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Water Balance of Freeze-Tolerant Insect Larvae Inhabiting Arid

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Water Balance of Freeze-Tolerant Insect Larvae Inhabiting Arid Евразиатский энтомол. журнал 14(1): 37–41 © EUROASIAN ENTOMOLOGICAL JOURNAL, 2015 Water balance of freeze-tolerant insect larvae inhabiting arid areas in Eastern Siberia (Yakutia, Russia) Âîäíûé áàëàíñ ìîðîçîòîëåðàíòíûõ íàñåêîìûõ, îáèòàþùèõ â óñëîâèÿõ ñóõîãî êëèìàòà Âîñòî÷íîé Ñèáèðè (ßêóòèÿ, Ðîññèÿ) N.G. Li Í.Ã. Ëè Institute for Biological Problems of Cryolithozone, Russian Academy of Sciences, Siberian Branch, Lenina Ave. 41, Yakutsk, Republic Sakha (Yakutia) 677980 Russia. E-mail: [email protected] Институт биологических проблем криолитозоны СО РАН, пр. Ленина 41, Якутск, Республика Саха (Якутия) 677980 Россия. Key words: Aporia crataegi, Upis ceramboides, Pieris rapae, Delia floralis Fallen, resistance to drought, cuticle water permeability, rates of water loss, metabolic rates, cocoon, Eastern Siberia. Ключевые слова: Aporia crataegi, Upis ceramboides, Pieris rapae, Delia floralis Fallen, устойчивость к засухе, водопроницаемость кутикулы, скорость потери воды, скорость метаболизма, кокон, Восточная Сибирь. Abstract. Climate in Yakutia is characterized by low winter лежащие к Dipera, характеризуются высокой проницае- and hot summer temperatures that cause extreme low air мостью клеточной стенки тела. Это связано с тем, что humidity dropping down to 30 % seasonally. Therefore, in- биологический цикл развития этих видов сопровождает- sects in Yakutia are seasonally faced with extremely dry air ся низкой степенью экспозиции по отношению к сухому which necessitated them to evolve special adaptation mecha- воздуху. Для них замерзание клеточной жидкости, иници- nisms. In this study the estimation of water balance for freeze- ированное лёд-нуклеирующими белками, вероятно, яв- tolerant insect larvae, Aporia crataegi L., Upis ceramboides ляется существенной частью водосохраняющего меха- L., Pieris rapae L., Delia floralis Fallen, was based on mea- низма в зимний период. В противоположность этим видам, surements of rates of water loss, respiration and total water гусеницы Aporia crataegi L. обитают в условиях высокой content. It would appear that Upis ceramboides, Pieris rapae степени экспозиции к сухому воздуху и поэтому имеют and Delia floralis larvae have a high permeability for their низкую кутикулярную водопроницаемость, сравнимую body wall that is associated with low degree of their resistance с таковой для африканских жуков. Этот механизм позво- to dry air. For these larvae, freezing of body liquid initiated by ляет данному виду сохранять до 70 % воды в организме, ice nucleating proteins seems to be a sufficient part of their несмотря на экстремально низкую влажность воздуха в water saving mechanism during winter. However, Aporia cra- окружающей их среде. В соответствии с данным исследо- taegi caterpillars highly exposed to dry environmental condi- ванием, другой механизм поддержания водного баланса в tions have low cuticular water permeability similar to that of зимний период, связанный с продукцией лёд-нуклеиру- African beetles. This mechanism allows the insect to retain ющих белков, не является существенным для данного significant amounts (up to 70 %) of water within their bodies вида. Наконец, кокон, в котором гусеницы находятся с despite the extreme dry conditions that surround them. This осени, всю зиму и весной, также защищают их от дегидра- study shows that the water balance of these larvae during тации в «сухие» сезоны года. winter associated with the production of ice-nucleating pro- teins transforming water into ice in an insect’s haemolymph is insufficient for the species investigated. Furthermore, the co- Introduction coon protects the caterpillars from desiccation from early One of the most important environmental factors autumn until spring. determining the performance of insects in dry areas is Резюме. Климат в Якутии характеризуется низкими the level of humidity. There are few general survival зимними и высокими летними температурами, что являет- strategies used by insects to be drought resistant. They ся причиной высокой степени сухости воздуха, достигаю- either may evolve ability to tolerate extensive loss of щей 30 % в отдельные периоды. Поэтому насекомые, оби- body water by means of anhydrobiosis [Cornette et al., тающие в таких условиях, выработали в процессе эволюции 2011] or they may develop drought tolerance by reduc- определенные механизмы адаптации. В данном исследова- ing transcuticular permeability of their body wall [Lund- нии оценка водного баланса для нескольких морозотоле- heim, Zachariassen, 1993]. Finally, they may use behav- рантных видов (Aporia crataegi L., Upis ceramboides L., ioral implications for avoiding excessive water loss such Pieris rapae L., Delia floralis Fallen, личинки, принадлежа- щие