Linking land, air and sea: potential impacts of biomass burning and the resultant haze on marine ecosystems of Southeast Asia

Abstract

Burning of crop residue and forest stands is a method commonly used to prepare land for agriculture in several countries within equatorial Asia (Gautam et al., 2013; Gadde et al., 2009; Aiken, 2004) and Central and South America (Anderson et al., 1996; de Vasconcelos et al., 2013a). Atmospheric emissions and smoke plumes (henceforth ‘haze’) from the burning of such biomass are impossible to contain and result in the depreciation of air quality of surrounding areas (Huang et al., 2013; de Vasconcelos et al., 2013b). In Southeast Asia, biomass burning is widely adopted in Kalimantan and Sumatra in Indonesia by plantation developers and smallholders (Tacconi & Vayda, 2006), with burning activities peaking during the intermonsoon dry season of July to October and intensifying during El Niño–Southern Oscillation (ENSO) years (Nichol, 1998; Wang et al., 2004). Prevailing northerly winds transport the resultant haze from areas of origin towards nearby Brunei, Malaysia, Philippines, Singapore and Thailand (Heil & Goldammer, 2001; Aiken, 2004). Biomass burning in Indonesia has intensified in frequency and severity since the 1970s (Heil & Goldammer, 2001), and transboundary haze is now an annual regional phenomenon. In June 2013, regional air pollution indices reached record highs, with values deemed hazardous in Singapore, Indonesia and Malaysia, prompting some affected areas to declare states of emergency (Carrasco, 2013). The AVHRR/3 sensor on NOAA Satellite 18 detected 437 discrete hotspots on Sumatra in a single day (24th June 2013), each presumably corresponding to a burning or recently burnt area. The effects of biomass burning and transboundary haze are far-reaching (Lohman et al., 2007). Losses in regional economies from the 1997 Southeast Asian haze episode were estimated to be USD 8.9–9.7 billion (Barber & Schweithelm, 2000). Hazardous air quality increased incidences of respiratory problems (Kunii et al., 2002) and mortality (Sastry, 2002), and lowered foetal and infant survival rates (Jayachandran, 2005). Biomass burning has also resulted in habitat and biodiversity loss, fragmentation of terrestrial ecosystems and disruption in terrestrial ecosystem functions (Kobayashi et al., 2004; Cheyne, 2008; Yule, 2010; Posa et al., 2011). The impacts of biomass burning and transboundary haze on terrestrial and atmospheric systems are immediate and obvious. Studies on biomass burning and haze have so far centered on atmospheric chemistry (Chang et al., 2013; Permadi & Oanh, 2013; Okada et al., 2001; Anderson et al., 1996), and regional biogeochemistry (Brauer & Hisham-Hashim, 1998). However, the synergistic effects of terrestrial biomass burning and resultant haze on marine systems have been scarcely addressed (Tacconi et al., 2008; Sundarambal et al., 2010a). Given the interconnectedness of atmospheric, terrestrial and marine ecosystems (McCauley et al., 2012) and the severity of biomass burning and haze episodes, we postulate that effects on marine systems are more critical than currently appreciated. There is an urgent need to fill these gaps in knowledge. Here, we discuss key putative impacts of biomass burning and haze, and the implications of these stressors on marine ecosystems (see Fig. 1), as well as propose potential research foci and solutions. Our focus on Southeast Asia is timely, with recurring episodes of biomass burning and transboundary haze escalating in prominence in the past several years. Information from such an opportune case-study for impacts to marine systems would be an important baseline for similar investigations in locations where biomass burning is also a significant issue. Biomass burning increases topsoil and ash runoff in streams and rivers (Rodenburg et al., 2003) and eventually the sea. In addition, over 100 compounds are released into the atmosphere when vegetative material is burnt, including oxides of carbon and nitrogen, ammonia and polynuclear aromatic hydrocarbons, which then enter marine ecosystems through wet deposition (Radojevic, 2003). Terrestrially derived nitrogen has been identified as a key cause of eutrophication in marine systems (Nixon, 1995) and eutrophication is one of the primary causes of seagrass bed loss (Orth et al., 2006). In hermatypic corals, elevated nutrients lead to higher bleaching risk by increasing zooxanthellae density in coral tissue when acting in concert with stressors such as ocean acidification (Cunning & Baker, 2013). Exposure to elevated nutrient levels also increases coral sensitivity to incident light (Wiedenmann et al., 2013) and decreases upper thermal bleaching thresholds (Wooldridge, 2009; Wooldridge & Done, 2009). Nutrient enrichment has been found to reduce reproductive fitness and increase mortality rates for some marine organisms as well (Loya et al., 2004; Sundbäck et al., 2010). During haze episodes, nitrogen and phosphorus concentrations in coastal waters off Singapore increased by three to eight orders of magnitude (Sundarambal et al., 2010a). Despite the rise in nutrient concentrations, eutrophication did not occur due to the high-nutrient baseline concentrations already present in the Singapore Straits (Sundarambal et al., 2010b). Still, these