Challenging the 'Immunity Hypothesis': Primary or secondary parasitism as different survival strategies for the harlequin mistletoe Lysiana exocarpi (Behr) Tiegh

Abstract

The relationship between host plants and parasitic plants is considered a unique and fascinating model to explore different aspects in plant physiology, especially concerning water relations and nutrient use, given that host and parasite share these resources. An even more intriguing dynamic occurs when a parasite parasitizes another parasite (epiparasitism). In theory, these epiparasites should show even more specialized physiological functions to be capable to withdraw water and nutrients from the hemiparasite, such as maintaining even lower water potential and dealing with stronger nutrient imbalance. Here we studied leaf morpho-physiological responses of the Australian harlequim mistletoe (Lysiana exocarpi) and box mistletoe (Amyema miquelii) acting as hemiparasites on pink gum (Eucalyptus fasciculosa) and Lysiana exocarpi as an epiparasite on A. miquelii parasitizing E. fasciculosa. We explored the water and nutrient use and partitioning between the different plants involved (host–mistletoe–epiparasite). We found that L. exocarpi showed physiological and morphological differences that represent a more acquisitive strategy of resource use with higher stomatal conductance, water use efficiency, specific leaf area and K and Mg leaf concentration when growing as an epiparasite compared to the same species growing as primary parasite. Amyema miquelii traits remained constantly similar irrespective whether as primary parasite or with an epiparasite sharing its resources while the effect of the epiparasite is mostly depicted in its host's host species. In conclusion, our findings suggest that by adjusting some traits, epiparasitism is an alternative option for the harlequin mistletoe. Moreover, regardless of the host–parasite association, the primary host is the most affected by the epiparasitism.