Parthenium avoids drought: Understanding the morphological and physiological responses of the invasive herb Parthenium hysterophorus to progressive water stress

Highlights

• Parthenium hysterophorus displayed drought avoidance in response to water stress.

• Juvenile and adult plants maintained positive net photosynthesis under water stress.

• Juvenile and adult P. hysterophorus reduced above-ground biomass to conserve water.

• Morpho-physiological alterations enhanced the water-use efficiency of P. hysterophorus.

Abstract

Parthenium hysterophorus L. is a noxious annual invasive herb which threatens biodiversity, food security and human and animal health in various tropical and sub-tropical regions globally. Given that these regions, including South Africa, experience frequent drought events, it is important that the invasive potential of this weed be better understood in the context of water stress. This study aimed to assess the physiological and morphological responses of P. hysterophorus to water stress. To elicit these responses, juvenile and adult plants were progressively water stressed over a six-week period. Despite significant reductions in leaf water potential, relative leaf water content and stomatal conductance from severe soil water stress, plants maintained positive net photosynthesis, albeit at a severely reduced rate. Concomitantly, water-use efficiency of P. hysterophorus increased by more than 300 %. Morphologically, water-stressed plants exhibited reductions in leaf area and leaf number, with adults accelerating flower production when compared to well-watered plants. Linked to this, were alterations in biomass, with juveniles and adults reducing above-ground biomass by 75 % and 35 %, respectively. Overall, many of the physiological and morphological responses are indicative of a largely drought avoidance strategy, allowing P. hysterophorus to persist during periods of water-stress as leafy basal rosettes (juveniles) or as reproductive herbs (adults). This research yielded valuable insights into the underlying water relations of P. hysterophorus, and how these may relate to the potential spread, detriment and management of the weed in various sub-tropical environments.

Introduction

Native to Central and South America, the herb Parthenium hysterophorus L. (Asteraceae: Heliantheae) is a noxious annual invasive plant prevalent in at least 50 tropical and sub-tropical countries across the globe (Dhileepan and Strathie, 2009; Adkins and Shabbir, 2014). In South Africa, P. hysterophorus is recognised as one of the country’s most threatening invasive plants, with large populations continuing to spread in KwaZulu-Natal, Mpumalanga, North-West and Limpopo provinces (Terblanche et al., 2016). Parthenium hysterophorus grows and matures rapidly (4–6 weeks), producing prolific amounts of seed (∼30 000 seeds/plant) which form extensive and persistent seedbanks (Strathie et al., 2011). The weed readily invades and colonises a wide variety of environments, including road-verges, rail-sides, cultivated lands, watercourses, pastures as well as natural grassland and savanna habitats (Strathie et al., 2011). Invasions of P. hysterophorus impose severe ecological and socio-economic impacts, including reductions to crop yields, displacement of native species, losses to livestock and their productivity as well as threats to human and animal well-being (Adkins and Shabbir, 2014). Further concern surrounds predictions by McConnachie et al. (2010), which suggests that large portions of sub-Saharan Africa are climatically suited and susceptible to further P. hysterophorus invasion.

Numerous environmental factors are known to constrain the establishment and proliferation of invasive plants within their introduced ranges (Theoharides and Dukes, 2007; McConnachie et al., 2010). In the absence of natural predators and pathogens (termed ‘biotic release’), weed invasions are largely regulated by the prevailing abiotic conditions (Melbourne et al., 2007), the most prominent of which is climate (Theoharides and Dukes, 2007). Climatic variables, particularly temperature, rainfall and their interaction (seasonality), often predict the potential distribution and invasiveness of weeds at a broad scale (Sakai et al., 2001). Furthermore, this is also influenced by the ecology and adaptability of the weed itself (Friedman and Rubin, 2015). For annual species, like P. hysterophorus, seasonal germination during the warm spring and summer months affords plants’ favourable growing temperatures, but simultaneously increases their dependency on the availability of water in the soil (Friedman and Rubin, 2015). Soil moisture availability is largely determined by the amount and frequency of precipitation in sub-tropical regions, meaning that the high variability in annual and seasonal rainfall within these regions of South Africa (MacKellar et al., 2014) is likely to expose short-lived plants to periods of water stress.

Water stress is one of the most important physiological constraints to tropical and sub-tropical invasive weeds, widely accepted to limit their productivity, growth, reproduction and lifespan (Touchette et al., 2007; Oliver et al., 2010). Drought events are characterised by prolonged periods of below-average rainfall, which result in the progressive decline and subsequent shortage of soil water available to plants (Touchette et al., 2007). Periods of water stress may elicit a myriad of morphological and physiological plant responses, which can be generally classified as ‘drought escape’,’ drought avoidant’ or ‘drought tolerant’ (Lawlor, 2012). Drought escape allows plants to complete their life-cycle before the onset of severe water stress (drought stress), typically by accelerating flowering and seed set prior to senescence (Verslues et al., 2014). Whereas drought avoidance serves to minimise plant water loss and/or increase water uptake, and frequently includes increases in root biomass, decreases in leaf area and reductions in stomatal conductance (McCann and Huang, 2008). Drought tolerance however, is largely metabolic seeking to maintain cell turgor and function, mainly through osmotic adjustment, in which plants accumulate solutes to better retain water (Touchette et al., 2007; Lawlor, 2012). Although drought tolerance and avoidance are common responses to ongoing water stress, species-specific studies are required to identify the underlying mechanisms and to what extent these responses are likely to be elicited.

Described as a C₃-C₄ intermediate species (Moore et al., 1987), P. hysterophorus is physiologically a highly responsive weed, capable of phenotypically adapting to and overcoming various environmental constraints (Kohli et al., 2006; Cowie et al., 2018). Despite this plasticity, soil moisture remains one of the few abiotic limitations to the annual lifecycle and distribution of the weed (Dhileepan et al., 2000; McConnachie et al., 2010). Although seeds are resilient and can persist in dry soil for many years, their germination is highly dependent upon rainfall, with seedlings typically emerging throughout spring to summer, in areas with summer rainfalls > 500 mm (McConnachie et al., 2010). Young seedlings will often transition through a leafy basal rosette stage before maturing (flowering), however, during periods of water stress young plants may persist as rosettes awaiting favourable rainfall (Annapurna and Singh, 2003). As adults, water availability is linked to the flowering phenology of P. hysterophorus, with decreasing soil moisture prompting earlier flowering and seed set (Bajwa et al., 2017). Despite limited understanding of P. hysterophorus’s water-relations, recent studies have shown that the weed may complete its life-cycle at soil moistures as low as 50 % field capacity (Bajwa et al., 2017; Nguyen et al., 2017). This suggests that P. hysterophorus plants possess a strategy to persist and set seed during periods of water stress.

Global climate models predict that increasing temperatures and decreasing rainfall, will result in much of South Africa experiencing more frequent and severe drought events (MacKellar et al., 2014; Chami and Moujabber, 2016). However, it is not fully understood how many of the country’s most problematic invasive weeds will respond, nor if these species are physiologically able to tolerate increases in water stress. Given the threat P. hysterophorus poses to South African agriculture, natural areas and human and animal health, it is imperative that the invasive potential of the weed be better understood in the context of the weed’s ability to cope with water stress. This study aimed to identify and assess the morphological and ecophysiological responses of P. hysterophorus to progressive water stress at different growing stages. To better elicit and assess these responses, both juvenile and adult plants were progressively watered stressed, simulating a natural dry period over a six-week period.