concentrations can trigger eutrophication in oligotrophic systems such as coral reefs and other nutrient-depleted shallow coastal areas with inadequate tidal flushing (Sundarambal et al., 2010b). Topsoil runoff that results from biomass burning increases sediment load in nearby watersheds and coastal waters (Rodenburg et al., 2003). Accumulated sediment particles on sedentary marine organisms cause tissue abrasion and anoxia, leading to bleaching and necrosis (Philipp & Fabricius, 2003; Weber et al., 2006). Suspended sediment particles contribute to turbidity and limit available light for photosynthetic and photosymbiotic organisms (Rogers, 1990). Corals living under high sediment loads expend energy on clearing sediment while coping with photosynthetic stress (Brown & Howard, 1985; Weber et al., 2006). Energy budgets are further compromised as the influx of sediment particles makes these readily available for uptake despite being poorer in nutritive quality when compared to zooplankton (Corner & Davies, 1971). Ingestion of these particulates compensates for light attenuation to a limited extent, but continuous exposure eventually leads to net losses of tissue mass and lipids (Anthony & Fabricius, 2000). Sustained sediment loading also affects coral growth and recruitment, compresses biotic zones, and alters community composition (Babcock & Davies, 1991; Fabricius, 2005; Dikou & van Woesik, 2006; Dikou, 2009), resulting in mortality in extreme cases (Dikou & van Woesik, 2006). Haze episodes can reduce photosynthetically active radiation (PAR, 400–700 nm) by up to 92% in terrestrial forests (Davies & Unam, 1999). Such a reduction in PAR was suboptimal for canopy trees and result in negative carbon balance for understory species (Strauss-Debenedetti & Bazzaz, 1996; Yanhong et al., 1996). During El Niño years, drought and haze resulted in high defoliation rates and decreased growth rates by up to 46% in rainforest plants (Yoneda et al., 2000). Although the effects of haze on the primary productivity of coral reefs, mangrove forests and seagrass beds have never been assessed, we hypothesize that they exhibit similar responses. Organisms hosting symbiotic zooxanthellae can acclimate to low light conditions by lowering their respiration rates (Rodolfo-Metalpa et al., 2008) and increasing symbiont density or chlorophyll concentration within their tissues (Falkowski & Dubinsky, 1981; Iglesias-Prieto & Trench, 1994; Titlyanov et al., 2001). Corals for example, are capable of acclimating to light availability by up to two orders of magnitude (Falkowski & Dubinsky, 1981), facilitated by variants of zooxanthellae maintaining photo-optimal efficiency (Hennige et al., 2008, 2010). Photoacclimation to low light levels occurs over time-frames short enough to respond to haze effects. However, this is a suboptimal state for the organisms as persistent low light conditions and high symbiont density increase the likelihood of bleaching (Cunning & Baker, 2013). These acclimation processes can also be subject to genetic constraints, and the delay for an adaptive response further compromise the abilities of these corals to repair damaged tissue, deposit optimal δ13C in skeletal structures, and recover from the effects of synergistic impacts (Falkowski & Dubinsky, 1981; Risk et al., 2003; Titlyanov & Titlyanova, 2009). Although lowered PAR values can affect marine productivity, consistently high PAR levels, in conjunction with high sea surface temperatures during ENSO years, exacerbated mass bleaching events (Brown, 1997; Dunne & Brown, 2001). Dry conditions during ENSO years further intensify biomass burning and haze episodes, enhancing surface radiation absorption and decreasing light intensity (Ilyas et al., 2001). Atmospheric attenuation from haze events can thus mitigate some of the effects of high PAR and elevated sea surface temperature during ENSO years to marine organisms (Kwiatkowski et al., 2013; Gill et al., 2006; Mumby et al., 2001). However, lowered PAR may not always be accompanied by a reduction in photosynthesis. In terrestrial environments, elevated aerosol levels, such as from biomass burning, promoted primary productivity by increasing the amount of diffuse solar radiation (Oliveira et al., 2007; Mercado et al., 2009). In marine systems, light in the water is already diffused, and organisms are unlikely to benefit from further increases in diffused radiation. The overall biological responses to the synergistic effects due to the decrease in PAR levels during severe haze episodes remain unknown. During mass burning episodes, visibility can decrease from 10 km to almost 0 km (Wang et al., 2004). The significant reduction in visibility poses high risks for some of the world's busiest airline hubs and shipping lanes (Nichol, 1998; Chou, 2006) and has been implicated in several vessel collisions (Nichol, 1998). Collisions between tankers may leak quantities of oil, phenol and toxic chemicals that have immediate lethal effects on estuarine and marine biodiversity (Jackson et al., 1989; Koto et al., 2013) or cause sublethal effects such as erosion of mucus membranes, cell damage, population reductions and suppressed immune responses (Dyrynda et al., 2000; Peterson et al., 2003). Southeast Asia is an archipelagic region, with extensive coastlines and shallow