Dynamics of soil microarthropod populations affected by a combination of extreme climatic events in tropical home gardens of Kerala, India

Highlights

• Effects of natural extreme climate events in tropical home gardens were studied.

• Drought followed by flooding drastically reduced soil microarthopods density.

• Biological soil quality was restored after drought but not soil microarthropods density.

• Plant species richness supported the re-establishment of the soil microarthopods populations.

Abstract

Climate change is predicted to increase drought and flooding events in the coming decades, especially in the tropics; we need to understand the short-term responses of plant community and soil microarthropods populations to these extreme events.Yet most of our current knowledge on this comes from manipulative studies in temperate regions. The present study reports the impact of a severe summer drought followed by a catastrophic flood in 2018 on soil microarthropod density and biological soil quality across 25 tropical home gardens. Drought reduced the density of organisms six-fold and flooding caused a further threefold reduction. Biological soil quality in the home gardens that were not flooded was restored during the monsoon season but this was just partially possible for microarthropod population size. Three months after flooding, the microarthropod groups encountered were generally able to re-establish their population to the condition prior to flooding. However, none of the group recovered to the mean seasonal values. The severity of previous drought seemed to have overridden any possible adaptation to annual summer water scarcity. Plant species richness in home gardens played a key role towards mitigation and possible resilience to disturbance of these ancient agroecosystems. The capacity of the soil microarthropod communities to recover over the long term after extreme climatic events and its relevance to maintaining ecosystem functions and services in home gardens through soil fertility warrant further investigation.

Introduction

Extreme climate events such as drought and floods are expected to have substantial impacts on plant and soil communities at local scales (Garcia et al., 2014). As a result of the ongoing climate change, the intensity and frequency of such extreme events is expected to increase in the future (Coumou and Rahmstorf, 2012; IPCC, 2013) and this urges a better understanding of their impacts on agroecosystems. The tropics are reported to have high vulnerability to climate change (Randell and Gray, 2019) and tropical regions like India have been experiencing increased extreme precipitation events associated with floods in the past two decades (Sudheer et al., 2019).

Soil moisture has often been reported to be the most important environmental variable affecting soil fauna community (Verhoef and van Selm, 1983; Kardol et al., 2011). According to the U.S. Global Change Research Program’s 2009 report, altered precipitation patterns will result in periods of drought and flooding. Drought periods are likely to have substantial effects on soil organisms – such as soil microarthropods - abundance and community structure, thus affecting important soil organism-mediated ecosystem processes. Drought can directly affect the soil community by causing desiccation of fauna, influencing their survival and inducing physiological and behavioural changes (Hilligsøe and Holmstrup, 2003). Drought can also affect soil organisms indirectly by decreasing the decomposition rate (Smith, 2012), altering soil characteristics (Sowerby et al., 2010) and plant cover (with its microclimate effects), influencing bottom-up effects (Vestergard et al., 2015). Consequently, drought was shown to reduce soil microarthropod abundance (Lindberg et al., 2002), but in areas with repeated summer drought the population may recover over a short period (Holmstrup et al., 2013), especially in extreme habitats (Florian et al., 2019). On the flip side, altered precipitation patterns can result in floods, which cause the quick development of anaerobic conditions in soil, resulting in marked changes in soil chemistry (soil pH, organic carbon) (Unger et al., 2010), causing a reduction in plant growth (Bange et al., 2016; Nguyen et al., 2018) and affecting reproductive properties like seed growth and germination (Unger et al., 2010). Hence floods have negative impacts on plant communities and soil microarthropods, since they are intimately connected through herbivory and symbiosis, and indirectly by plant decomposition (Sylvain and Wall, 2011).

Soil microarthropods represent an important component of soil-living communities and play a role in maintaining soil quality and health (Doran and Zeiss, 2000; Kibblewhite et al., 2008). They are involved in many processes such as translocation, breaking and decomposition of organic matter, nutrient cycling, soil structure formation, and consequently water regulation (Wall et al., 2008; Soong et al., 2016; Neher and Barbercheck, 2019). Extreme climate events leading to changes in microarthropod communities can alter belowground biological processes with potential consequences for ecosystem functions. However, despite studies on soil mesofauna conducted in the context of environmental change are not lacking (Kardol et al., 2011; Xu et al., 2012; Phillips et al., 2019; Yu et al., 2021), most of such research has taken place under manipulative conditions or in natural ecosystems of temperate regions, focusing mainly on mites and springtails (Pflug and Wolters, 2001; Lindberg, 2003; Kardol et al., 2011; Xu et al., 2012; Holmstrup et al., 2013; González-Macé and Scheu, 2018; Siebert et al., 2019). To our knowledge none of these studies were the result of extreme naturally-occurring climate events in tropical agricultural fields.

Microarthropod groups are likely to be differentially affected by extreme climate events depending on their ecological adaptations (Lindberg and Bengtsson, 2005), in particular with regard to the soil habitat. In fact, some groups are highly sensitive to changes in soil quality because they live, feed and reproduce in the soil, and are extremely adapted to specific soil conditions (Parisi et al., 2005; Parisi and Menta, 2008). These specific adaptations of some microarthropod groups to soil conditions make them suitable candidates for estimating soil quality (Menta and Remelli, 2020). Intimately linked to soil biota is the related plant community, whose plant species richness is a strong driver of the structure and functioning of soil food webs (Eisenhauer et al., 2013). Plant species richness increases overall root biomass (Cardinale et al., 2007), litter quality and quantity, and soil water content, with indirect positive effects on soil microbial biomass and the density of microfauna and mesofauna detritivores (Hooper et al., 2000; Eisenhauer et al., 2013; Murugan et al., 2020). In turn, changes in the microarthropod community can affect soil nutrient cycling and thus the plant community as a whole (Wardle et al., 2004; Yergeau et al., 2007; Sabais et al., 2012).

In 2018, during the summer season (January to May), the southern Indian state of Kerala received 40 % less precipitation compared to the long-term seasonal mean. Afterwards, from June to August 2018 during the monsoon season, Kerala was characterized by unusually high precipitation and was affected by severe flooding, which caused the evacuation of over a million people. Kerala is well known for its biodiverse home gardens (“HGs”), where cultivated plants are managed with almost zero input from agrochemicals, making these agroecosystems a widely recognized model of sustainability (Jose and Shanmugaratnam, 1993; Mohan et al., 2007). Tropical HGs are considered to be highly valuable traditional agroecosystems (Kumar et al., 1994; Sankar and Chandrashekara, 2002; Galluzzi et al., 2010) and are classified as in-situ conservation sites in accordance with the Convention on Biological Diversity (1992).

The present study was carried out in a village in Kerala, India, in 25 H Gs, 19 of which were severely affected by the 2018 flood. The aim of the work was to study the soil microarthropod community’s response to the drought and the immediately following flood event.

We hypothesized that: (i) the combination of drought followed by flood drastically reduces the density of microarthropods, directly and by altering soil properties; (ii) the microarthropod groups are differentially affected by drought but similarly impacted by the major flood, and the groups with overall higher reproduction rate and dispersal capacity conducting their life more at the soil surface recover more quickly; (iii) higher plant cover and plant species richness enhance higher microarthropod density, soil quality and the recovery of both parameters after flood due to increased root and microbial biomass and higher quantity and quality of litter; and (iv) the presence of more lignified plant functional groups (trees, shrubs) is associated with higher resistance to decomposition and soil disturbance.