The role of temperature in reproductivity trade-offs and life span in a winter-adaptive arthropod

doi:10.21203/rs.3.rs-1855609/v1

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The role of temperature in reproductivity trade-offs and life span in a winter-adaptive arthropod

https://doi.org/10.21203/rs.3.rs-1855609/v1

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Temperature plays a key role in the development and population maintenance of arthropods, especially for those living in cold environments. In the temperate zone, one of the most common soil-dwelling arthropods is Collembola. Instead of tracking warm and thermal temperature ranges, some Collembola species are psychrotrophic, i.e., they are well-adapted to lower temperatures. We investigated Desoria ruseki (Isotomidae), a Collembola species widely distributed in high latitudes in the Palearctic and adapted to winter, to determine the crucial temperature conditions for the sustainability of field populations of this winter-adaptive arthropod. We incubated the adult individuals of the species at six temperatures ranging from − 5°C to 30°C for 98 days. We found that 0°C and 5°C, corresponding to the temperatures when the species is active in the field between late autumn (November) and early spring (April), were the best temperatures for the survival of the lab individuals. However, they died out quickly at temperatures above 20°C without laying eggs. In contrast, the species could lay eggs between 0℃ and 15℃: the higher the temperature was, the earlier they laid eggs. In addition, longer periods were needed for juveniles to hatch from eggs at lower temperatures. Our study indicates that, rather than colder conditions, hotter environments are likely to be more detrimental to the winter-adaptive Collembola species, thereby suggesting major threats to biodiversity at high latitudes under the current global warming regimes.

Arthropods

Winter activity

Cold tolerance

Population

Environmental filtering

Psychrophile

Temperature is one of the main factors that determines the survivorship and reproduction process of organisms. Arthropods are ectotherms, and many terrestrial meso- or microarthropods adopt diapause modes to pass over winter periods to avoid cold temperatures (Cáceres 1997; Koštál 2006; Saunders 2020). A few arthropod species are cold-tolerant or cold-adapted (Füreder 1999; Hågvar 2010) and active during winter and in polar regions with low temperatures (Sømme 1989; Worland and Block 2003; Slatyer et al. 2022). Although many studies have addressed diverse mechanisms adopted by the adults of arthropods to survive in winter, the response of the reproduction process to temperature change has received little attention (Block 1990; Vernon and Vannier 2002; Hågvar et al. 2020). The success of oviposition and egg hatching are the fundamental keys for the population maintenance of cold-adapted species.

Collembola are one of the most successful arthropods that colonize almost all terrestrial ecosystems (Hopkin 1998; Carapelli et al. 2019). Cold-adapted Collembola species have been found to survive at -30°C or -50°C in Antarctica. The genus Desoria is a group of psychrophilic Collembola that are widely distributed in moderate and high latitudes in the Northern Hemisphere. Their activities are different from the dormant overwintering survival patterns of other arthropods distributing in temperate regions. This means that the Collembola that develop and are active in winter may have homology with psychrophilic insect species; cold is also an important survival guarantee for metabolism maintenance in these psychrophilic animals and is a prerequisite for their population maintenance (Huey et al. 2021)

Some Collembola species are globally active in winter but not in summer (Zhang et al. 2014, 2017; Matsumoto et al. 2018, 2019). They likely reproduce in winter or early spring under low temperatures in this region. Temperature is a key factor affecting reproduction and ovarian development in cold-adapted arthropods (Birkemoe and Leinaas 1999; Danks 2004). Desoria species distribute abundantly in winter in the northeastern central and high-latitude regions of China. Collembola engages in winter snow-surface activities only in late autumn, early winter and late early spring in the Sanjjiang valley of northern Heilongjiang Province and Jilin Province of China (Zhang et al. 2017), while it is absent in the same area in spring, summer or early autumn (Feng et al. unpublished data). Collembola are active in winter in mid- and high-latitude regions, and their cold-environment behaviors are essential for their survival; any adaptation to the environment should mainly depend on high and low ambient temperatures. In the present study, we investigated the effects of temperature on the mortality of adults and the length of oviposition and egg hatching of the winter-active Collembola species, D. ruseki. We hypothesized that (1) D. ruseki has a higher mortality ratio at higher temperatures and (2) D. ruseki shows higher oviposition and hatch ratios at higher temperatures.

Study area

The study area was located in a snow-winter dry-hot summer climate zone (43°81’N, 126°43’E) according to the Köppen-Geiger Climate Classification (Kottek et al. 2006). Vegetation is dominated by Larix olgensis, Corylus heterophylla, Echinochloa crusgalli, and Carex sp.. The annual average temperature is 3.9°C, the lowest temperatures in January range from -18°C to -20°C, and the highest average temperatures in July range from 21°C to 23°C. The average annual precipitation is 650-750 mm, and the sunshine duration is between 2300 and 2500 hours.

Adult raring and reproduction

Specimens of D. ruseki were collected on March 9^th using pitfall traps placed on the snow surface (Appendix: Fig. A) in a larch forest plantation located in northeastern China. The mean temperature in March was between -3°C and 4°C, with the highest daytime temperature of 7.3°C. To normalize the Collembola status before laboratory experiments, all specimens of D. ruseki were first cultivated in a climate chamber (air temperature 5°C, air humidity 85%, illumination intensity of 62750 lux, 12:12-hour light:dark cycle) for three days without food provided. To test the effects of temperature on the mortality, oviposition and hatchability of D. ruseki, we set the cultivation temperatures at six levels, i.e., 0°C, 5°C, 10°C, 15°C, 20°C, and 25°C. At each temperature 100 individuals of Collembola was cultured in a jar (10 cm high and 5 cm in diameter) covered by a humid paper. Approximately 2 g of pre-dried leaf litter of barnyard grass (Echinochloa crusgalli) was provided as a food resource for Collembola. All jars were placed in chambers with 85% air humidity, 62750 lux illumination intensity, and a 12:12-hour light:dark cycle. The dead individuals, laid eggs and hatched eggs were counted and removed every three days since the start of the experiment.

