A multiverse of trophic networks and coevolutionary trajectories among holoparasitic Orobanchaceae and their animal associates: a global perspective.

Holoparasitism, in achlorophyllous, fully heterotrophic plants, is one of the most peculiar symbioses in the plant world. In particular, holoparasites from Orobanchaceae, the largest parasitic plant family, have evolved unique visual and olfactory signals in the plant kingdom, and thus play a key role in the evolution of animal-plant adaptations. Holoparasitism offers excellent case studies of the effects of a specialised interaction on multiple aspects of plant ecology and evolution, including pollination, herbivory, and speciation. In this paper, we present the first global study of these interactions using morphological and molecular tools, summarising almost 20 years of field studies. These observations were supplemented with literature data and internet sources, ultimately encompassing more than 1370 observations from 76 countries in Europe, America, Africa, Asia, and Australia. We found data on animals interacting with 130 species of 16 holoparasitic genera from the Orobanchaceae family. This study represents the first comprehensive study of animals which use these plants as food, shelter, hunting grounds, or part of their development cycles. Our work has resulted in recognising 667 animal species from 34 orders, 163 families, and 434 genera, with a predominance of arthropods (91% of species recorded) followed mainly by gastropods (ca. 4%), mammals (2%), birds and reptiles (0.6% each). Besides the combination of different pollinator and herbivore species, parasitic plants also attract a range of other animals, such as carnivores and parasitoids, creating a habitat with multitrophic and multilayered relationships. Our research sheds light on the intricate interactions mediated by parasitic plants and animals, opening the path for further elucidating the ecological and evolutionary drivers of holoparasite diversity and their broader ecological role.