang GZ, Zhu YH, Wu Y, Cao YF, Bian JH (2019) Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia 191: 83-96. https://doi.org/10.1007/s00442-019-04455-4
https://doi.org/10.1007/s00442-019-04455...
, Gooding et al. 2020Gooding EL, Kendrick MR, Brunson JF, Kingsley-Smith PR, Fowler AE, Frischer ME, Byers JE (2020) Black gill increases the susceptibility of white shrimp, Penaeus setiferus (Linnaeus, 1767), to common estuarine predators. Journal of Experimental Marine Biology and Ecology 524: 1-6.https://doi.org/10.1016/j.jembe.2019.151284
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). For example, Møller and Nielsen (2007Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88 (4): 871-881. https://doi.org/10.1890/06-0747
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) showed that prey species with high malaria prevalence have higher predation risk than those with a low prevalence. Moose, Alces alces (Linnaeus, 1758), and voles, Microtus townsendii (Bachman, 1839), are very different in size, but both are more prone to predation when they have heavy parasite burden (Steen et al. 2002Steen H, Taitt M, Krebs CJ (2002) Risk of parasite-induced predation: an experimental field study on Townsend’s voles (Microtus townsendii). Canadian Journal of Zoology 80(7): 1286-1292.https://doi.org/10.1139/Z02-115
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, Joly and Messier 2004Joly DO, Messier F (2004) The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves? Oecologia 142(3): 586-590. https://doi.org/10.1007/s00442-004-1802-1
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). Several possible mechanisms for the synergistic effects of parasites and predators on host/prey mortality have been proposed, such as deteriorated body condition (Wirsing et al. 2002Wirsing AJ, Steury TD, Murray DL (2002) Relationship between body condition and vulnerability to predation in red squirrels and snowshoe hares. Journal of Mammalogy 83(3): 707-715. https://doi.org/10.2307/1383534
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, Hoey and McCormick 2004Hoey AS, McCormick MI (2004) Selective predation for low body condition at the larval-juvenile transition of a coral reef fish. Oecologia 139(1): 23-29. https://doi.org/10.2307/40006407
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), reduced escape ability (Alzaga et al. 2008Alzaga V, Vicente J, Villanua D, Acevedo P, Casas F, Gortazar C (2008) Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behavioral Ecology and Sociobiology 62(5): 769-775. https://doi.org/10.1007/s00265-007-0502-3
https://doi.org/10.1007/s00265-007-0502-...
), and increased metabolism and energy output (Haye and Ojeda 1998Haye PA, Ojeda FP (1998) Metabolic and behavioral alterations in the crab Hemigrapsus crenulatus (Milne-Edwards 1837) induced by its acanthocephalan parasite Profilicollis antarcticus (Zdzitowiecki 1985). Journal of Experimental Marine Biology and Ecology 228(1): 73-82. https://doi.org/10.1016/s0022-0981(98)00007-0
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, Krams et al. 2013Krams I, Kivleniece I, Kuusik A, Krama T, Freeberg TM, Mänd R, Vrublevska J, Rantala MJ, Mänd M (2013) Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle. Acta Ethologica 16(3): 163-172. https://doi.org/10.1007/s10211-013-0147-3
https://doi.org/10.1007/s10211-013-0147-...
). However, the underlying mechanism by which parasite-infected prey are more vulnerable to predation is obscure.

Animals respond to the threat of predation via a series of defensive responses, including flight, freezing, risk assessment, increased alertness and fear, or analgesia (Lima and Dill 1990Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68(4): 619-640. https://doi.org/10.1139/z90-092
https://doi.org/10.1139/z90-092...
, Kavaliers and Colwell 1994Kavaliers M, Colwell DD (1994) Parasite infection attenuates nonopioid mediated predator-induced analgesia in mice. Physiology & Behavior 55(3): 505-510. https://doi.org/10.1016/0031-9384(94)90108-2
https://doi.org/10.1016/0031-9384(94)901...
). In small mammals, analgesia induced by environmental stress factors is a fundamental component of the defensive repertoire, promoting the coordinated expression of other defensive behaviors (Colwell and Kavaliers 1993Colwell DD, Kavaliers M (1993) Evidence for involvement of endogenous opioid peptides in altered nociceptive respon ses of mice infected with Eimeria vermiformis. Journal of Parasitology 79(5): 751-756. https://doi.org/10.2307/3283615
https://doi.org/10.2307/3283615...
, Caio 2011Caio M (2011) Modulation of nociceptive-like behavior in zebrafish (Danio rerio) by environmental stressors. Psychology and Neuroscience 4(1): 149-155. https://doi.org/10.3922/j.psns.2011.1.017
https://doi.org/10.3922/j.psns.2011.1.01...
). Thus, the decreased analgesia may impair the defensive ability of small mammals and then increase their vulnerability to predation (Ives and Dobson 1987Ives AR, Dobson AP (1987) Antipredatory behaviour and the population dynamics of simple predator-prey systems. American Naturalist 130(3): 431-447.https://doi.org/10.1086/284719
https://doi.org/10.1086/284719...
, Tambeli et al. 2012Tambeli CH, Fischer L, Monaliza SL, Menescal-de-Oliveira L, Parada CA (2012) The functional role of ascending nociceptive control in defensive behavior. Brain Research 1464: 24-29. https://doi.org/10.1016/j.brainres.2012.05.010
https://doi.org/10.1016/j.brainres.2012....
, Lamana et al. 2018Lamana MS, Miranda J, Tobaldini G, Fischer L, Tambeli CH (2018) Pain chronification and chronic pain impair a defensive behavior, but not the ability of acute pain to facilitate it, through the activation of an endogenous analgesia circuit. Behavioral Neuroscience 132(6): 614-623.https://doi.org/10.1037/bne0000255
https://doi.org/10.1037/bne0000255...
).