Data analysis

The Z scores obtained based on a normal distribution were employed to normalize the data to evaluate the oviposition changes in different temperature zones. A comparison of oviposition among different temperatures was conducted using one-way ANOVA, and the adjustment method for p values for multiple comparisons was that of Tukey’s test. The significance level of the statistical tests was P=0.05.

The cultivation temperature affected the mortality ratio of D. ruseki, showing a higher mortality ratio as the cultivation temperature increased. The mortality ratio was below 5% at 5°C, 7% at 10°C, nearly 9% at 15°C, and 17% above 20°C (Fig. 1). All individuals died at 30°C within two days. For adult lifespan, the longest lifespan was 84 days at 0°C, followed by 69 days at 5°C, less than 15 days at 10°C ~ 25°C and − 5°C and less than 1 day at 30°C (Appendix: Fig. B).

Temperature also affected the total oviposition ratio, the length and distribution of the oviposition period and egg hatching time of D. ruseki. The oviposition period was within 12 days at 15°C but was longer at 5°C (63 days), 10°C (24 days) and 0°C (30 days) (Fig. 2a). The total oviposition ratio was not significantly different among 0°C, 10°C, and 15°C but was significantly higher at 5°C (AONVA, F = 3.47, p = 0.04, Fig. 2b). Individuals cultivated at 15°C laid their eggs first (after 9 days), followed by those at 10°C (18 days) and 5°C (21 days), and lastly those at 0°C (66 days).

Cultivated eggs hatched the fastest at 15°C (within 15 days), followed by 5°C, 0°C, and 10°C, for 19, 21, and 24 days, respectively (Fig. 3). The cultivation temperature also affected the hatching ratio (ANOVA, p > 0.05), with the highest ratio of 64% at 5°C, followed by 60%, 47% and 38% at 0°C, 10°C, and 15°C, respectively.

This study confirmed that temperature plays significant but different roles in the survival, oviposition, and egg hatching processes of winter-active Collembola D. ruseki. Adults of D. ruseki maintained the lowest mortality ratios at 0°C and 5°C and showed increasing mortality with increasing temperature. This strongly supports their high activity in winter and early spring and rarely recorded activity in summer seasons in our study region (Zhang et al. 2014, 2017; Hao et al. 2020; Feng et al. unpublished).

In contrast, the oviposition ratios were higher and the speed of egg hatching of D. ruseki was faster at 10°C and 15°C. This agrees with the key effects of living temperatures on the development of Collembola (Widenfalk et al. 2016). Importantly, egg hatching and later jurvenile development were inhibited or even stopped at 0°C. This indicates that in our study region, D. ruseki likely oviposited and hatched their eggs in autumn rather than in winter when the average daily environmental temperature was below 5°C in November (Guo et al. 2018). For reproduction, decreasing temperatures for hatching individuals are more conducive to survival. This developmental feature confirms that the developmental temperature of insects is limited to a certain range (Dixon et al. 2009).

Our study confirmed that D. ruseki is a winter-preferred species, supporting the viewpoint that Desoria species evolved from cold regions to temperate or tropical areas (Collins et al. 2020). In the context of global warming, temperate regions at high latitudes likely experienced an increase in temperature. If the temperature increased in the native distribution region of D. ruseki in early spring, this would be bound to reduce the adult population, which may further shrink the distribution of psychrophilic species (Aerts 2006; Freeman et al. 2018). The temperature threshold was higher than 15°C, and the population development of D. ruseki was greatly inhibited with increasing temperature; however, the geographical distribution and Collembola thermal tolerance should be combined with environmental studies that account for the local microclimate and cover more species (Escribano-Álvarez et al. 2022). In conclusion, our study revealed distinct but significant effects of temperature on different life stages of winter-active Collembola. The results suggest that global warming in the future likely affects the population dynamics and distribution of winter-active animals through different mechanisms.

CONFLICT OF INTEREST

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

ACKNOWLEDGMENTS

The Scientific Research Planning Project of Jilin Provincial Department of Education (No. JJKH20210409KJ), Jilin Province Science and Technology Development Plan Project (No. 20200201003JC), Strategic Priority Research Program of Chinese Academy of Sciences (XDA28020201), the National Natural Sciences Foundation of China (No. 42071059), the Program of Introducing Talents of Discipline to Universities (No. B16011), National Science & Technology Fundamental Resources Investigation Program of China (2018FY100300) supported this research.

DATA AVAILABILITY STATEMENT

The data that supports the findings of this study are available in the supplementary material of this article.

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No competing interests reported.

AppendixSupplementarymaterialsA.pdf
Figure A. The field sampling habitat in early winter
AppendixSupplementarymaterialsB.pdf
Figure B. Adult life expectancy at different temperatures
AppendixSupplementarymaterialsC.pdf
Figure C. Ontogeny development: Different developmental stages of Desoria ruseki eggs and larvae at 5°C

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The role of temperature in reproductivity trade-offs and life span in a winter-adaptive arthropod

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Abstract

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Introduction

Materials And Methods

Results

Discussion

Declarations

References

Additional Declarations

Supplementary Files

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