Termite mound architecture regulates nest temperature and correlates with species identities of symbiotic fungi

Termite mound architecture regulates nest temperature and correlates with species identities of symbiotic fungi
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白蚁丘结构调节巢穴温度并与共生真菌的物种特性相关

DOI:
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发表时间:
2019
期刊:
影响因子:
2.7
通讯作者:
J. Rikkinen
J. Rikkinen
中科院分区:
生物学3区
文献类型:
--
作者:
Risto Vesala;Anni Harjuntausta;Anu Hakkarainen;P. Rönnholm;P. Pellikka;J. Rikkinen

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背景 由大白蚁属白蚁建造的大型复杂土丘是许多干旱非洲景观的特征,包括肯尼亚南部察沃生态系统的稀树草原、丛林和干燥森林。白蚁与白蚁属丝状真菌专性共生。这些昆虫从环境中收集死去的植物材料,并将其存放在巢穴中,其中难以消化的细胞壁化合物被真菌有效分解。建造地上土丘是为了增强巢穴通风并维持巢穴内部有利于真菌生长的小气候。目标 在察沃生态系统中,两种大白蚁物种与三种不同的白蚁共生体相关,每个白蚁巢内始终单一培养一种真菌物种。由于白蚁物种之间和内部的蚁丘结构差异很大,我们探索了巢穴温度调节策略和真菌共生体的物种特性之间的潜在关系。方法测量了 164 个大白蚁丘的外部尺寸,并通过对核糖体 DNA 的内部转录间隔区 (ITS) 区域进行测序来鉴定培养的白蚁属物种。我们还记录了几个白蚁丘的年度温度状况,以确定不同季节白蚁丘结构和巢穴温度之间的关系。结果 土丘结构对巢穴温度有重大影响。具有开放式通风系统的大土堆记录的温度总是相对较低,而具有封闭式通风系统的土堆和具有开放式通风系统的小土堆的内部温度始终较高。三种真菌共生体在不同土丘中的分布并不是随机的,其中一种真菌仅限于“热巢”。结论我们的结果表明,不同的鸡蚁菌种对温度的要求不同,其中一种栽培种相对不耐低温。我们研究区域的优势大白蚁物种可以明显改变其土丘结构,以满足几种不同共生体的热需求。然而,共生体身份和土丘结构之间似乎存在危险的平衡,因为嗜热真菌物种的维持显然需要减少土丘结构,这反过来又导致气体交换不足。因此,我们的研究得出的结论是,虽然小土丘的有限通风能力严格限制了昆虫群体的生长,但在这种情况下,改善巢穴通风必然会导致巢穴温度过低,对共生真菌产生负面影响。
Background Large and complex mounds built by termites of the genus Macrotermes characterize many dry African landscapes, including the savannas, bushlands, and dry forests of the Tsavo Ecosystem in southern Kenya. The termites live in obligate symbiosis with filamentous fungi of the genus Termitomyces. The insects collect dead plant material from their environment and deposit it into their nests where indigestible cell wall compounds are effectively decomposed by the fungus. Above-ground mounds are built to enhance nest ventilation and to maintain nest interior microclimates favorable for fungal growth. Objectives In Tsavo Ecosystem two Macrotermes species associate with three different Termitomyces symbionts, always with a monoculture of one fungal species within each termite nest. As mound architecture differs considerably both between and within termite species we explored potential relationships between nest thermoregulatory strategies and species identity of fungal symbionts. Methods External dimensions were measured from 164 Macrotermes mounds and the cultivated Termitomyces species were identified by sequencing internal transcribed spacer (ITS) region of ribosomal DNA. We also recorded the annual temperature regimes of several termite mounds to determine relations between mound architecture and nest temperatures during different seasons. Results Mound architecture had a major effect on nest temperatures. Relatively cool temperatures were always recorded from large mounds with open ventilation systems, while the internal temperatures of mounds with closed ventilation systems and small mounds with open ventilation systems were consistently higher. The distribution of the three fungal symbionts in different mounds was not random, with one fungal species confined to “hot nests.” Conclusions Our results indicate that different Termitomyces species have different temperature requirements, and that one of the cultivated species is relatively intolerant of low temperatures. The dominant Macrotermes species in our study area can clearly modify its mound architecture to meet the thermal requirements of several different symbionts. However, a treacherous balance seems to exist between symbiont identity and mound architecture, as the maintenance of the thermophilic fungal species obviously requires reduced mound architecture that, in turn, leads to inadequate gas exchange. Hence, our study concludes that while the limited ventilation capacity of small mounds sets strict limits to insect colony growth, in this case, improving nest ventilation would invariable lead to excessively low nest temperatures, with negative consequences to the symbiotic fungus.