A global analysis of water and nitrogen relationships between mistletoes and their hosts: Broad-scale tests of old and enduring hypotheses

Abstract

Mistletoes use far more water per unit carbon fixed during photosynthesis than their hosts (i.e. they have lower 'water use efficiency', WUE). The widely cited 'nitrogen-parasitism hypothesis' posits that N is the most limiting resource for mistletoes and that they use their faster transpiration rates to acquire sufficient N from the host xylem. In a rather different context, the 'mimicry hypothesis' arose in the literature suggesting that some mistletoes mimic the morphology of host leaves in order to deploy higher N leaves without suffering higher levels of herbivory. These two non-exclusive hypotheses share the common goal of trying to explain patterns of mistletoe leaf N concentration. We set out to test the generality of both hypotheses at broad geographic scale using data for 168 mistletoes-host pairs, from 39 sites, encompassing all continents except Antarctica. We drew together data from published literature and our own field data on two key plant functional traits, leaf N concentration (Nmass) and leaf carbon isotopic composition (δ13C) (representing long-term WUE and degree of stomatal control over photosynthesis). Key findings included (i) little or no support for the N-parasitism hypothesis: differences in mistletoe and host Nmass explained only 3% variation in differences in leaf δ13C, and mistletoe-host differences in leaf δ13C were unrelated to whether or not the hosts were N-fixers (presumed to have higher N concentration in xylem sap); (ii) partial support for the mimicry hypothesis: mimic mistletoes generally had higher Nmass when associated with N-fixing hosts (but, on non-N-fixing hosts there was no such pattern); and (iii) more broadly, mistletoes showed similar trait responses as their hosts to environmental drivers; for example, they showed similar-magnitude shifts in Nmass and δ13C in relation to site aridity. Contrary to current belief, our findings suggest that nitrogen is not the limiting nutrient for mistletoes, at least not the main component driving the faster transpiration rates. Our results also give insight into the evolution of mimicry in mistletoes and show, for the first time, that mistletoes are also constrained by local water availability, exhibiting clear trait adaptations to environmental gradients. By reconsidering these issues at broad geographic scale and across a large number of species, our findings substantially modify current knowledge on the ecology and physiology of mistletoes and their hosts.