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Short Communication - Effect of Temperature on Reproductive Fitness of the Engorged Tick, Haemaphysalis longicornis (Acari: Ixodidae).

Byline: Qingying Jia, Hui Wang, Tianhong Wang, Na Dong, Shuguang Ren, Xiaolong Yang, Jingze Liu and Zhijun Yu

Abstract

The tick Haemaphysalis longicornis is of great medical and veterinary importance, and can transmit a great diversity of pathogens. The current study investigated the effects of temperature on reproductive fitness of the engorged H. longicornis, results indicated that the engorged H. longicornis could survive all treatments at 0AdegC and 4AdegC, and pre-ovipositon periods were prolonged after 0AdegC, 4AdegC and 40AdegC treatment, whereas it was shortened after 37AdegC stress (P<0.05). The oviposition periods were varied among different temperature treatments, and the 0AdegC and 4AdegC treatments showed no influences, whereas the prolonged exposure to high temperatures (37AdegC and 40AdegC) led to a shorter oviposition periods which subsequently resulted in a low REI.

Most incubation periods of eggs were shortened after temperature treatments on the engorged H. longicornis, and 37AdegC stress for more than 10 days resulted in no hatchment. Stress at 0AdegC on engorged ticks caused no effects on egg viability, whereas 4AdegC and prolonged 37AdegC and 40AdegC treatments on engorged H. longicornis decreased the hatchment rate of their eggs. These findings suggest that the tick H. longicornis could adapt a wide range of climate conditions and showed high tolerance to cold and low tolerance to heat.

Key words

Haemaphysalis longicornis, Temperature stress, Oviposition, Fecundity.

As obligate hematophagous ectoparasites, ticks are recognized as notorious arthropod vectors which transmit the most diversity of pathogens and rank second only to mosquitoes causing life-threatening zoonotic diseases (Sonenshine and Roe, 2014). To date, approximately 900 species of ticks have been described and they have a worldwide distribution from arctic to tropical regions (Dantas-Torres et al., 2012). Climate is one of the main limiting factors which influences the geographical distribution of a tick species (Estrada-Pena, 1999; Despins, 1992), and the questing activities, offhost inter-stadial periods and development of ticks are largely depending on the ambient temperatures (Randolph, 2004).

However, survival abilities under extreme environmental conditions are varied among species (Dantas-Torres et al., 2012; Dantas-Torres and Otranto, 2011), and probably playing vital roles in population maintenance of ticks (Randolph, 2004). Hence, information on the effects of temperature on life cycle and biological characteristics of ticks is important for future control measures making (Adejinmi and Akinboade, 2011; Khalid et al., 2017).

The tick Haemaphysalis longicornis is widely distributed in New Zealand, Australia (Tenquisf and Charleston, 2001) and Eastern Asia (Teng and Jiang, 1991), and can transmit a wide variety of pathogens including spotted fever group Rickettsia, Borrelia, Bartonella, Anaplasma, Ehrlichia, Theileria and Babesia (Yu et al., 2015). Recently, it has been proved to serve as reservoir and vector of severe fever with thrombocytopenia syndrome virus, which has caused many death in China, Japan and Korea (Luo et al., 2015). The whole life cycle of H. longicornis requires a mean duration of 135.8 days under laboratory conditions (Liu and Jiang, 1998), whereas under field conditions, the development periods vary dramatically in different months caused by fluctuating environmental conditions (Zheng et al., 2011).

Therefore, it remains need to be determined how the temperature stress affects the biological characteristics of the tick H. longicornis. In the current study, the engorged female ticks were stressed at different temperatures, and their survival and reproductive fitness were analyzed, which would provide more information on future forecast of tick dispersion under global climate changes, and advance our knowledge for the control of tick-borne diseases.

Materials and methods

All ticks used in this study were the second generation ticks originated from the adult H. longicornis collected from vegetation by flag-dragging in Xiaowutai National Natural Reserve Area (39Adeg50'to 40Adeg07'N, 114Adeg47' to 115Adeg30'E) in Hebei Province, north China. They were allowed to feed on the ear of rabbits, and the non-parasitize stages were maintained in colony incubator under laboratory conditions (23+-1AdegC, 75+-5% RH with a light: dark regime of 6: 18 h). The engorged females were collected and used on the day detached freely.

After detachment, the engorged females were rinsed with water, dried with tissue paper, and weighed individually. Females that within the normal range of the engorged body weights (174.3-317.7 mg) were placed into individual glass tubes. A group of 3 females was maintained in colony incubator and served as control. The remaining groups (three females each) were exposed to 0AdegC and 40AdegC for 12 h, 24 h, 48 h and 72 h, and at 4AdegC and 37AdegC for 5 d, 10 d, 15 d and 20 d, respectively. Each single female was observed daily, and after above exposure they were transferred back to the colony incubator.

