Do secondary compounds inhibit microbial- and insect-mediated leaf breakdown in a tropical rainforest stream, Costa Rica?

Abstract

We examined the hypothesis that high concentrations of secondary compounds in leaf litter of some tropical riparian tree species decrease leaf breakdown by inhibiting microbial and insect colonization. We measured leaf breakdown rates, chemical changes, bacterial, fungal, and insect biomass on litterbags of eight species of common riparian trees incubated in a lowland stream in Costa Rica. The eight species spanned a wide range of litter quality due to varying concentrations of nutrients, structural and secondary compounds. Leaf breakdown rates were fast, ranging from 0.198 d(-1 )(Trema integerrima) to 0.011 d(-1) (Zygia longifolia). Processing of individual chemical constituents was also rapid: cellulose was processed threefold faster and hemicellulose was processed fourfold faster compared to similar studies in temperate streams. Leaf toughness (r = -0.86, P = 0.01) and cellulose (r = -0.78, P = 0.02) were the physicochemical parameters most strongly correlated with breakdown rate. Contrary to our initial hypothesis, secondary compounds were rapidly leached (threefold faster than in temperate studies), with all species losing all secondary compounds within the first week of incubation. Cellulose was more important than secondary compounds in inhibiting breakdown. Levels of fungal and bacterial biomass were strongly correlated with breakdown rate (fungi r = 0.64, P = 0.05; bacteria r = 0.93, P < 0.001) and changes in structural compounds (lignin r = -0.55, P = 0.01). Collector-gatherers were the dominant functional group of insects colonizing litterbags, in contrast to temperate studies where insect shredders dominate. Insect biomass was negatively correlated with breakdown rate (r = -0.70, P = 0.02), suggesting that insects did not play an important role in breakdown. Despite a wide range of initial concentrations of secondary compounds among the eight species used, we found that secondary compounds were rapidly leached and were less important than structural compounds in determining breakdown rates.

Leaf breakdown in a natural open tropical stream

“…Leaching occurs throughout the decomposition process (Gessner et al, 1999); however, in the present study, the reductions in total polyphenols and condensed tannins occurred slowly, particularly during the first month of incubation, due to the hardness of the leaves, which protects against water loss (Edwards et al, 2000). However, these results are inconsistent with several studies in tropical streams (Albariño and Balseiro, 2002;Schlickeisen et al, 2003;Ardón and Pringle, 2008), although they agree with the studies of Gonçalves et al (2012aGonçalves et al ( , 2012b on native detritus in Brazilian savanna streams.…”

“…According to Gonçalves et al (2006a), these two groups could be responsible for structuring the invertebrate community due to their strong colonization capacities, regardless of litter quality or the stage of decomposition. Litter species with low decomposition rates may be more important as substrates for the fixation of invertebrates and may eventually become the source of fine particles (Ardón and Pringle, 2008). In the present study, both B. platypoda and C. cereifera decomposed slowly.…”

“…In a laboratory study, Canhoto and Graça (1999) showed that secondary compounds decreased fungal biomass on leaves. In contrast, Ardón and Pringle (2008) suggested that secondary compounds in leaves might not persist long enough to limit microbial or insect damage because of the rapid leaching of total phenolics, condensed tannins and hydrolyzable tannins. Indeed, their results indicate that structural compounds are important in determining fungal and bacterial biomasses during leaf breakdown, supporting our results.…”

Relationships of shredders, leaf processing and organic matter along a canopy cover gradient in tropical streams

“…Evidence from global studies indicates high variability in shredder occurrence and in breakdown rates across tropical sites (Boyero et al, 2012(Boyero et al, , 2015, which corroborates contrasting results obtained in tropical regions. A growing body of evidence emphasizes the importance of algal carbon in tropical food webs of forested small streams (Salas and Dudgeon, 2001;Mantel et al, 2004;Brito et al, 2006;Li and Dudgeon, 2008;Lau et al, 2009;Neres-Lima et al, 2016;Brett et al, 2017) and it has been claimed that the contribution of macroinvertebrate shredders to leaf breakdown is small in certain tropical running waters due their scarcity (Dudgeon and Wu, 1999;Dobson et al, 2002;Gonçalves et al, 2006bGonçalves et al, , 2007Ardón and Pringle, 2008;Alvim et al, 2015). On the other hand, there is contrary evidence of high diversity and abundance of macroinvertebrate shredders, high secondary production and importance on leaf breakdown (Cheshire et al, 2005;Camacho et al, 2009;Yule et al, 2009;Encalada et al, 2010;Masese et al, 2014;Tonin et al, 2014;Andrade et al, 2017;Neres-Lima et al, 2017).…”

A decomposição de detritos foliares de espécies nativas e exótica e a colonização de macroinvertebrados em um riacho tropical localizado na Floresta Nacional de Ipanema, SP, Brasil

“…Sua remoção tem grandes efeitos sobre estes ecossistemas, já que afeta diretamente o aporte de detritos vegetais e a disponibilidade alimentar dos invertebrados aquáticos (Ardón & Pringle, 2008;Kominoski et al, 2012), gerando assim impactos sobre a composição da fauna de organismos macroinvertebrados. (Danger & Robson, 2004;Spanhoff et al, 2007;Yoshimura, 2012).…”