Effects of biotic disturbances on forest carbon cycling in the United States and Canada

Forest insects and pathogens are major disturbance agents that have affected millions of hectares in North America in recent decades, implying significant impacts to the carbon (C) cycle. Here, we review and synthesize published studies of the effects of biotic disturbances on forest C cycling in the United States and Canada. Primary productivity in stands was reduced, sometimes considerably, immediately following insect or pathogen attack. After repeated growth reductions caused by some insects or pathogens or a single infestation by some bark beetle species, tree mortality occurred, altering productivity and decomposition. In the years following disturbance, primary productivity in some cases increased rapidly as a result of enhanced growth by surviving vegetation, and in other cases increased slowly because of lower forest regrowth. In the decades following tree mortality, decomposition increased as a result of the large amount of dead organic matter. Net ecosystem productivity decreased immediately following attack, with some studies reporting a switch to a C source to the atmosphere, and increased afterward as the forest regrew and dead organic matter decomposed. Large variability in C cycle responses arose from several factors, including type of insect or pathogen, time since disturbance, number of trees affected, and capacity of remaining vegetation to increase growth rates following outbreak. We identified significant knowledge gaps, including limited understanding of carbon cycle impacts among different biotic disturbance types (particularly pathogens), their impacts at landscape and regional scales, and limited capacity to predict disturbance events and their consequences for carbon cycling. We conclude that biotic disturbances can have major impacts on forest C stocks and fluxes and can be large enough to affect regional C cycling. However, additional research is needed to reduce the uncertainties associated with quantifying biotic disturbance effects on the North American C budget

<i>Cronartium ribicola</i> isolates and mitoviral contigs detected in their transcriptomes de-novo assembled in RNA-seq analysis.

<p><i>Cronartium ribicola</i> isolates and mitoviral contigs detected in their transcriptomes de-novo assembled in RNA-seq analysis.</p

Sequence alignment analysis of the putative RNA-dependent RNA polymerases (RdRp) of <i>Cronartium ribicola</i> mitoviruses (CrMV1 to CrMV5).

<p>Six conserved RdRp motifs (I to VI) among Cri-MVs are labelled according to previous report (Hong et al. 1999). Alignment analysis was performed using CLUSTAL program, and it included four other mitovirus species: FcoMV1 (BAQ36630), HfMV1 (AIU44705), HmMV1-18 (BAD72871), and SsMV1 (YP_009121785). Symbols (*), (:), and (.) below the sequences are used to indicate identical amino acids, or residues with chemical-similarities at higher and lower levels respectively.</p

Genomic variations of <i>Cronartium ribicola</i> mitoviruses (CrMVs) in BC and OR regions.

<p>Genomic variations of <i>Cronartium ribicola</i> mitoviruses (CrMVs) in BC and OR regions.</p

Distribution of minor allele frequency (MAF) of single nucleotide polymorphism (SNP) sites in the genomes of <i>Cronartium ribicola</i> mitoviruses (CrMV1 to CrMV5) as detected by RNA-Seq analysis.

<p>Distribution of minor allele frequency (MAF) of single nucleotide polymorphism (SNP) sites in the genomes of <i>Cronartium ribicola</i> mitoviruses (CrMV1 to CrMV5) as detected by RNA-Seq analysis.</p

Genomic RNA abundance of <i>Cronartium ribicola</i> mitoviruses (CrMV1 to CrMV5) as measured by qRT-PCR analysis.

<p><i>C</i>. <i>ribicola tubulin</i> transcript was used as the calibrator for normalization of input RNA levels across the 15 fungal isolates that are listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0154267#pone.0154267.t001" target="_blank">Table 1</a>. For each mitovirus, RNA levels in different fungal isolates were calculated according to the 2^−ΔΔCt algorithm using <i>C</i>. <i>ribicola</i> isolate BC-a6 as the reference. Means for relative levels of viral RNA accumulation in each type of samples are shown. Bars with different letters were significantly different using t-test (<i>P</i> <0.05). One, two, and three stars (*) indicate <i>P</i> <0.05, <i>P</i> <0.01, and <i>P</i> <0.001, respectively. Four comparisons were made as: (1) <i>avcr2</i> isolates (BC-a6, BC-a20, and BC-a28) <i>vs</i>. <i>vcr2</i> isolates (OR-a1, OR-a2, and OR-a3) at the aeciospore stage; (2) <i>avcr2</i> isolates (OR-sus1, OR-sus2, and OR-sus3) <i>vs</i>. <i>vcr2</i> isolates (OR-res1, OR-res2, and OR-res3) at the mycelium growth stage inside the cankered stem; (3) <i>avcr2</i> isolates at the stage of aeciospores (BC-a6, BC-a20, and BC-a28) <i>vs</i>. urediniospore (BC-u2a, BC-u3, and BC-u48), and <i>vs</i>. the stage of mycelium growth inside cankered stem (OR-sus1, OR-sus2, and OR-sus3), and different letters indicate significant differences between groups (p<0.05); (4) <i>vcr2</i> isolates at the stage of aeciospore (OR-a1, OR-a2, and OR-a3) <i>vs</i>. the stage of mycelium growth inside cankered stem (OR-res1, OR-res2, and OR-res3).</p

Phylogenetic tree analysis of the novel <i>Cronartium ribicola</i> mitoviruses (CrMV1 to CrMV5) and representative species (with GenBank accession numbers) of the genus <i>Mitovirus</i>.

<p>Neighbor-joining method was used for the phylogenetic analysis based on full-length alignment of RNA-dependent RNA polymerases (RdRp). Bootstrap support resulting from 1000 replicates is shown on the internodes and branch lengths correspond to genetic distance; the scale bar at lower left corresponds to a genetic distance of 0.2 for the RdRp sequences.</p