Gall‐forming and free‐feeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly

Abstract

In contrast to most insect guilds, gall-forming insects are thought to reach highest diversity on sclerophyllous vegetation, such as Neotropical savannas and Mediterranean vegetation types. The water and nutrient stress endured by meristems of canopy trees in tall wet tropical rainforests may cause leaf sclerophylly. Hence, the upper canopies of such ecosystems may represent a suitable habitat for gall-forming insects. At the San Lorenzo Protected Area, Panama, we estimated free-feeding herbivory and gall densities within five sites in 2003 and 2004, by surveying leaves in vertical and horizontal transects. In each sample, we recorded leaf density (mature and young foliage), free-feeding herbivore damage and number of galls, including the presence of live larvae, parasitoids or fungi. We surveyed 43 994 leaves, including 231 plants and 73 tree and liana species. We collected 5014 galls from 17 host-plant species, including 32 gall species of which 59% were restricted to the canopy (overall infestation rates: 2.4% in 2003, 5.5% in 2004). In 2003, 16% of the galls were occupied by live larvae, against 5% in 2004. About 17-20% of leaves surveyed suffered from free-feeding herbivory. Leaf sclerophylly increased significantly with sampling height, while free-feeding herbivory decreased inversely. Conversely, the number of live galls collected in the canopy was 13-16 times higher than in the understorey, a pattern consistent across sites and years. Hence, the probability of gall survivorship increased with increasing leaf sclerophylly as death by fungi, parasitoids or accidental chewing were greater in the understorey. Increasing harsh ecophysiological conditions towards the upper canopy appear favourable to galls-forming population maintenance, in support of the hypothesis of harsh environment. Hence, gall diversity and abundance in the upper canopy of tall tropical forests are perhaps among the highest in the world.

Vertical canopy gradient shaping the stratification of leaf‐chewer–parasitoid interactions in a temperate forest

“…We expect both groups to be more parasitized lower in the canopy, but we expect semiconcealed hosts to be more abundant higher in the canopy, in accordance with the hypothesis that the harsh upper canopy environment favors concealed or semiconcealed feeders (Ribeiro & Basset, 2007). Moreover, in tropical forests, there are differences in parasitoid community composition between exposed and semiconcealed feeders (Hrcek, Miller, Whitfield, Shima, & Novotny, 2013), and here, we expect a similar pattern.…”

“…Therefore, the higher diversity recorded in the first level might be due to the involvement of understory species, supporting our original hypothesis. The higher diversity of the third level might be explained by the presence of species‐rich semiconcealed feeders, which were considerably less numerous in the first level, supporting the original hypothesis of the competitive advantage of the concealed feeders in the harsh upper canopy environment (Chaij et al., 2016; Paniagua et al., 2009; Ribeiro & Basset, 2007). However, in our study, due to the absence of the upper canopy per se, differences in the ecological conditions (e.g., solar radiation, temperature, wind speed; Basset, Horlyck, et al., 2003; Parker, 1995) between the second and third levels were blurred.…”

“…These results suggest that, even though semiconcealed feeders are less protected than concealed ones, they still have an advantage over exposed feeders, at least, in temperate forests. In brief, because they are less vulnerable to harsh conditions and predators (Novotny et al., 2006; Ribeiro & Basset, 2007), they can occupy higher forest levels, reducing parasitism.…”

Variation in community structure of gall‐inducing insects associated with a tropical plant supports the hypothesis of competition in stressful habitats

“…The environmental stress hypothesis (ESH) predicts that gallinducing insect diversity should be greater in more stressful/xeric habitats (Fernandes & Price, 1988). The mechanisms underlying greater species richness in xeric habitats involve evolutionary and ecological processes (Fernandes & Price, 1988;Price, Fernandes, & Waring, 1987;Ribeiro & Basset, 2007). Among ecological mechanisms, the actions of parasites and predators (third trophic level) are thought to be less effective at regulating gall-inducing insect diversity in xeric habitats, thus leading to greater diversity of gallers in such habitats (Castellanos, Cuevas-Reyes, Rios-Casanova, Oyama, & Quesada, 2006).…”

“…Studies have also shown that plants growing on water-and nutrient-deprived soils are more sclerophyllous (Poorter, Niinemets, Poorter, Wright, & Villar, 2009) and accumulate higher levels of chemical compounds . Thus, internalfeeding gall-inducing insects attacking such plants would experience greater protection from their natural enemies (Hardy & Cook, 2010;Ribeiro & Basset, 2007). These hypotheses have been supported by several studies conducted in tropical (Fernandes, Gonçalves-Alvim, & Carneiro, 2005;Jesus, Silva, & Fernandes, 2012;Julião, Almada, & Fernandes, 2014;Lara, Fernandes, & Gonçalves-Alvim, 2002) and temperate (Fernandes, Duarte, & Lüttge, 2003;Fernandes & Price, 1988 habitats.…”