Latitudinal variation in seed predation correlates with latitudinal variation in seed defensive and nutritional traits in a widespread oak species

Abstract

Background and Aims Classic theory on geographical gradients in plant–herbivore interactions assumes that herbivore pressure and plant defences increase towards warmer and more stable climates found at lower latitudes. However, the generality of these expectations has been recently called into question by conflicting empirical evidence. One possible explanation for this ambiguity is that most studies have reported on patterns of either herbivory or plant defences whereas few have measured both, thus preventing a full understanding of the implications of observed patterns for plant–herbivore interactions. In addition, studies have typically not measured climatic factors affecting plant–herbivore interactions, despite their expected influence on plant and herbivore traits. Methods Here we tested for latitudinal variation in insect seed predation and seed traits putatively associated with insect attack across 36 Quercus robur populations distributed along a 20° latitudinal gradient. We then further investigated the associations between climatic factors, seed traits and seed predation to test for climate-based mechanisms of latitudinal variation in seed predation. Key Results We found strong but contrasting latitudinal clines in seed predation and seed traits, whereby seed predation increased whereas seed phenolics and phosphorus decreased towards lower latitudes. We also found a strong direct association between temperature and seed predation, with the latter increasing towards warmer climates. In addition, temperature was negatively associated with seed traits, with populations at warmer sites having lower levels of total phenolics and phosphorus. In turn, these negative associations between temperature and seed traits led to a positive indirect association between temperature and seed predation. Conclusions These results help unravel how plant–herbivore interactions play out along latitudinal gradients and expose the role of climate in driving these outcomes through its dual effects on plant defences and herbivores. Accordingly, this emphasizes the need to account for abiotic variation while testing concurrently for latitudinal variation in plant traits and herbivore pressure.

Latitudinal gradient in the intensity of biotic interactions in terrestrial ecosystems: Sources of variation and differences from the diversity gradient revealed by meta‐analysis

“…We found that herbivory and carnivory measured on standardised prey, including non‐native plant species/genotypes (Lu et al, 2019) or their seeds (Chen et al, 2017; Hargreaves et al, 2019), plasticine insect models (Roslin et al, 2017; Zvereva et al, 2019), non‐native live insect prey (Jeanne, 1979) and artificial bird nests (McKinnon et al, 2010), yield stronger latitudinal patterns than are obtained when predation is measured on natural prey, at least for ectothermic consumers. This difference can be explained by the latitudinal changes in local adaptations of native plant/prey, for example in anti‐herbivore defences in plant seeds (Chen et al, 2017; Moreira et al, 2020) and in the behavioural and life history anti‐predator adaptations in birds (Díaz et al, 2013; Freeman et al, 2020), whereas standardised models did not participate in evolution (Freeman et al, 2020).…”

Mucilage binding to ground protects seeds of many plants from harvester ants: A functional investigation

“…An association between temperature and seed mucilage quantity has previously been reported and the authors attributed the cause to water stress (Teixeira et al., 2020). Additionally, higher seed predation pressure in warmer places (Moreira et al., 2020; Noroozi et al., 2016) could select for more tightly bound seeds as a defence against granivory. A correlation between mucilage and solar radiation has not been proposed in the literature.…”

Search for top‐down and bottom‐up drivers of latitudinal trends in insect herbivory in oak trees in Europe

“…Plant species at lower latitudes commonly experience higher rates of herbivory than plants growing further from the Equator (Coley & Barone, 1996; Lim et al., 2015; Moreira et al., 2018; Schemske et al., 2009) and thus tropical plant species may evolve higher levels of anti‐herbivore defences (Abdala‐Roberts et al., 2016; Hahn et al., 2019; Johnson & Rasmann, 2011; Pearse & Hipp, 2012). While early reviews reported patterns supporting these predictions (Coley & Aide, 1991; Coley & Barone, 1996; Dyer & Coley, 2002), several studies in recent decades have found either no evidence for a latitudinal gradient in herbivory and plant defences (Gaston et al., 2004; Moles et al., 2011; Moles & Westoby, 2003) or increase in herbivory and defences with latitude (Adams et al., 2009; Del‐Val & Armesto, 2010; Gaston et al., 2004; Martz et al., 2009; Moreira et al., 2018, 2020; Pennings et al., 2009; Stark et al., 2008; Woods et al., 2012). Given these inconsistencies, it is of great importance to identify the mechanisms underlying the substantial variation in herbivory and plant defences across latitudes, as herbivory is an important ecological process that modulates primary productivity by altering the recruitment, mortality and growth of plants.…”