How will bark contribute to plant survival under climate change? A comparison of plant communities in wet and dry environments. Julieta Rosell, Instituto de Ecología, Universidad Nacional Autónoma de México [email protected] INTRODUCTION Climate change and the effect on vegetation structure and function Climate change is bringing new conditions of temperature, rainfall, and fire regime in most of the world (Ipcc, 2014). These new conditions are affecting ecosystems worldwide, including forests. Forests in general, and tropical forests in particular, have a very strong role in the regulation of climate (Bonan, 2008) and are crucial to the provision of multiple ecosystem services (Brandon, 2014). Because of this importance, there is an ever- increasing interest in understanding how tropical forests respond to these new climate conditions (Cavaleri et al., 2015). Understanding the mechanistic causes of these responses is crucial to manage the effect of climate change on terrestrial ecosystems. Several studies have addressed the effect of new climate conditions on plant traits and performance (Corlett & Westcott, 2013; Soudzilovskaia et al., 2013; Law, 2014; Tausz & Grulke, 2014). These studies have indicated that, for example, plants have started to produce flowers and leaves earlier in spring (Cleland et al., 2012), and that higher net primary productivity will increase as a result of climate change in certain areas (Nemani et al., 2003), whereas increased tree mortality will be expected in others (Anderegg et al., 2013). Most studies have mainly focused on well known organs such as leaves (Li et al., 2015) and wood (Choat et al., 2012). Despite being so important for plant function and representing a significant amount of biomass, the role of bark in the response to climate change and in plant survival in general is unclear. This project aimed to examine the role of bark on key plant functions that could aid in managing the effects of climate change on vegetation. The role of bark in plant function Bark is the part of tree trunks we see every day. Immensely varied and often beautiful, bark is the complex and mostly living region of the stem external to the wood (Evert & Eichhorn, 2006) (Fig. 1) Bark is extremely important for plants, being involved in many vital functions (Romero, 2014). Bark transports photosynthates, protects stems from fire, pathogens, and herbivore damage (Gill & Ashton, 1968; Romero & Bolker, 2008; Romero et al., 2009; Lawes et al., 2011), stores water and other compounds (Srivastava, 1964; Scholz et al., 2007; Rosell et al., 2014), provides mechanical support to stems (Niklas, 1999; Rosell & Olson, 2007; Rosell et al., 2014), and contributes to photosynthesis (Pfanz et al., 2002). The many functions bark performs are reflected in its complex anatomical structure. Bark includes a mostly living inner portion (inner bark), specialized in photosynthate transport, storage and photosynthesis, and an outer mostly dead region (outer bark) associated mainly with protection against fire (Graves et al., 2014) (Fig. 1). Despite its remarkable diversity and conspicuousness, and the many roles it performs, the contribution of bark to plant survival is not well documented (Paine et al., 2010; Poorter et al., 2014). 1 Figure 1. Bark has a complex structure composed of a mostly living inner layer of tissues and a mostly dead outer region. Bark and plant responses to climate change Some poorly understood contributions of bark to plant function are particularly important in the context of climate change. One of these functions is storage. Water and starch storage in stems is usually credited to wood, which seems to contribute to leaf and flower flushing, especially in seasonal areas (Borchert, 1994; Chapotin et al., 2006b). However, bark almost certainly also makes a vital contribution to stem storage (Srivastava, 1964), but it is not clear how this storage compares to that carried out by wood. In addition to leaf flushing, water and solutes in bark could also buffer fluctuations in water availability in stems (Scholz et al., 2007), contributing to the refilling of vessels after embolism (Hölttä et al., 2006; Zwieniecki & Holbrook, 2009; Nardini et al., 2011). Because of all of these potential roles, assessing bark’s role in storage is crucial for understanding plant survival under the increasingly dry conditions expected under climate change in many areas (Allen et al., 2010). In addition to storage, bark also seems to be very important for the mechanical support of stems (Niklas, 1999). Because of its position farthest from the neutral axis (Niklas, 1992) and because of its relatively high abundance in terminal branches and twigs (Rosell & Olson, 2014), bark could be decisive in whether a twig breaks, leaving the stem wounded and unprotected. Despite this potentially important role, bark mechanical behavior has been assessed only in a few taxa (Bauer & Speck, 2012; Rosell & Olson, 2014). As a result, we understand little about bark