Experimental evidence from laboratory has shown that predator or predator cues could activate the analgesic system in mice and rats (Kavaliers and Colwell 1991Kavaliers M, Colwell DD (1991) Sex differences in opioid and non-opioid predator-induced analgesia in mice. Brain Research 568(1-2): 173-177. https://doi.org/10.1016/0006-8993(91)91394-G
https://doi.org/10.1016/0006-8993(91)913...
, 1994Kavaliers M, Colwell DD (1994) Parasite infection attenuates nonopioid mediated predator-induced analgesia in mice. Physiology & Behavior 55(3): 505-510. https://doi.org/10.1016/0031-9384(94)90108-2
https://doi.org/10.1016/0031-9384(94)901...
). Meanwhile, endoparasitic infections such as coccidia or nematodes reduce this analgesia when the rodents are exposed to predator stimuli (Kavaliers et al. 2000Kavaliers M, Colwell DD, Choleris E (2000) Parasites and behaviour: an ethopharmacological perspective. Parasitology Today 16(11): 464-468. https://doi.org/10.1016/S0169-4758(00)01786-5
https://doi.org/10.1016/S0169-4758(00)01...
). Notably, most studies on nociceptive res ponses have been performed on mice and rats under laboratory conditions. Whether parasitic infections decrease analgesia in wild rodents exposed to predators and if this affects their popu lation survival remains unclear.

Our previous study showed that the combined effects of coccidia infection and predators decrease the overwinter survival of root voles, Microtus oeconomus (Pallas, 1776) (Shang et al. 2019Shang GZ, Zhu YH, Wu Y, Cao YF, Bian JH (2019) Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia 191: 83-96. https://doi.org/10.1007/s00442-019-04455-4
https://doi.org/10.1007/s00442-019-04455...
). Coccidia are the most prevalent parasites in root voles (Cao et al. 2014Cao YF, Nie XH, He H, Du SY, Duszynski DW, Bian JH (2014) Gastrointestinal parasites of root voles, Microtus oeconomus (Rodentia: Muridae), from Haibei area, Qinghai Province, China. Comparative Parasitology 81(2): 185-190. https://doi.org/10.1654/4675.1
https://doi.org/10.1654/4675.1...
, Nie et al. 2014Nie XH, Cao YF, Du SY, He H, Bian JH (2014) Intestinal parasite prevalence in root voles (Microtus oeconomus) from field enclosures. Acta Theriologica Sinica 34(2): 172-180.https://doi.org/10.16829/j.slxb.2014.02.009.
https://doi.org/10.16829/j.slxb.2014.02....
). The current study aims to evaluate whether coccidia infection increases the predation vulnerability of root voles via decreased analgesia. This work builds on the previous (Shang et al. 2019Shang GZ, Zhu YH, Wu Y, Cao YF, Bian JH (2019) Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia 191: 83-96. https://doi.org/10.1007/s00442-019-04455-4
https://doi.org/10.1007/s00442-019-04455...
) to test two hypothe ses: 1) coccidia infection reduces predator-induced analgesia in root voles; 2) individuals with reduced analgesia have lower overwinter survival.

MATERIAL AND METHODS

Statement of animal right

The use of animals in this study was in accordance with the guidelines of the regulations of experiments on animals and was approved by the animal Ethics and Welfare committee of the Northwest Institute of Plateau Biology, Chinese Academy of Science.

Laboratory experiments

The laboratory experiments were conducted at the Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, China. Root voles were housed singly in clear polyethylene cages (36 × 20 × 17 cm3) with wood shavings and maintained at 20 ± 2 °C under a 12:12 h light: dark cycle. Food and water were availed ad libitum. Twenty voles, six months and older, of each sex from a laboratory colony were divided into two groups: coccidia-infected (hereafter PA+) and parasite-free groups (hereafter PA-). Half of the PA+ and PA- groups were exposed to predator odor (hereafter PR+PA+ or PR+PA-), and the other half to a control odor (hereafter PR-PA+ or PR-PA-). Each of the four treatments involved five voles per sex, and the initial vole body mass of the four treatments did not differ (F3,36 = 0.187, p = 0.904).

