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. 2019 Oct 10;13(10):e0007766.
doi: 10.1371/journal.pntd.0007766. eCollection 2019 Oct.

Enduring extreme climate: Effects of severe drought on Triatoma brasiliensis populations in wild and man-made habitats of the Caatinga

Affiliations

Enduring extreme climate: Effects of severe drought on Triatoma brasiliensis populations in wild and man-made habitats of the Caatinga

Antonia C Ribeiro et al. PLoS Negl Trop Dis. .

Abstract

Background: Triatoma brasiliensis, a triatomine-bug vector of Chagas disease, evolved in the semiarid Caatinga, where it occupies rocky outcrops, shrubby cacti, and human dwellings. Dwellings and rocks are considered high-quality microhabitats for this saxicolous species, whereas cacti probably represent secondary, lower-quality microhabitats. This 'microhabitat-quality hierarchy' hypothesis predicts that T. brasiliensis populations occupying dwellings or rocks should endure harsh environmental conditions better than their cactus-living relatives.

Methods/findings: We tested this prediction by comparing T. brasiliensis infestation (proportion of microhabitats with bugs), density (bugs per microhabitat), and crowding (bugs per infested microhabitat) in dwellings, rocks, and cacti sampled before and during the extreme drought that ravaged the Caatinga in 2012-2016. We used random-intercepts generalized linear mixed models to account for microhabitat spatial clustering and for variations in bug-catch effort; we assessed model performance and computed model-averaged effect estimates using Akaike's information criterion. Pre-drought infestation was similar across microhabitat types; during the drought, infestation remained stable in dwellings and rocks but dropped in cacti. Pre-drought bug density declined from dwellings to rocks to cacti; an additional decline associated with the drought was largely comparable across microhabitats, albeit perhaps somewhat larger in cacti. Finally, pre-drought bug crowding was higher in dwellings than in rocks or cacti and changed little during the drought-possibly with a downward trend in dwellings and an upward trend in cacti.

Conclusions: Triatoma brasiliensis populations fared better in dwellings and rocks than in cacti during extreme drought. Estimates of microhabitat and drought effects on infestation, density, and crowding suggest that only a few cacti (versus many rocks and dwellings) represent good-quality habitat under such extremely harsh conditions. Our findings provide empirical support to the microhabitat-quality hierarchy hypothesis, and imply that T. brasiliensis can endure extreme climate by exploiting high-quality microhabitats, whether wild or man-made, in the semiarid Caatinga.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The microhabitats of Triatoma brasiliensis: Human dwellings, rocky outcrops, and shrubby cacti.
The lower panel illustrates the hypothesis that microhabitat quality varies along a gradient running from top-quality dwellings through high-quality rock microhabitats (the primary habitat of the species) to lower-quality cacti (most likely secondary habitat); alternatively, a small minority of cacti may also represent high-quality habitat (white asterisk).
Fig 2
Fig 2. The microhabitat-quality hierarchy hypothesis: Predictions about habitat and drought effects.
Arrows in the plots emphasize drought-associated changes predicted by the microhabitat-quality hierarchy hypothesis. Note that we illustrate two alternatives for bug crowding in cacti–either it declines with the drought, suggesting that virtually all cacti are low-quality for the bugs (darker orange), or it increases, suggesting that a few cacti are high-quality and can act as ‘safe havens’ that sustain relatively large colonies (lighter orange, with a white asterisk emphasizing the link with Fig 1).
Fig 3
Fig 3. Rainfall in the study area, 2000–2018.
Total annual and mean annual rainfall for the pre-drought (2000–2011, blue), drought (2012–2016, orange), and post-drought (2017–2018, grey) periods. Blue–orange gradation indicates that drought effects were barely perceptible in 2012, and orange–grey gradation that drought effects were still at its peak in early 2017. Lighter-blue bars indicate pre-drought years with rainfall below the overall mean (713 mm; empty bar in the right-hand panel). Pre-drought field trips are indicated by green arrowheads, and drought field trips by red arrowheads, along the x-axis. The graphs summarize daily rainfall data from the Russas rainfall station (Fundação Cearense de Meteorologia e Recursos Hídricos; data available at http://www.funceme.br/).
Fig 4
Fig 4. Observed microhabitat infestation by Triatoma brasiliensis, bug density, and bug crowding.
Summary metrics by microhabitat (dwellings = triangles; rocks = squares; cacti = circles) both before (‘pre-drought’, blue) and during the drought (‘drought’, orange), with 85% confidence intervals (CI). Note that y-axes are on log10 scale.
Fig 5
Fig 5. Microhabitat and drought effects on wild and synanthropic Triatoma brasiliensis populations: Model-averaged slope-coefficient estimates and confidence intervals (CI).
Microhabitat effects are represented in yellow, drought effects in red, and microhabitat ×ばつ drought interactions in orange; intercepts (grey) are included for reference; the dashed horizontal line at zero indicates no effect.

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