What Drives the Erasure of Protected Areas? Evidence from the Brazilian Amazon

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Consequence of stress response to combined stress

Due to the intensity, and duration of stress combination, the consequence of the combined stress varies (Tab. 1). Negative interactions of combined stresses can result in more severe adverse effects on the plant. For example, in Arabidopsis and barley, plants exhibited an aggravating effect on photosynthesis when they were exposed to drought and salinity simultaneously (Ahmed et al., 2013). The adverse effects of nutrient deprivation on plant growth and development are exacerbated when it comes in combination with other abiotic stresses because nutrients are required for the synthesis of ROS (Mittler and Blumwald, 2015; Mittler, 2017). Sometimes the adverse effect is more significant than the addition of two stresses. As a classical case of negative interaction, the antagonistic role in combined stress of drought and heat stress have been studied in many plants (VILE et al., 2011;
Prasad et al., 2011; Suzuki et al., 2014; Soolanayakanahally, 2018; Zinta et al., 2018). Under high-temperature stress, plants increase stomatal conductance and thereby reduce leaf temperature through transpiration (Salvucci and Crafts-Brandner, 2004; Way and Oren, 2010). Drought stress usually results in stomatal closure and higher leaf temperature, leading to a decrease in C fixation and thus limiting photosynthesis (Chaves et al., 2003). Taken together, plant growth was significantly reduced under drought and heat stresses and was even more detrimental under their combination (Vile et al., 2012; Prasad et al., 2011).
However, in some cases, combined stress is beneficial to plants in comparison to single stresses. As indicated, heat and drought stress negatively affected Arabidopsis biomass in many ways, but the increase of ambient CO2 concentration significantly alleviated the adverse effects. This mitigation effect of CO2 may be due to the rise of carbon fixation at high CO2 concentrations, which in turn up-regulates the synthesis of antioxidants (polyphenols, ASC and CAT). Through multi-omics analysis, Zinta et al. (2018) revealed that high CO2 alleviates the stress effects by inhibition of photorespiration and H2O2 synthesis. In Medicago truncatula, drought decreases stomatal conductance and promotes the synthesis of ascorbate and glutathione, which in turn improves plant tolerance to ozone (O3) (IYER et al., 2013). Henriet et al. (2020) illustrated that the moderate drought mitigated the negative effect of sulfur deficiency on the accumulation of S-rich globulins in seeds, due to a lower seed sink strength for nitrogen.
Moreover, continuous stress may cause stress memory or priming, which can pave the way to protect plants from future challenges (Hilker et al., 2015; Hilker and Schmülling, 2019). Stress memory is demonstrated to build plant resistance to the very same stress, or even another abiotic stress (Kissoudis et al., 2014; Rejeb et al., 2014). Virlouvet et al. (Virlouvet and Fromm, 2014) revealed that Arabidopsis plants undergoing drought remained at partial stomatal closure during a watered recovery period, facilitating reduced transpiration during subsequent dehydration stress. A systems-biology approach pointed out one gene module that coordinated changes in transcription memory responses established in maize (Virlouvet et al., 2018). It is also shown that pre-harvest UV-C treated plants displayed a stronger resistance to infection in strawberry leaves and led to reduced symptoms (Xu et al., 2019). Likewise, tomato seedlings treated by osmotic stress show adaptation to salinity and drought stress that is mediated by ABA (Andujar et al., 2011). This priming allows plants to respond more quickly to environmental challenges.
It should be noted that plant responses to sequential stresses in any order of the two stresses are often similar. For example, similar adverse effects of physiological limitations were found in the sequential treatment of the two strains in Arabidopsis (Zandalinas et al., 2019), barley (Hordeum vulgare) (Rollins et al., 2013), tobacco (Nicotiana tabacum) and citrus (Citrus reticulata) (Zandalinas et al., 2017), whether drought stress followed heat stress or heat stress followed drought stress. Plants were more severely damaged by combined stresses than by single stress, indicating that the response mechanisms of different plants to combined drought and high-temperature stresses are relatively conserved.
The positive or negative interactions between the combined stresses varied depending on the plant species. Adverse effects were found in wheat when plants were subjected to combined salt and heat stress (Keles and Öncel, 2002). However, the combination of salt and high-temperature stress mitigated the effects of single salt stress on the tomato. Under combined salt and heat stress, tomatoes accumulated large amounts of glycine betaine and trehalose in response, resulting in higher photosynthetic efficiency and leaf water potential. The accumulation of substances such as Glycine Betaine helps to maintain high K+ concentrations, thus ensuring a low Na+/K+ ratio and protecting the plant from salt stress (RIVERO et al., 2013). In addition, Glycinebetaine protects PSII from heat-induced inactivation (Allakhverdiev et al., 2003) and inhibits salt-induced K+ efflux (Cuin et al., 2008; Cuin and Shabala, 2005). Trehalose is important in maintaining photosynthetic capacity (Lunn, 2007) and also contributes to cellular resistance to oxidative stress (Chen and Murata, 2008; Garg et al., 2002). Meanwhile, under combined salt and heat stress, H2O2 accumulation and oxidative protein damage were inhibited, thereby protecting plants from oxidative stress (RIVERO et al., 2013).
In conclusion, plant response to combined stresses needs to be analysed case-by-case. It has been shown that abiotic stress can increase or reduce the resistance of plants to biotic stress. Heat stress leads to the accumulation of reactive oxygen species (ROS) and increases resistance to rice blast in rice (Oryza sativa) (Averyanov et al., 2000); drought and salt stress treatments also increase resistance to pathogens (Achuo et al., 2006). In contrast, abiotic stress has been reported to reduce tolerance to biotic stresses in Arabidopsis. For example, it has been shown that the expression of defence genes is down-regulated in virus-treated plants under combined drought and heat stress, which led to the deactivation of defence responses and higher susceptibility of plants (Prasch and Sonnewald, 2013). Cases of reverse interaction effect existed between N-deficiency and Botrytis infection (Soulie et al., 2020). In addition, high temperature-induced early flowering and suppressed resistance to abiotic stress in Arabidopsis (Liu et al., 2017). Thus, whether abiotic stresses can increase or reduce resistance to another stress depends on the intrinsic, timing, and intensity of the individual stress, as well as their interactions.