Parasite infection

Voles in the PA+ group were once orally administered with 2000 coccidia oocysts suspended in 0.1 mL distilled water on June 3rd, 2019. Their oocyte levels were comparable to the oocysts per gram in the feces of coccidia-infected root voles studied by Shang et al. (2019Shang GZ, Zhu YH, Wu Y, Cao YF, Bian JH (2019) Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia 191: 83-96. https://doi.org/10.1007/s00442-019-04455-4
https://doi.org/10.1007/s00442-019-04455...
). Meanwhile, each vole in the PA- group was treated with a single orogastric gavage dose of 0.1 mL combinatorial anthelmintic comprising 6.25 × 10-4 mL diclazuril solution (Weierkong, Sichuan) and a 2 mg ivermectin tablet (Weierkong). Combinatorial anthelmintics can effectively expel nematodes, cestodes, and coccidia (Yang et al. 2018Yang YB, Shang GZ, Du SY, Zhang X, Wu Y, Bian JH (2018) Maternal density stress and coccidian parasitism: Synergistic effects on overwinter survival in root voles. Functional Ecology 32: 2181-2193. https://doi.org/10.1111/1365-2435.13129
https://doi.org/10.1111/1365-2435.13129...
).

Our pilot study found that the latency period for coccidia infection in root voles was 6-7 days, and the maximum oocyst output occurred 9-10 days post-infection. Accordingly, we measured nociceptive responses on June 13th, 2019.

Predator odor exposure

Voles were exposed to predator or control odors on June 4-13th, 2019. Silver fox, Vulpes vulpes (Linnaeus, 1758), odor was used to stimulate predation risk, while the rabbit odor, Oryctolagus cuniculus f. domesticus (Linnaeus, 1758) was used as control (Wang and Liu 2002aWang ZL, Liu JK (2002a) Effect of silver fox odor on breeding and foraging of root voles. Acta Theriologica Sinica 22(1): 22-29.https://doi.org/10.16829/j.slxb.2002.01.005
https://doi.org/10.16829/j.slxb.2002.01....
, Bian et al. 2005bBian JH, Wu Y, Liu JK (2005b) Effect of predator-induced maternal stress during gestation on growth in root voles Microtus oeconomus. Acta Theriologica 50(4): 473-482. https://doi.org/10.1007/BF03192640
https://doi.org/10.1007/BF03192640...
). Since the major predators in the study area - Buteo hemilasius Temminck & Schlegel, 1844 or Mustela altaica Pallas, 1811 - are protected animals in China, capturing and collecting fresh feces and urine for 15 consecutive days was challenging. Wang and Liu (2002aWang ZL, Liu JK (2002a) Effect of silver fox odor on breeding and foraging of root voles. Acta Theriologica Sinica 22(1): 22-29.https://doi.org/10.16829/j.slxb.2002.01.005
https://doi.org/10.16829/j.slxb.2002.01....
, 2002bWang ZL, Liu JK (2002b) The effects of silver fox odor on behaviors of root voles. Acta Ecologica Sinica 22: 554-558.) found that the silver fox odor could change the behavioral responses of root voles. Thus, our study used silver foxes for predator stimulation instead of natural predators.

Fresh silver fox and rabbit feces and urine were collected in trays under the animal cages daily. Each tray was washed with 500 mL distilled water, and the washing water strained through a filter with a 100 mesh screen (Bian et al. 2005aBian JH, Wu Y, Liu JK (2005a) Breeding behavior under temporal risk of predation in male root voles (Microtus oeconomus). Journal of Mammalogy 86(5): 953-960. https://doi.org/10.2307/4094441
https://doi.org/10.2307/4094441...
). Filtered solutions from each animal species collected at different times were thoroughly mixed. At the onset of the laboratory experiment, filter papers infused with predator or control odors were randomly placed in the vole cages three to four times a day between 8:00 am and 11:00 pm. This period was chosen because root voles are primarily diurnal (Sun et al. 1982Sun RY, Zheng SW, Cui RX (1982) Home range of the root vole Microtus oeconomus. Acta Theriologica Sinica 2: 219-231.). Each exposure to predator or control odor lasted 30-60 s.

Nociceptive responses

The nociceptive responses of voles were measured on June 3rd, 2019, prior to parasitic infection. The initial nociceptive res ponse latency did not differ among voles in the four treatments (F3,36 = 0.165, p = 0.919). Nociception was measured based on the latency of foot-lifting or licking responses to an aversive thermal stimulus (“hot plate,” CAT.NO.T-91-S, CT, USA). Each measurement was replicated thrice in each individual. The individual was immediately removed from the heated surface following the response display and returned to its cage. If no response was observed within 60 s, the test was terminated, and the vole returned to its cage (Kavaliers and Colwell 1994Kavaliers M, Colwell DD (1994) Parasite infection attenuates nonopioid mediated predator-induced analgesia in mice. Physiology & Behavior 55(3): 505-510. https://doi.org/10.1016/0031-9384(94)90108-2
https://doi.org/10.1016/0031-9384(94)901...
). In the present study, all voles displayed nociceptive responses within 60 s.

Field experiments

Field experiments were conducted at the Haibei Alpine Meadow Ecosystem Research Station, Menyuan County, appro ximately 155 km north of Xining, Qinghai Province, China (37°37’N, 101°12’E). The station has an elevation of 3200 m, is surrounded by mountains, and has an average annual temperature and precipitation of -1.6 °C and 560 mm, respectively (Li et al. 2004Li YN, Zhao XQ, Cao GM, Zhao L, Wang QX (2004) Analyses on climates and vegetation productivity background at Haibei Alpine Meadow Ecosystem Research Station. Plateau Meteorology 23(4): 558-566.).