Diptera) была основана на измерении скорости потери as migration to protected sites [Holmstrup, 2001]. воды, скорости метаболизма и содержания воды в орга- Climate in Yakutia is characterized by low winter and низме. В соответствии с полученными данными, Upis hot summer temperatures that cause extreme low air ceramboides, Pieris rapae, Delia floralis, личинки, принад- humidity reaching up to 30 % in varied periods [Shver, 38 N.G. Li ) r –2,0_ venting it from excessive water loss [Kristianssen et al., u o h 2009]. Interestingly, that this species is not only freeze _ / –2,5 g ( tolerant, but has also developed ability to supercool- s _ s –3,0 ing. The study was based on measurements of rates of o l _ water loss and metabolism of the larvae and data were r –3,5 e t then related to water balance curve of the African desert a _ w –4,0 beetles obtained by Zachariassen with co-authors [Za- f o y =0,902x –3,48 _ chariassen et al., 1987]. According to fig. 1, the regres- e –4,5 t a r sion line presents the rates of water loss of various _ g –5,0 o species of African beetles that linearly relate to their L –5,5 metabolic rate implying that the line provides an ap- _ _ _ _ _ –3 –2 –1 0 1 2 proximate measure of the rate of respiratory water loss. Log metabolic rate ( lO2 /min) It was concluded that due to low air humidity in the frozen pupal chambers under the bark in winter and Fig. 1. Rate of water loss and metabolic rate of Acanthocinus poor water diet in the combination with low humidity in aedilis larvae (redrawn after [Kristiansen et al., 2009]. Solid line summer, the Siberian timberman is likely to have the presents rate of transpiratory water loss of East African habitat similar water balance problems as African insects and carabids and tenebrionids, plotted as a function of their therefore their cuticular water permeability was close to metabolic rate [Zachariassen et al., 1987] that of African beetles. The study [Kristianssen et al., Ðèñ. 1. Ñêîðîñòü ïîòåðè âîäû è ñêîðîñòü ìåòàáîëèçìà 2009] apparently testifies that supercooled state of over- ëè÷èíîê Acanthocinus aedilis, ðèñ. âçÿò èç [Kristiansen et al., 2009]. Ðåãðåññèîííàÿ ëèíèÿ ïðåäñòàâëÿåò ñêîðîñòü ïîòåðè wintering insects seems to be the most critical factor òðàíñïèðàòîðíîé âîäû âîñòî÷íî-àôðèêàíñêèìè æóêàìè determining their low transcuticular permeability. More ñåìåéñòâà Carabidae è Tenebrionidae êàê ôóíêöèÿ èõ ñêîðîñòè data is required for understanding extent, to which wa- ìåòàáîëèçìà [Zachariassen et al., 1987]. ter balance depends from cold adaptation strategy. To fill a gap in this field, freeze tolerant Aporia crataegi L. Izumenko, 1982; Gavrilova, 2003]. Therefore, insects in caterpillars (Lepidoptera: Pieridae) were used in this Yakutia seasonally face extremely dry air conditions. research to learn the mechanism they use to adapt to Investigation of adaptation mechanisms to extreme con- dry air conditions in central Yakutia, as compared to ditions is a matter of significant interest but the problem other insects inhabiting this region. has not been yet systematically studied. As broadly known, insects inhabiting temperate and Materials and Methods cold regions evolve two general strategies to be cold hardy. They may seek to avoid freezing, in many cases Insects. Leaf nests, each containing a few caterpil- by allowing their body fluids to stay supercooled at low lars, were collected in the vicinity of the Russian city temperatures, or they may develop tolerance to freezing Yakutsk (62° N, 130° W) in different seasonal periods [Salt, 1961; Lee, 2010]. Usually, freeze-avoiding insects when experiments were planned to be conducted. Be- avoid freezing by removing or inactivating all particles fore the experiments the caterpillars were removed from that potentially may cause freezing. Insects surviving their nests and were kept at +4 °C during 2 hours for freezing establish a protective extracellular freezing at a cleaning their gut. high subzero temperature by the aid of potent extracel- Only overwintering specimens were used without pre- lular ice nucleating agents (INAs), produced for this incubation at +4 °C because their guts were empty. The function [Zachariassen et al., 2011]. mean initial body weight of the caterpillars was 8.3 mg. In their studies, Lundheim and Zachariassen stated Determination of seasonal variations in water con- that because the vapour pressure of ice is lower than tent. To determine water content the caterpillars were that of supercooled water at the same temperature the dried to constant weight at 60°C. Weight loss was hibernating freeze avoiding (supercooled) insects may determines by weighing the animals before and after lose substantial amounts of body water during winter desiccation on a Mettler AC88 balance. [Lundheim, Zachariassen, 1993]. Therefore, freeze avoid- Preparation of hemolymph samples.
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