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Convergent physiological alterations of the combined stress response.

When plants are exposed to abiotic stresses, morphological and physiological alteration is mostly expected. Due to the nature of individual stress, how the plants perceive the stress varies. Different abiotic and biotic stress treatment can lead to some common processes as well as unique responses in physiological and molecular aspects.
Specific physiological strategies were commonly employed to respond to stress combinations. Stomatal changes are one of the critical components in regulating this process. The case of heat and drought stress described above has shown a perfect example of the conflicting need for stomatal adjustment toward individual stress. A negative effect on plant photosynthesis is expected when plants limit stomatal conductance in order to reduce transpiration. Another example is when plants were under combined heat and high light stress, both photosynthetic rate and stomatal conductance decreased and leaf temperature increased under high-temperature stress in plants. The effects were more severe under combined drought and high-temperature stress because under drought stress, the stomata of the leaves are usually closed, resulting in lower CO2 availability and limiting photosynthesis (Chaves et al., 2003).
Besides, sugar metabolism is altered in response to environmental stress. Soluble sugars, such as sucrose, fructose and glucose, are not only the metabolic building blocks and energy source but also function as signalling hub that interplay with hormones and nutrients in the fine-tuning of plant growth (Li and Sheen, 2016; Sakr et al., 2018). In cotton (Gossypium hirsutum), soluble sugars could affect auxin biosynthesis through Phytochrome Interacting Factors (PIF) proteins, which lead to anther abortion under heat stress (Min et al., 2014). Additionally, cell wall invertase hydrolyses sucrose and alters carbohydrate partitioning hence modulating defence responses (Tauzin and Giardina, 2014). Downregulation of cell wall-bound invertase expression and activity were observed in combined heat and drought stress (Prasch and Sonnewald, 2013).

