How does mistletoe infection affect seasonal physiological responses of hosts with different leaf phenology?

Highlights

• Infected and non-infected branches showed distinct stomata responses depending on host phenology.

• Differences in regulation of water loss between branches were more apparent in the wet season.

• Pre-dawn leaf water potentials were consistently more negative for infected branches.

• Leaf mobile nutrient concentrations were lower in infected branches.

• Host species adjust at the individual level to mistletoe physiological stress throughout the year.

Abstract

Plants should have the ability to perceive physiological changes within their branches when infected by mistletoes, adjusting the use of resources between infected and uninfected branches which can be crucial for their survival in the long-term. Here we investigated how branches infected by the mistletoe Passovia ovata (Pohl ex DC.) Tiegh. and uninfected branches within the same individual tree respond to seasonal environmental changes across two hosts of contrasting leaf phenology (the evergreen Miconia albicans (SW.) Triana and the deciduous Byrsonima verbascifolia (L.) DC.). We measured key leaf traits (instantaneous gas exchange rates, diurnal courses of stomatal conductance, leaf water potential, specific leaf area and leaf macronutrient concentrations) during the peak of the wet and dry season in a seasonal savanna of central Brazil. Pre-dawn leaf water potentials were consistently more negative for infected branches of both hosts, suggesting that overnight water refilling of infected branches was more limited. However, infected and uninfected branches exhibited similar leaf water potentials at midday, suggesting that they undergo similar imbalances in water supply and demand during periods of high atmospheric evaporative demand. Infected and non-infected branches of the evergreen mistletoe showed tighter regulation of water loss, whereas infected branches of the deciduous host were less constrained in regulating leaf transpiration. We also found differences for nutrient concentrations: N, P and K were lower, while Ca was higher in leaves of infected branches. Physiological changes induced by mistletoe infection affected host performance, and were reflected in water and nutrient use differences between infected and uninfected branches. Our findings show that infection responses by mistletoes can be detected between branches within individual trees, and that host species with distinct patterns of leaf phenology are capable to adjust, at the individual level, to cope with mistletoe's imposed physiological stress throughout the year.

Introduction

Parasites are defined as organisms that live in or on another organism and take part or all resources they need to survive from their hosts, not only reducing growth, survival and reproductive success of the parasitized individual, but also impacting the host population dynamics (Anderson and May 1978). Parasites should adjust the level of host exploitation to an optimum (Bull, 1994; Ebert and Bull, 2003) in a manner in which they acquire the resources for their reproduction and decrease the costs associated with extreme exploitation (Gandon et al., 2001). This trade-off should shift exploitation to an optimum level: when the cost of virulence (i.e. likelihood of survival) is high, parasites should diminish the draining of resources, and vice-versa (Frank, 1996). These costs are related to reduction of life expectancy of the host (e.g., through increased susceptibility to stresses, such as drought and high irradiances), which in turn decreases the likelihood of parasites to complete their life cycle.

Parasitism in plants has evolved at least 8 different times in the evolutionary history and each family of the Santalales order is known to have evolved parasitic taxa (Nickrent et al., 2010). Although clade evolution occurred independently, the parasitic life-form requires highly convergent functional traits, such as succulent leaves with large stomata (Glatzel and Geils, 2009; Scalon et al., 2016) and high rates of stomatal conductance, due to similar selective pressures and physiological constraints related to host resources’ exploitation (Scalon and Wright, 2015). Mistletoes from the Loranthaceae family are aerial hemiparasites that connect to the branches of their hosts parasitizing their xylem, but producing leaves, forming a photosynthetically active canopy (Glatzel and Geils, 2009). By competing with the host for water and mineral nutrients, the mistletoe can negatively affect the host allometry, reducing growth and reproduction (Press and Phoenix, 2005; Tennakoon and Pate, 1996), decreasing gas exchange and water balance (Meinzer et al., 2004; Scalon et al., 2017; Tennakoon and Pate, 1996), and even reduce host survival (Reid et al., 1992). Studies that compare infected and non-infected branches in the same individual tree (i.e., the host) have provided evidence of marked changes, such as drastic reductions in leaf area (Scalon et al., 2017), changes in wood and leaf anatomy, such as lower xylem and phloem area (Ozturk et al., 2019), and the lowering of leaf nutrient content and available cellular water (Cirocco et al., 2016, 2021). Together, these studies suggest that mistletoe parasitism imposes a shift towards a more resource-conservative strategy in the host (Wright et al., 2004).

These physiological impacts on host trees can affect different species within the plant community, since mistletoes are not necessarily host specific. While there are highly specific species, there are also generalist species that parasitize an extensive range of hosts, including exotic introduced plants (Norton and Carpenter, 1998). It is still unclear if the same mistletoe species can cause divergent responses in different host species or if hosts will be affected similarly. Since mistletoes are directly competing with their hosts for nutrients and water, in highly seasonal environments seasonal drought can be an additive stress effect for these host plants given the high evaporative demand of the atmosphere (Da Rocha et al., 2009). Thus, species which adopt different ecological strategies to deal with water deficit, such as showing distinct patterns of leaf phenology, may respond differently to mistletoe infection (Cocoletzi et al., 2020).

In the Cerrado savannas of Central Brazil (a seasonally dry low-nutrient ecosystem), the woody component of the vegetation typically consists of deciduous, deep-rooted and evergreen, predominantly shallow-rooted trees that have contrasting strategies of water and nutrient use and conservation (Goldstein et al., 2008). Evergreen species maintain their canopy throughout the year, increasing stomatal control during the dry season and tend to have lower leaf nutrient concentrations, while deciduous species shed their entire canopy towards the end of the dry period allowing rehydration and bud break, and generally display higher leaf nutrient concentrations (Franco et al., 2005; Meinzer et al., 1999). Because mistletoes tap water and nutrients from the host tree, infected branches are expected to be under strong competition with the mistletoe compared to a non-parasitised branch. However, these functional differences between evergreen and deciduous hosts may lead to distinct adjustments of water use and gas exchange for branches undergoing infection, depending on the host phenology.

Our aim here was to investigate the effects of mistletoe infection on hosts with contrasting leaf phenology and whether the responses changed seasonally. Hence, we compared physiological responses of infected and uninfected branches from two different host species, one evergreen and the other deciduous, during the dry and the wet season. Because of the resource imbalance caused by mistletoes directly retrieving nutrients and water from the infected host branches we expected that host leaves from infected branches would show a more conservative resource use strategy. Thus, leaves from infected branches would show lower nutrient concentration, lower photosynthetic rates and higher stomatal control of transpiration compared to uninfected branches. We also expected that leaves from infected branches would suffer further water limitation during the dry season, thereby increasing the need of strong stomatal control of leaf gas exchange in infected branches. Because the deciduous host is deep-rooted with access to more stable soil water resources and drops the leaves towards the end of the dry period, we expected that stomatal control of transpiration and maintenance of branch water balance would not be as crucial, while the evergreen host must rely on shallower water sources and would exert a stronger stomatal control of transpiration that would be exacerbated in the parasitized branches. During the wet season, as water is abundant in the system, we expected to find no differences between evergreen and deciduous hosts, although differences between infected and uninfected branches would remain.