After stressed at different temperatures, the mortality of the engorged female H. longicornis was determined. Biological characteristics of the survived females including pre-ovipositon period (number of days from detachment to the beginning of oviposition), oviposition period (number of days from the beginning to the end of oviposition), egg mass laid and the incubation period of the eggs (number of days from the beginning of oviposition to the hatching of the first larva) were recorded, and then the reproductive efficiency index (REI) (number of eggs/weight of the engorged female) was calculated (Dantas-Torres and Otranto, 2011). Analysis of variance was employed to test for the statistical significance of group differences using Statistica V6.0 (StatSoft, USA).

Results

The effects of temperature stresses on reproductive fitness of the engorged tick H. longicornis were listed in Table I. The engorged H. longicornis could survive all the time treatments at 0AdegC and 4AdegC, and both the temperature stress increased the pre-oviposition periods (P<0.05), except the group stressed at 4AdegC for 20 days failed to oviposit. When stressed at 37AdegC and 40AdegC, the prolonged exposure time (48 h and 72 h at 40AdegC, 15 days and 20 days at 37AdegC) resulted in 67% mortality of engorged H. longicornis. When stressed at 37AdegC, the 5 days and 10 days exposure groups showed shorter preoviposition periods (P<0.05). When stressed at 40AdegC, the 12 h and 24 h exposure prolonged the preoviposition periods (P <0.05) (Table I).

For the oviposition periods of H. longicornis, most temperature stresses showed no effects, except the groups exposed at 37AdegC for 5 days and 10 days, and 40AdegC for 24 h (P 0.05). With prolongation of time exposure at 4AdegC, 37AdegC and 40AdegC, the REI of H. longicornis declined progressively. The incubation periods were shortened when stressed at 37AdegC for 5 days and 40AdegC for 12 h, and at 0AdegC regardless of the exposure time (P0.05), whereas other treatment groups all resulted in low hatchments (Table I).

Discussion

Thepresentstudyinvestigatedtheeffectsoftemperature stress on fecundity of the engorged H. longicornis. Results indicated that the engorged H. longicornis showed high tolerance to cold and low tolerance to heat, as exposure at 37AdegC for 15 days and 20 days, and at 40AdegC for 48 h and 72 h resulted in 67% mortality, whereas no mortality was observed when stressed at 0AdegC and 4AdegC, though these stressed at 4AdegC for 20 days failed to oviposition. The high temperature stress (~40AdegC) resulting in death of H. longicornis has been described previously (Heath, 2016). The tick H. longicornis is found freeze susceptible, and the low temperature stress can enhance the cold hardiness of unfed ticks (Yu et al., 2014).

In China, the unfed nymphal and adult H. longicornis are able to survive overwinter in the field, and the adults are active from April when the lowest teperature around 5AdegC to September with lowest temperature around 10AdegC, which offers possibilities to meet low temperatures for engorged females (Zheng et al., 2012 In New Zealand, all fed and unfed stages of H. longicornis as well as eggs can overwinter (Heath, 2016). All of these demostrated considerable level of cold tolerance of the engorged H. longicornis.

Table I.- The effect of temperature on the reproductive parameters of the engorged female Haemaphysalis longicornis.

Temp.###Time###Engorgement weights###Mortality###Pre-ovipositon###Oviposition period###REI###Incubation period###Hatchment rate

###(mg)###(%)###period (d)###(d)###(d)###(%)

###Range###Mean+-###Range###Mean+-###Range###Mean+-###Range###Mean+-###Range###Mean+-###Range###Mean+-

###SEM###SEM###SEM###SEM###SEM###SEM

23AdegC###-###215.8-262.5 243.5+-14.2###0###4-6###5.0+-0.6a###14-15###14.7+-0.3a###8.5-9.6###9.1+-0.3a###22-24###23.0+-0.6a###87.9-97.6###92.8+-2.8a

40AdegC###12h###231.3-238.8 235.3+-2.2###0###8-13###10.7+-0.5b###13-16###14.0+-1.0a###8.9-10.1###9.5+-0.3a###16-20###18.3+-1.2b###91.6-93.6###92.8+-0.6a

###24h###183.6-284.0 220.2+-32###0###10-12###11.3+-0.7b###7-11###9.3+-1 2b###6.3-7.8###7.0+-0.5b###21-24###22.0+-1.0a###32.5-48.9###40.6+-4.7b

###48h###208.8-230.7 221.7+-8.5###67###10###10.0###11###11.0###0-8.7###2.9+-2.9###24###24.0###0-38.9###13.0+-13.0b

###72h###174.3-257.7 225.6+-25.9###67###15###15.0###9###9.0###0-5.2###1.7+-1.7###NA###NA###NA###NA

37AdegC###5d###201.1-291.8 255.7+-26.2###0###2-4###3.0+-0.6b###15-18###16.3+-0.9b###9.4-10.2###9.9+-0.3a###31-39###36.0+-2.5b###4.9-38.4###17.0+-10.7b

###10d###195.1-181.2 234.0+-25.2###0###2-4###3.0+-0.6b###5-17###9.3+-3.8b###3.2-6.2###3.8+-1.2b###NA###NA###NA###NA