Signalling mechanisms of combine stress :

To balance the trade-off of fitness costs and stress tolerance, a complex signalling regulatory crosstalk is mostly needed when facing combined environmental stresses. Studies have highlighted several common signalling components including calcium-dependent protein kinase, redox, mitogen-activated protein kinase (MAPK), transcription factors and hormone (Miltter et al., 2016; Zhang et al., 2017).
Second messengers, such as Ca2+ signalling pathways (Fig. 1), redox, and electrical signalling networks, play a crucial role in regulating cellular responses to the environment because of the rapid increase after stress stimulation (Gilroy et al., 2014; Ranty et al., 2016). Ca2+ is an essential second messenger for plants and an important regulator of plant growth and development, as well as an essential component of the plant cell wall (Hepler et al., 2005). Ca2+ functions in concert with other critical second messengers like ROS. Osmotic stresses as well as oxidative stresses, heavy metals, and ABA can cause elevated free Ca2+ concentrations in cytoplasm and induce redox perturbations in cells (Zhu et al., 2016). The Ca2+ and ROS signals are usually coupled with the propagation of electrical signals (Choi et al., 2017). A rapid increase in the rate of ROS production occurs as a response to stress conditions. The ROS molecules that mediate signalling functions include hydrogen peroxide (H2O2), singlet oxygen, hydroxyl radical and superoxide anion radical. The activation of mitogen-activated protein kinase (MAPK) cascade by H2O2 and subsequent upregulation of specific stress-related genes in Arabidopsis is a perfect example of ROS-mediated stress-response (Mittler et al., 2004). Nonetheless, Ca2+ and ROS-mediated responses of plants to environmental constraints just form the tip of the iceberg. The mechanism of stress-response in plants is highly intricate and requires several integrated pathways to be activated in response to external stresses. Also, evidence has been found that ROS and NO levels are regulated by auxin. Besides, the GLUTAMATE RECEPTOR-LIKE (GLR) has been reported to play an important regulatory role in electrical and Ca2+-mediated signal transduction (Stephens et al., 2008; Vincill et al., 2012).

Table of contents :

General Introduction
1 Protected Areas as Conservation Tools in the Brazilian Amazon
1.1 State of the Brazilian Legal Amazon within Brazil
1.2 Protected Areas to Safeguard Biodiversity and Reduce Greenhouse Gas Emissions
2 Challenges Associated with PA Designation and Maintenance
2.1 Conflicts over Land-Use and Location Bias
2.2 Have Protected Areas Been Effective?
2.2.1 Methodological Challenges
2.2.2 Summary of Main Empirical Results
3 Protected Area Downgrading Downsizing and Degazettement
3.1 Definition, Description and Extent in the Brazilian Amazon
3.2 PADDD as an outcome of the conservation-development trade-off in the Brazilian Amazon?
Chapter 1: What drives the Erasure of PAs? Evidence from the Brazilian Amazon
Chapter 2: Does the Selective Erasure of Protected Areas Raise Deforestation in the Brazilian Amazon?
Chapter 3: Who benefits from PADDD in the Brazilian amazon?
4 References
1 Chapter 1 What Drives the Erasure of Protected Areas? Evidence from the Brazilian Amazon
1 Introduction
2 Agency Perspectives on PA Size Reductions
2.1 Agency Benefits/Costs from Reducing Enforced PAs
2.1.2 Environment Agency (E)
2.1.3 Tradeoffs
2.2 Allowing for Illegal Environmental Damage in PAs
2.2.1.1 Probabilities of Illegal Activities
2.2.2 Implications for Agencies from Illegal Activities
3 Data & Empirical Strategy
3.1 Data
3.1.1 Scope & Observational Units
3.1.2 Dependent Variable (PADDD)
3.1.3 Independent Variables
3.2 Empirical Strategy
4 Results
4.1 Descriptive Statistics
4.2 Deforestation inside PAs
4.3 Drivers of PA Size Reductions
4.4 Drivers of PA Size Reductions – Robustness Checks
5 Discussion
6 References
2 Chapter 2 Does the Selective Erasure of Protected Areas Raise Deforestation in the Brazilian Amazon?
1 Introduction
2 Historical Background & Conceptual Model
2.1 Deforestation & Forest Protection in the Brazilian Amazon
2.2 Impacts of Protection & PA size reductions
2.2.1 Deforestation Baselines & PA Impacts By Location
2.2.2 Locations & Impacts of PA size reductions
3 Empirical Approach
3.1 Impact Estimation: matching both before & after erasures of protected areas
3.2 Data
3.2.1 Units of Observation
3.2.2 Variables
3.3 Method
3.3.1 Nearest-neighbour matching
3.3.2 Match Quality
3.3.3 Adding Temporal Analyses
3.4 PA Subsets: varying in expected impacts
4 Results
4.1 Descriptive Statistics
4.1.1
4.1.1 Protection Subsets vs. Unprotected (in terms of 2001-2008 deforestation)

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