How does mistletoe infection affect seasonal physiological responses of hosts with different leaf phenology?
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.
Section snippets
Material and methods
This study was conducted at the ‘‘Roncador’’ Ecological Reserve from the Brazilian Institute of Geography and Statistics (RECOR/IBGE), located 33 km south of Brasília, Brazil (15° 56′ S, 47 ° 53′ W), at 1100 m above sea level. The average annual precipitation is approximately 1500 mm with a pronounced dry season from May through September and a mean annual temperature ranging from 20 to 26 °C within years (Fig. S1). The predominant soils are acidic (pH ≈ 4.5), deep and well-drained Oxisols (
Results
Prior to the measurements, infected and uninfected branches did not differ in number of leaves or in total leaf area (Fig. S2, Table S1), independent of the host. During the wet season, leaves from infected branches showed lower maximum photosynthetic rates (Amax) and lower stomatal conductance (gs-max) at Amax compared to uninfected branches irrespective of the host (paired t-tests, P < 0.05; Fig. 1, Table S2). However, contrary to our expectation that the presence of the mistletoe would
Discussion
Our expectations were partially corroborated by the data, since host nutrient concentrations and physiological responses differed between infected and non-infected branches. Differences were more apparent under non-limiting soil water conditions (wet season) and optimal levels of light and temperature, as shown by the values of Amax and gs-max. However, during the dry season, the mistletoe infection resulted in lower stomatal regulation (i.e., higher gs-max in infected branches) in the
Author contributions
Marina C. Scalon: Conceptualization, Methodology, Data curation, Writing- Original draft preparation. Davi R. Rossatto: Data curation, Writing- Reviewing and Editing. Augusto C. Franco: Supervision, Writing- Reviewing and Editing.
Declaration of Competing 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.
Acknowledgements
MCS is supported by a postdoctoral fellowship from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior). DRR is recipient of a CNPq Research Productivity fellowship (302897/2018-6) ACF is recipient of a CNPq Research Productivity fellowship (311362/2019-2). We thank RECOR/IBGE for the logistic support.
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