contribution to stem stiffness and how this contribution varies across species (Rosell et al., 2014). Assessing bark mechanical performance is crucial to predict the effect on tree crowns of the increasingly stronger and more frequent hurricanes affecting tropical areas (Knutson et al., 2010). Another factor that will be affected as a result of climate change is fire regime (Rocca et al., 2014). The combination of drier and warmer conditions will increase the likelihood of fire in many areas (Moritz et al., 2012). Bark has been shown to be a crucial region protecting plants from fire (Lawes et al., 2011). Bark not only protects the cambium from direct burning, but also from the effects of very high temperatures on the integrity of the conductive system (Michaletz et al., 2012). In this regard, bark thickness is a crucial trait reflecting the degree of protection provided by bark against the damages of fire (Pausas, 2015). The likelihood of plant survival after fire has been modeled based on bark thickness, and thresholds have been established for some vegetation types (Hoffmann et al., 2012; Lawes et al., 2013). These thresholds could be a good starting point to assess the 2 vulnerability of plant communities to the effect of more frequent fires resulting from the new conditions of climate change. Another crucial gap in our understanding of the ecological role of bark has to do with its role in the carbon cycle. We lack precise estimates of the amount of carbon stored in bark (Paul et al., 2008), mainly because estimates come from the forestry literature, where bark of crowns is usually neglected. Bark can represent a large proportion of twig biomass, being 50% or more of the stem transectional area (Rosell et al., 2014), so current estimates likely understimate the amount of bark carbon in forests. The current estimate that15% of plant biomass in forests is represented by bark (Jenkins et al., 2003) will likely increase significantly when crowns are taken into account. Better estimates of bark biomass are vital to understand the amounts and patterns of carbon sequestration in the biosphere. This project addressed the role of bark in three basic functions, namely water and carbohydrate storage, protection from fire, and mechanical support, and the role of bark in the carbon cycle. These questions are very important in the context of climate change, which predicts a higher risk for plant communities as a result of increasing temperatures, drought, fire, and hurricane activity (Dale et al., 2001; Choat et al., 2012), and which requires a clearer understanding of the carbon stored in forests (Pan et al., 2011). Study sites: Chamela-Cuixmala and Los Tuxtlas Reserves To examine the role of bark in these key aspects, this project was carried out in two Mexican Man and the Biosphere Reserves, the Chamela-Cuixmala and Los Tuxtlas reserves, which offered an ideal comparison of dry and wet environments. The Chamela- Cuixmala reserve is located in the Pacific coast of Mexico (Fig. 2) and is mostly dominated by seasonally dry tropical forest. The mean annual precipitation at the site is 748 mm and the mean annual temperature is 24.9 ºC. It is a highly seasonal environment with practically all of its rain falling between July and October (Lott et al., 1987). The Chamela-Cuixmala Reserve is highly biodiverse. It includes more than 1200 species of vascular plants, 427 species of vertebrates and more than 2000 species of insects, including a very high level of endemism (Lott & Atkinson, 2002; Pescador-Rubio et al., 2002). In addition to its biodiversity, the Chamela-Cuixmala Reserve is particularly important because it represents one of the few protected areas of seasonally dry tropical forest in Mexico and in the world. The Chamela-Cuixmala reserve also includes a dozen villages and towns in its area of influence, many of which make use of the resources of their local dry forests (Sánchez- Azofeifa et al., 2009). These villages represent pressures for the forest in the reserve also as a result of agricultural practices. In addition to these pressures, the reserve has started to be affected strongly by climate change. Trends have been already detected for longer dry seasons (Yamanaka, 2012), and also for more frequent hurricanes. The site has been severely disturbed by two very recent hurricanes, Jova in October 2011 (Álvarez-Yepiz et al., 2015) and Patricia in October 2015. Although the area usually gets most of its rain from tropical storms in the Pacific, these storms do not usually make landfall, but simply bringing rain on their margins. These two recent hurricanes, which made landfall directly in the area of the Reserve, could reflect a future trend of more frequent and more severer hurricanes at this site as part of climate change effects in the tropical Pacific (Knutson et al., 2010). 3 !"# %"# &"# $"# '"# Figure 2. Chamela-Cuixmala reserve location in the Pacific coast of Mexico (a), its seasonally dry tropical forest (b), and bark diversity (c-e).