Root vole populations in this area fluctuate annually, usually with relatively low numbers in late winter and spring, increasing throughout the breeding season, and declining after the breeding season; multi-year cycles are weak or absent (Jiang et al. 1991Jiang Y, Wei S, Wang Z, Zhen Y, Cui R (1991) Productivity investigation of the root vole (Microtus oeconomus) population in the Haibei alpine bushland (Potentilia fruticosa) I. Population dynamics. Acta Theriologica Sinica 11(4): 270-278.https://doi.org/10.16829/j.slxb.1991.04.006
https://doi.org/10.16829/j.slxb.1991.04....
). In this study area, root voles prefer dense vegetation, mainly Elymus nutans (Poaceae), in habitat selection. The average population in the habitat ranged from 217 to 280 voles ha-1 in autumn, even up to 400 ha-1 where grazing activities were limited (Bian et al. 1994Bian JH, Fan NC, Jing ZC, Shi YZ (1994) Studies on the successive relation between small mammal community and plant community in alpine meadow. Acta Theriologica Sinica 14(3): 209-216 https://doi.org/10.16829/j.slxb.1994.03.009
https://doi.org/10.16829/j.slxb.1994.03....
, Sun et al. 2002Sun P, Zhao XQ, Xu SX, Zhao TB, Zhao W (2002) Changes after snow of the population characteristics of root vole (Microtus oeconomus). Acta Theriologica Sinica 22(2): 318-320. https://doi.org/10.16829/j.slxb.1982.02.014
https://doi.org/10.16829/j.slxb.1982.02....
). The breeding season typically lasts from April to October. Juveniles reach puberty and breeding age at approximately 50 and 70 days, respectively (Liang et al. 1982Liang JR, Zeng JX, Wang ZW, Han YC (1982) Studies on growth and development in the root vole (Microtus oeconomus). Acta Biology Plateau Sinica 1: 195-208.). The primary predators in the study area are falcons, Falco tinnunculus Linnaeus, 1758, buzzards, Buteo hemilasius Temminck & Schlegel, 1844, and weasels, Mustela altaica Pallas, 1811.

Experimental facility

The field experiments were carried out in four 0.15 ha (50 × 30 m) outdoor enclosures located in an old E. nutans meadow. Major plants included E. nutans, Poa spp., Thalictrum alpinum, and Kobresia humilis. The vegetative cover provided a dense leaf layer, forming a natural refuge for root voles. The enclosures were constructed using galvanized steel panels (1.5 and 0.5 m above and below ground, respectively) but without wire mesh roofs. Further, the enclosures had a series of low panels (~0.3 m high) along the exterior walls every 10 m, allowing terrestrial and avian predators to enter but prevented voles from exiting the enclosures. The vegetation conditions are similar in each enclosure. Each enclosure was equipped with 60 laboratory-made wooden traps (Bian et al. 2011Bian JH, Wu Y, Getz LL, Cao YF, Chen F, Yang L (2011) Does maternal stress influence winter survival of offspring in root voles Microtus oeconomus? A field experiment. Oikos 120(1): 47-56. https://doi.org/10.1111/j.1600-0706.2010.18165.x
https://doi.org/10.1111/j.1600-0706.2010...
), spaced in 5 × 5 m grids.

Founder populations

Forty-eight voles of each sex, six months or older, from a laboratory colony were used to establish founder populations on October 16, 2017. The voles were divided into two nociception levels according to thermal response latency (“hot plate,” CAT.NO.T-91-S, CT, USA); high response latency group (hereafter group H; 53.92 ± 0.11) and low response latency group (hereafter group L; 49.3 ± 0.09). The nociceptive response latency of group H was significantly higher than group L (F1,94 = 1011.93, p < 0.001). Earmarked voles from group H were released into two enclosures, while earmarked voles from group L were released into the other two enclosures. Each enclosure contained 12 voles per sex, and each treatment was conducted in duplicate. The density of the founder population (160 voles ha-1) was in line with natural densities in autumn (Bian et al. 1994Bian JH, Fan NC, Jing ZC, Shi YZ (1994) Studies on the successive relation between small mammal community and plant community in alpine meadow. Acta Theriologica Sinica 14(3): 209-216 https://doi.org/10.16829/j.slxb.1994.03.009
https://doi.org/10.16829/j.slxb.1994.03....
, Sun et al. 2002Sun P, Zhao XQ, Xu SX, Zhao TB, Zhao W (2002) Changes after snow of the population characteristics of root vole (Microtus oeconomus). Acta Theriologica Sinica 22(2): 318-320. https://doi.org/10.16829/j.slxb.1982.02.014
https://doi.org/10.16829/j.slxb.1982.02....
).

Prior to the experiment, all voles were treated with a combinatorial anthelmintic to eliminate parasites and ensure homogeneity. Besides, all enclosures were trapped for two weeks to remove small resident mammals. We also ensured the initial vole body mass did not differ between the enclosures (F1,94 = 0.004, p = 0.95).

Vole trapping

Live trapping began on October 28th, 2017, after the voles had acclimated to the enclosures for two weeks, and lasted for 141 days (at the end of March 17th, 2018). Standard capture-record-recapture methods were used throughout the present study. Six trapping sessions were conducted, each consisting of three trapping days. The time interval between two trapping sessions was approximately one month. Each trap was baited with carrots, set between 8:00 am and 5:30 pm, checked every two hours and closed when trapping did not occur. Following capture, the individual was identified and their sex recorded.