###15d###180.9-243.6 212.2+-18.1###67###3###3.0###7###7.0###0.6-7.7###3.0+-2.4###NA###NA###NA###NA

###20d###212.1-254.0 237.9+-13.0###67###3###3.0###5###5.0###0-4.4###1.5+-1.5###NA###NA###NA###NA

4AdegC###5d###235.3-280.9 257.0+-13.2###0###10-11###10.3+-0.3b###11-19###13.3+-2.8a###10.0-10.1 9.8+-0.3a###19-24###21.0+-1.5a###70.9-92.6###84.9+-7.0b

###10d###224.5-251.9 237.0+-8.0###0###15-16###15.3+-0.3b###11-13###12.0+-0.6a###4.0-10.1###7.2+-1.8b###20-23###21.3+-0.9a###42.6-80.0###58.8+-11.1b

###15d###179.3-294.3 228.0+-34.3###0###22-26###24.7+-1.3b###10-13###12.0+-1.0a###1.8-9.2###4.9+-2.2###21###21.0###0-36.5###15.6+-10.9

###20d###228.4-317.7 262.4+-27.9###0###NA###NA###NA###NA###NA###NA###NA###NA###NA###NA

0AdegC###12h###186.1-222.7 208.9+-11.4###0###7-8###7.3+-0.3b###12-19###14.7+-2.2a###10.5-11.1 8.9+-0.2a###18-23###20.0+-1.5b###85.4-95.9###87.9+-5.1a

###24h###232.5-291.7 254.9+-18.5###0###7-9###8.0+-0.6b###14-16###15.0+-0.6a###9.9-10.5###8.2+-0.2a###18-19###18.2+-0.3b###85.1-95.3###91.2+-3.5a

###48h###203.4-238.1 223.0+-10.3###0###8-9###8.7+-0.3b###12-14###12.7+-0.7a###10.7-11.3 8.9+-0.2a###18-19###18.2+-0.3b###80.0-95.0###85.9+-4.6a

###72h###180.1-224.5 208.3+-14.2###0###8-10###8.7+-0.7b###14-15###14.3+-0.3a###9.8-10.7###8.2+-0.3a###20-21###20.7+-0.3b###81.5-90.8###86.6+-2.7a

Pre-ovipositon periods of H. longicornis were prolonged after 0AdegC, 4AdegC and 40AdegC treatment, whereas it was shortened after 37AdegC stress (P<0.05), which indicated that the engorged H. longicornis could adapt a wide range of temperatures. This has been proved by the long active months from April to September in the field (Zheng et al., 2012). Correspondingly, the tick Rhipicephalus sanguineus has been reported to oviposit at 37AdegC (Jacobs et al., 2004), whereas oviposition did not occurr in H. leachi leachi (Adejinmi and Akinboade, 2011). Possible explanation may attribute to the different metabolic rates of theses ticks when facing extreme conditions (Adejinmi and Akinboade, 2011).

The oviposition periods of H. longicornis were varied among different temperature stress, and the 0AdegC and 4AdegC treatment showed no influences, whereas the prolonged exposure to high temperatures (37AdegC and 40AdegC) led to a shorter oviposition periods which subsequently resulted in a low REI. Additionally, the 4AdegC treatment for 10 days and 15 days also resulted in a low REI, which suggested that the low temperature treatments still cause some harmful effects on the tick H. longicornis though the exposure time was not long enough to stop oviposition. Similar phenomenon was also observed in R. sanguineus stressed at 8AdegC for 60 days which could also oviposit but without hatchement (Dantas-Torres and Otranto, 2011). Most incubation periods of eggs were shortened after temperature treatment on the engorged H. longicornis, and 37AdegC stressed for more than 10 days resulted in no hatchment.

Treatments at 0AdegC on engorged ticks displayed no effects on egg viability, whereas 4AdegC, and pronlonged 37AdegC and 40AdegC treatments on engorged H. longicornis decreased the hatchment rate, and this may due to that the engorged females have started oviposition during temperature stress, and hence the eggs were also subjected to stress.

Conclusions

The results obtained in the current study suggested that the tick H. longicornis could adapt a wide range of climate conditions and showed high tolerance to cold and low tolerance to heat. These findings advanced our knowledge on the field adaptation of H. longicornis and provided new insights into the epidemiology of H. longicornis-borne diseases. However, further investigation remains required to explore the intriguing adaptation of this tick species under background of global climate changes.

Acknowledgements

This work was supported by National Natural Science Foundation of China (31400342), the Natural Science Foundation of Hebei Province (C2015205124) and Natural Science Research Programs of the Educational Department of Hebei Province (BJ2016032).

Statement of conflict interest

The authors have no competing interests.

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Author:Jia, Qingying; Wang, Hui; Wang, Tianhong; Dong, Na; Ren, Shuguang; Yang, Xiaolong; Liu , Jingze; Yu,
Publication:Pakistan Journal of Zoology
Article Type:Report
Date:Feb 28, 2018
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