The effect of repeated periods of drought and aestivation on Allolobophora chlorotica reproductive output

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Abstract

Increasing drought frequency under climate change is expected to intensify periods of suboptimal soil moisture, adversely affecting earthworms and other soil biota. To survive desiccation, some earthworms enter aestivation, a state of reduced metabolic activity during which reproduction and ecosystem service provision are suspended. However, the capacity of earthworms to recover from repeated drying events remains poorly understood. This study examined how multiple drought-aestivation cycles influence the reproductive performance of Allolobophora chlorotica , one of the most common UK earthworm species. Adults were exposed to one, two or three 14-day drying periods to gravimetric moisture contents of ∼11-13 wt% in loamy soil, each followed by three days under favourable moisture conditions. After the final exposure, earthworms were placed in groups of four into optimally moist soil for 50 days to reproduce. Cocoon number, mass, viability and incubation time were measured as indicators of reproductive success. Cocoon production declined significantly with increasing aestivation frequency (p < 0.001), being lowest during Days 1-10 of recovery (∼0-0.02 cocoons earthworm -1 day -1 ), peaking between Days 20-30 (∼0.08-0.16 cocoons earthworm -1 day -1 ) and declining over the final 20 days (∼0.08-0.12 cocoons earthworm -1 day -1 ). Unexpectedly, earthworms previously exposed to drying and aestivation produced more (226 vs 171 cocoons, p < 0.05) and heavier (6.701 ± 1.205 vs 6.036 ± 1.256 mg, p < 0.05) cocoons than those kept under constant high moisture, suggesting compensatory growth upon rehydration and possibly reflecting food limitation or soil compaction in controls. Cocoon viability and incubation time did not differ significantly between treatments. Across treatments, earthworm mass strongly predicted fecundity as heavier individuals produced more (p < 0.001) and heavier (p <0.001) cocoons, and cocoon mass was positively correlated with hatching success (p < 0.001). Overall, Al. chlorotica displayed resilience to short-term, intermittent drought through aestivation, but reproductive success remained sensitive to the combined effects of soil moisture, food availability, and soil structure. These findings highlight the importance of considering multiple environmental constraints when predicting soil fauna responses to increasing drought frequency and duration.
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Abstract Increasing drought frequency under climate change is expected to intensify periods of suboptimal soil moisture, adversely affecting earthworms and other soil biota. To survive desiccation, some earthworms enter aestivation, a state of reduced metabolic activity during which reproduction and ecosystem service provision are suspended. However, the capacity of earthworms to recover from repeated drying events remains poorly understood. This study examined how multiple drought-aestivation cycles influence the reproductive performance of Allolobophora chlorotica, one of the most common UK earthworm species. Adults were exposed to one, two or three 14-day drying periods to gravimetric moisture contents of ∼11-13 wt% in loamy soil, each followed by three days under favourable moisture conditions. After the final exposure, earthworms were placed in groups of four into optimally moist soil for 50 days to reproduce. Cocoon number, mass, viability and incubation time were measured as indicators of reproductive success. Cocoon production declined significantly with increasing aestivation frequency (p < 0.001), being lowest during Days 1-10 of recovery (∼0-0.02 cocoons earthworm-1 day-1), peaking between Days 20-30 (∼0.08-0.16 cocoons earthworm-1 day-1) and declining over the final 20 days (∼0.08-0.12 cocoons earthworm-1 day-1). Unexpectedly, earthworms previously exposed to drying and aestivation produced more (226 vs 171 cocoons, p < 0.05) and heavier (6.701 ± 1.205 vs 6.036 ± 1.256 mg, p < 0.05) cocoons than those kept under constant high moisture, suggesting compensatory growth upon rehydration and possibly reflecting food limitation or soil compaction in controls. Cocoon viability and incubation time did not differ significantly between treatments. Across treatments, earthworm mass strongly predicted fecundity as heavier individuals produced more (p < 0.001) and heavier (p <0.001) cocoons, and cocoon mass was positively correlated with hatching success (p < 0.001). Overall, Al. chlorotica displayed resilience to short-term, intermittent drought through aestivation, but reproductive success remained sensitive to the combined effects of soil moisture, food availability, and soil structure. These findings highlight the importance of considering multiple environmental constraints when predicting soil fauna responses to increasing drought frequency and duration. Competing Interest Statement The authors have declared no competing interest.

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