Survival rate and population size estimations

We estimated the apparent survival (hereafter “survival”) and recapture probability (hereafter “recapture”) using the standard open population Cormack-Jolly-Seber model (Lebreton et al. 1992Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62(1): 67-118. https://doi.org/10.2307/2937171
https://doi.org/10.2307/2937171...
) in the MARK program (White and Burnham 1999White GC, Burnham KP (1999) Program MARK: Survival estimation from populations of marked animals. Bird Study 46(Suppl.): S120-S139. https://doi.org/10.1080/00063659909477239
https://doi.org/10.1080/0006365990947723...
). The recapture probability was evaluated under the assumption that the individual was alive and in the sample (Cooch and White 2006Cooch EG, White GC (2006) Program MARK: a gentle introduction. Available from http://www.phidot.org/software/mark/docs/book
http://www.phidot.org/software/mark/docs...
). The data comprised a capture history of 96 voles in six trapping sessions from October 28th, 2017, to March 17th, 2018. First, RELEASE in the MARK program was used to conduct a goodness-of-fit test for the global models, namely ΦTR × T, with both vole survival and recapture dependent on treatment, “TR,” and time, “T.” The goodness-of-fit of the global model was assessed by testing the assumptions of independence and homogeneity of individuals in the enclosures. The goodness-of-fit tests were not significant for voles (tests 2 and 3, RELEASE: χ 2 = 12.64, df = 18, p = 0.81), suggesting that voles in the enclosures were independent and that the model fits were acceptable. We then used a bootstrap-based goodness-of-fit test to estimate the c-hat value (a variance inflation factor; 1.92), which was adjusted to 1.92 in the global models.

Second, we selected the models as described in our previous study (Yang et al. 2018Yang YB, Shang GZ, Du SY, Zhang X, Wu Y, Bian JH (2018) Maternal density stress and coccidian parasitism: Synergistic effects on overwinter survival in root voles. Functional Ecology 32: 2181-2193. https://doi.org/10.1111/1365-2435.13129
https://doi.org/10.1111/1365-2435.13129...
). Briefly, parsimonious models were selected based on the QAICc values, which allows a compromise between bias and precision when the global model does not fit the data (Anderson et al. 1994Anderson DR, Burnham KP, White GC (1994) AIC model selection in overdispersed capture-recapture data. Ecology 75(6): 1780-1793. https://doi.org/10.2307/1939637
https://doi.org/10.2307/1939637...
) and incorporates a variance inflation factor. Third, we tested the hypothesis that nociception influences vole overwinter survival. For the test, a parsimonious model containing the treatment factor was compared with neighboring populations without the factor, using QAICc values. Subsequently, the model average was estimated from the mean monthly apparent survival probability.

We used the minimum number known alive method to estimate population sizes across trapping sessions in each enclosure. Mark-recapture sampling trials of known populations in the enclosures showed that the minimum number known alive was the best estimate of the actual population size relative to other estimators (Chambers et al. 1999Chambers LK, Singleton GR, Hinds LA (1999) Fertility control of wild mouse populations: The effects of hormonal competence and an imposed level of sterility. Wildlife Research 26(5): 579-591. https://doi.org/10.1071/WR98093
https://doi.org/10.1071/WR98093...
, Bian et al. 2011Bian JH, Wu Y, Getz LL, Cao YF, Chen F, Yang L (2011) Does maternal stress influence winter survival of offspring in root voles Microtus oeconomus? A field experiment. Oikos 120(1): 47-56. https://doi.org/10.1111/j.1600-0706.2010.18165.x
https://doi.org/10.1111/j.1600-0706.2010...
). The rate of population change for each enclosure was calculated using the following equation: rt=1/TlnNt+1/Nt, where Nt is the popu lation density at time t, Nt+1 is the population density during the subsequent trapping session, i.e., at time t +1, while T is the time interval between trapping sessions (Klemola et al. 2002Klemola T, Korpimäki E, Koivula M (2002) Rate of population change in voles from different phases of the population cycle. Oikos 96(2): 291-298. https://doi.org/10.1034/j.1600-0706.2002.960211.x
https://doi.org/10.1034/j.1600-0706.2002...
).

Statistical analysis

The vole population size (Poisson distribution) was ana lyzed using generalized linear mixed models, with log link functions in the SPSS v. 20 program (IBM, Armonk, NY, USA). Continuous variables were analyzed using a linear model. Data sampled repeatedly were analyzed using the repeated measures method, and all models were simplified by eliminating non-significant (p > 0.05) interactions. Post hoc comparisons of signifi cant effects were computed using the sequential Bonferroni post hoc procedure.

In the analyses of nociceptive responses, treatments were input into the models as fixed factors, and individual IDs were put as the random factors. In the analyses of population change rate and density, treatments and trapping sessions were input as fixed factors to test the primary and interaction effects separately. Meanwhile, enclosures were input as random factors. Since no sex differences were found for any parameter, the data for males and females were pooled during analyses.

RESULTS

Laboratory experiments

We found an effect of treatment on vole nociceptive responses (F3,34 = 8.89, p < 0.001). Compared with uninfected voles exposed to the control odor (50.70 ± 0.41; range from 49.07 to 53.7), uninfected voles exposed to the predator odor had increased nociceptive latencies (53.65 ± 0.41; range from 51.73 to 55.77), indicating the induction of analgesia (PR-PA- vs. PR+PA-, p < 0.001). However, the response latencies of infected voles after exposure to the predator odor (52.11 ± 0.41; range from 51.40 to 53.23) were lower than those of uninfected voles (PR+PA+ vs. PR+PA-, p < 0.05; Fig. 1). Thus, coccidia infection altered the vole response to predator odor.

Figure 1
Vole nociceptive latencies among the four treatments. N=10, 10, 10 and 10 for the PR+PA+, PR+PA-, PR-PA+ and PR-PA- groups, respectively. Different letters represent significant difference between four treatments (p < 0.05). Data were expressed as the mean ± SE.

Field experiments

Among the various models describing survival, model 1, 2 and 3 were parsimonious models (Table 1). The differences of QAICc value between models 1, 2 and 3 are less than 2 (the differences between model 1 and 2, 3 is 0.11 and 1.71, respectively), thus these models are considered equally valid models. The model 1, 2 and 3 included the effect of time, treatment and interaction between time and treatment, indicating that time and treatment affected vole overwinter survival (Table 1). The average overwinter survival rates in group H and group L were 0.772 ± 0.01 and 0.755 ± 0.01, respectively (Fig. 2).

Figures 2-4
Monthly apparent survival probability (2), population change rate (3) and population size (4) of root voles during the live-trapping sessions under two different groups. H signifies that root voles with high thermal responses latency; L signifies that root voles with low thermal responses latency. n = 48 and 48 for H and L groups. Data were expressed as the mean ± SE.

Table 1
Best model structures for modeling survival of the root vole population. The model with the lowest QAICc is reported for the first time. The model structure for recapture remained the best model {P(TR + TR . S + TR . T)}. The effect of treatment is abbreviated TR; time effect, T; sex effect, S. The main effects are symbolized by a plus sign (+) and specific interactions are symbolized by a dot (.), and models including all combinations of additive and interaction effects are represent by an asterisk (*).

The population change rate was affected by time (F5,12 = 10.277, p < 0.05) and the interaction between time and treatment (F5,12 = 0.785, p < 0.05). However, no effect of treatment alone was found (F1,12 = 0.06, p = 0.81), indicating that only time and its interaction with the treatment affected population change rate. The average population change rates in the group H and group L were -0.008 ± 0.01 and -0.012 ± 0.01, respectively (Fig. 3). Meanwhile, the population density was affected by time (F5,12 = 53.203, p < 0.001) and treatment (F1,12 = 14.735, p < 0.05), but not the interaction between time and treatment (F5,12 = 0.736, p = 0.611). The group L vole populations demonstrated a higher density than group H (p < 0.05). Although the former had a 23.7 % higher density than the latter during the adaptive phase (the first 13 days), its population declined sharply to a size similar to group H at the end of the experiments (March 2018, Fig. 4).

DISCUSSION

The primary finding of this research was that coccidian infection in voles reduces analgesia induced by predator risk, resulting in a lower overwinter survival in root voles.

In small mammals, analgesia can promote defensive res ponses to stimuli and is advantageous in real-time or potentially dangerous situations (Kavaliers 1988Kavaliers M (1988) Evolutionary and comparative aspects of nociception. Brain Research Bulletin 21(6): 923-931. https://doi.org/10.1016/0361-9230(88)90030-5
https://doi.org/10.1016/0361-9230(88)900...
, Rodgers 1995Rodgers RJ (1995) Neuropharmacological aspects of adaptive pain inhibition in murine “victims” of aggression. Aggressive Behavior 21(1): 29-39. https://doi.org/10.1002/1098-2337(1995)21:1<29::AID-AB2480210106>3.0.CO;2-A, Kavaliers et al. 2000Kavaliers M, Colwell DD, Choleris E (2000) Parasites and behaviour: an ethopharmacological perspective. Parasitology Today 16(11): 464-468. https://doi.org/10.1016/S0169-4758(00)01786-5
https://doi.org/10.1016/S0169-4758(00)01...
). Laboratory studies have shown that mice and rats display analgesic response when exposed to predator or predator odors (Kavaliers 1990Kavaliers M (1990) Responsiveness of deer mice to a predator, the short-tailed weasel: population differences and neuromodulatory mechanisms. Physiological Zoology 63(2): 388-407.https://doi.org/10.1086/physzool.63.2.30158503
https://doi.org/10.1086/physzool.63.2.30...
, Rebecca 2003Rebecca MC (2003) Sex differences in drug- and non-drug-induced analgesia. Life Sciences 72(24): 2675-2688. https://doi.org/10.1016/s0024-3205(03)00178-4
https://doi.org/10.1016/s0024-3205(03)00...
). For instance, Furuya-da-Cunha et al. (2016Furuya-da-Cunha EM, Souza RR, Canto-de-Souza A (2016) Rat exposure in mice with neuropathic pain induces fear and antinociception that is not reversed by 5-HT2C receptor activation in the dorsal periaqueductal gray. Behavioural Brain Research 307, 250-257. https://doi.org/10.1016/j.bbr.2016.04.007
https://doi.org/10.1016/j.bbr.2016.04.00...
) found that mice reduce pain reactivity when exposed to predators. However, parasitic infections in mice reduce the analgesia following exposure to predators (Kavaliers et al. 1997Kavaliers M, Colwell DD, Perrot-Sinal TS (1997) Opioid and non-opioid NMDA-mediated predator-induced analgesia in mice and the effects of parasitic infection. Brain Research 766(1-2), 11-18. https://doi.org/10.1016/s0006-8993(97)00521-0
https://doi.org/10.1016/s0006-8993(97)00...
). Our results supported our first hypothesis that coccidia infection reduces predator-induced analgesia in root voles. To our knowledge, the present study is the first to test this hypothesis in wild rodents.

Although various reports have highlighted the positive role of analgesia induced by stress in animal defense responses (Amit and Galina 1986Amit Z, Galina ZH (1986) Stress-induced analgesia: Adaptive pain suppression. Physiological Reveiws 66(4): 1091-1120.https://doi.org/10.1152/physrev.1986.66.4.1091
https://doi.org/10.1152/physrev.1986.66....
, Butler and Finn 2009Butler RK, Finn DP (2009) Stress-induced analgesia. Progress in Neurobiology 88: 184-202. https://doi.org/10.1016/j.pneurobio.2009.04.003
https://doi.org/10.1016/j.pneurobio.2009...
, Thomson et al. 2020Thomson JS, Deakin AG, Cossins AR, Spencer JW, Young IS, Sneddon LU (2020) Acute and chronic stress prevents responses to pain in zebrafish: evidence for stress-induced analgesia. Journal of Experimental Biology 223(14): 1-11. https://doi.org/10.1242/jeb.224527
https://doi.org/10.1242/jeb.224527...
), the causal correlation between nociception and survival at the population level is obscure. Our study is the first to exami ne whether nociceptive responses affect the overwinter survival of small mammal populations. We found that pain-sensitive voles have lower overwinter survival than pain-inhibited voles. Firstly, the average overwinter survival rate of pain-sensitive voles was lower than it of pain-inhibited voles. Secondly, some pain-inhibited voles died during the two weeks of acclimatization (October 16-28th, 2017) prior to the mark-recapture experiment. Subsequently, the population of pain-sensitive voles had a higher density than pain-inhibited voles during the first trapping session. However, the population of pain-sensitive populations declined sharply at the end of the experiment (March 17th, 2018) to a size comparable to that of the pain-inhibited populations. This result indicates that pain-sensitive voles had lower survi val throughout the experiment, which last approximately five months. Finally, the pain-sensitive voles had a higher population change rate than pain-inhibited voles. Root voles do not breed in winter (Liang et al. 1982Liang JR, Zeng JX, Wang ZW, Han YC (1982) Studies on growth and development in the root vole (Microtus oeconomus). Acta Biology Plateau Sinica 1: 195-208.) and were prevented from entering or leaving the enclosures throughout the experimental period. Thus, the higher population change rate of pain-sensitive voles was only due to lower overwinter survival. These findings support our second hypothesis that voles with reduced analgesia have lower overwinter survival.

Numerous studies have found that extrinsic factors, including parasites (Ryberg et al. 2020Ryberg MP, Skov PV, Vendramin N, Buchmann K, Nielsen A, Behrens JW (2020) Physiological condition of Eastern Baltic cod, Gadus morhua, infected with the parasitic nematode Contracaecum osculatum. Conservation Physiology 8(1): coaa093.https://doi.org/10.1093/conphys/coaa093
https://doi.org/10.1093/conphys/coaa093...
), predators (Sheriff et al. 2020Sheriff MJ, Peacor SC, Hawlena D, Thaker M (2020) Non-consumptive predator effects on prey population size: A dearth of evidence. Journal of Animal Ecology 89(6): 1302-1316.https://doi.org/10.1111/1365-2656.13213
https://doi.org/10.1111/1365-2656.13213...
), climate (Rödel et al. 2004Rödel HG, Bora A, Kaetzke P, Khaschei M, Hutzelmeyer H, von Holst D (2004) Over-winter survival in subadult European rabbits: weather effects, density dependence, and the impact of individual characteristics. Oecologia 140(4): 566-576.https://doi.org/10.1007/s00442-004-1616-1
https://doi.org/10.1007/s00442-004-1616-...
), and food (Pedersen and Greives 2008Pedersen AB, Greives TJ (2008) The interaction of parasites and resources cause crashes in a wild mouse population. Journal of Animal Ecology 77(2): 370-377.https://doi.org/10.1111/j.1365-2656.2007.01321.x
https://doi.org/10.1111/j.1365-2656.2007...
), can directly or indirectly affect animal mortality. In our field experiments, parasites are removed in both treatments, and food and climatic conditions are consistent in all four enclosures. Moreover, some laboratory studies have shown that increased analgesia can enhance the anti-predator responses, increasing the survival probability (Ornstein and Shimon 1981Ornstein K, Shimon A (1981) Pinch-induced catalepsy in mice. Journal of Comparative and Physiological Psychology 95(5): 827-835. https://doi.org/10.1037/h0077827.
https://doi.org/10.1037/h0077827...
, Lichtman and Fanselow 1990Lichtman AH, Fanselow MS (1990) Cats produce analgesia in rats in the tail-flick test: naltrexone sensitivity is determined by the nociceptive test stimulus. Brain Research 533(1): 91-94. https://doi.org/10.1016/0006-8993(90)91800-v
https://doi.org/10.1016/0006-8993(90)918...
, Tambeli et al. 2012Tambeli CH, Fischer L, Monaliza SL, Menescal-de-Oliveira L, Parada CA (2012) The functional role of ascending nociceptive control in defensive behavior. Brain Research 1464: 24-29. https://doi.org/10.1016/j.brainres.2012.05.010
https://doi.org/10.1016/j.brainres.2012....
). For instance, predator-induced analgesia promoted anti-predator behaviors in mice, which decreased mortality when exposed to cats (Ornstein and Shimon 1981). Notably, voles prefer routes with higher vegetation cover to avoid predation risk (Merken et al. 1991Merkens M, Harestad AS, Sullivan TP (1991) Cover and efficacy of predator-based repellents for Townsend’s vole. Journal of Chemical Ecology 17(2): 401-412.https://doi.org/10.1007/BF00994341
https://doi.org/10.1007/BF00994341...
, Taraborelli et al. 2008Taraborelli PA, Moreno P, Srur A, Sandobal AJ, Martínez MG, Giannoni SM (2008) Different antipredator responses by Microcavia australis (Rodentia, Hystricognate, Caviidae) under predation risk. Behaviour. 145(6): 829-842. https://doi.org/10.1163/156853908783929115
https://doi.org/10.1163/1568539087839291...
). In this study, vegetation cover was low in winter, which may have enhanced predation risk by decreasing natural shelter. Therefore, in the present study, the lower survival of voles with reduced analgesia was due to the increased vulnerability to predator, which may relate to the decreased anti-predator behaviors.

Growing evidence suggests that predators and parasites can have non-additive effects on a shared group of prey or hosts, which can influence the population dynamics (Ramirez and Snyder 2009Ramirez RA, Snyder WE (2009) Scared sick? Predator-pathogen facilitation enhances exploitation of a shared resource. Ecology 90(10): 2832-2839. https://doi.org/10.2307/25592817
https://doi.org/10.2307/25592817...
, KrkoŠek et al. 2011Krkošek M, Connors BM, Ford H, Peacock S, Mages P, Ford JS, Morton A, Volpe J, Hilborn R, Dill LM (2011) Fish farms, parasites, and predators: implications for salmon population dynamics. Ecological Applications 21(3): 897-914.https://doi.org/10.1890/09-1861.1
https://doi.org/10.1890/09-1861.1...
, Duffy et al. 2011Duffy MA, Housley JM, Penczykowski RM, Caceres CE, Hall SR (2011) Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Functional Ecology 25(5): 945-953. https://doi.org/10.1111/j.1365-2435.2011.01872.x
https://doi.org/10.1111/j.1365-2435.2011...
, Marino and Werner 2013Marino JA, Werner EE (2013) Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival. Ecology 94(12): 2697-2708. https://doi.org/10.1890/13-0396.1
https://doi.org/10.1890/13-0396.1...
). Shang et al. (2019Shang GZ, Zhu YH, Wu Y, Cao YF, Bian JH (2019) Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia 191: 83-96. https://doi.org/10.1007/s00442-019-04455-4
https://doi.org/10.1007/s00442-019-04455...
) found that predators increase both the prevalence and intensity of coccidian infection in voles through immune suppression induced by predation stress. Meanwhile, the increased coccidia infection increases the predation risk, reducing the overwinter survival and population density of voles. The number of individuals present at the beginning of the spring breeding period depends on overwinter survival. Thus, the reduced overwinter survival plays a key crucial role in subsequent population fluctuations (Shang et al. 2020Shang GZ, Yang YG, Zhu YH, Wu XQ, Cao YF, Wu Y, Bian JH (2020) A complex regulating pattern induced by the effects of predation and parasites on root vole (Microtus oeconomus) populations during the breeding season. Journal of Mammalogy 101(5): 1345-1355. https://doi.org/10.1093/jmammal/gyaa084
https://doi.org/10.1093/jmammal/gyaa084...
). The present study provides possible insights on how coccidia infection increases the infection vulnerability of root voles. We demonstrate that coccidian infection attenuates predator-induced analgesia, and the reduced analgesia increases the susceptibility to predation.

ACKNOWLEDGEMENTS

This work was Funded by the National Natural Science Foundation of China (Grant 31570421, 31870397), Strategic Priority Research Program of Chinese Academy of Sciences (Grant XDA2005010406), the Natural Science Foundation of Qinghai Province (Grant 2018-ZJ-906), Joint Grant From Chinese Academy of Sciences - People’s Government of Qinghai Province on Sanjiangyuan National Park (Grant LHZX-2020-01) and Sanjiangyuan Animal Genome Project. We thank Yan-Bin Yang for his assistance in the field work and biochemical assays.

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Publication Notes

  • Available online:

    July 7, 2021
  • Zoobank Register:

    http://zoobank.org/A3EEA8A3-3CC2-461B-B351-CD39BE778C3B
  • Publisher:

    © 2021 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Edited by

Editorial responsibility:

Carolina Arruda Freire

Publication Dates

  • Publication in this collection
    04 Aug 2021
  • Date of issue
    2021

History

  • Received
    25 Apr 2021
  • Accepted
    24 June 2021
  • Published
    07 July 2021
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