seas that support high levels of endemism, and is considered one of the centres of global marine biodiversity (Myers et al., 2000; Barber, 2009). Due to unsustainable coastal development and anthropogenic activities, over 85% of coral reefs in Singapore, Indonesia and Malaysia are threatened (Burke et al., 2002). Similarly, at least 80% of all mangrove forests in Southeast Asia have been lost in the past 60 years (Polidoro et al., 2010; Yee et al., 2010) while terrestrial run-off, pollution, dredging and bottom trawling are some of the persistent threats facing seagrass ecosystems (Freeman et al., 2008; Unsworth & Cullen, 2010). In addition, the millions of people living within coastal areas depend heavily on marine natural resources for food and income (Vincent, 2011). Nevertheless, marine ecosystems in this region contribute greatly to global marine capture fisheries with Indonesia, Malaysia and Thailand ranked in the top 20 global exporters of fisheries products (Vannuccini, 2003). Indonesia and Thailand, for example, together contributed 19% by volume of the total fisheries products imported into the United States in 2007 (van Voorhees & Pritchard, 2008). The impacts of biomass burning and transboundary haze on marine productivity are currently unknown. The resulting stressors probably vary in occurrence and intensity among ecosystem types throughout the region with shallower waters closer to areas with prolonged burning activities likely to be most affected. Depending on prevailing wind conditions, the impact of transboundary haze to marine ecosystems within the region will also vary. In semi-enclosed and poorly flushed coastal ecosystems, cascading impacts from eutrophication events can lower outputs from high-density fish and shellfish farms common along coastal margins, potentially disrupting global fisheries supply and significantly affecting local and national economies (Chua et al., 1989; Naylor et al., 2000). Within highly interconnected marine systems, we expect haze-related stressors to have synergistic impacts on organism physiology and ecosystem function as multiple stressors intensify overall impacts on communities (Atalah & Crowe, 2010). However, research in this area is nascent at best. Smoke-haze events, while initially suppressing rainfall, ultimately cause more severe thunderstorms (Andreae et al., 2004). Storms affect coral reefs at various spatial and temporal scales, and result in depressed survival and recruitment rates in many coral species (James et al., 2007). For marine organisms already compromised in terms of energy budgets, immunity against diseases, restoration of damaged cells and reproductive capacities, synergistic impacts can feed into a positive feedback cycle that escalate risks to marine ecosystems and consequently affect marine ecosystem goods and services (Scheffer et al., 2001). There is still much to achieve in understanding how biomass burning and haze impact marine ecosystems. After wet deposition, the fate of the majority of aerosols and particulate organic matter emitted during biomass burning remains unclear (Sundarambal et al., 2010b). We propose research efforts to elucidate pathways for terrestrial and atmospheric inputs into the marine environment (Shinn et al., 2000; McTainsh & Strong, 2007), especially nutrients (e.g., oxides of carbon, nitrogen, ammonia, polynuclear aromatic hydrocarbons). To date, the impacts of only a small fraction of organic compounds have been investigated. We thus recommend studies into the sublethal effects of these particulates, in particular, their roles in altering organismal and systems biochemistry. Although marine ecosystems are highly connected (Cowen et al., 2007; Dorenbosch et al., 2007), stressors for one ecosystem are often not considered for another. On coral reefs, the effects of reduced PAR have been well-studied, but the same knowledge is severely lacking for adjacent mangrove and seagrass communities. Tracking environmental variables such as suspended solid values and PAR levels across ecosystems is recommended to obtain temporal variation in ecosystem patterns. Baseline datasets such as these will offer insights into the interactive and cascading secondary impacts of biomass burning and haze episodes. Additionally, we recommend prioritizing regional collaborations to gather, compile and share relevant data (e.g., baseline and current environmental parameters for atmosphere, wet deposition and coastal waters) on biomass burning and haze-related effects on marine ecosystems. Although costly, long-term monitoring is essential and should be reflected in management plans as long-term data provide insights into temporal variation in ecosystem patterns (Caughlan & Oakley, 2001; Loneragan et al., 2013). Regional collaborative monitoring and the development of focused programs can facilitate data gathering and analysis while decreasing costs. The framework to carry out regional collaborative monitoring is already in place; agencies such as Seagrass Watch and the Global Coral Reef Monitoring Network (GCRMN) have been monitoring habitats of interest on a global scale. The cooperation of such agencies with scientific and government bodies in Southeast Asia can aid in the rapid sharing and dissemination of information. It is time to recognize biomass burning and haze as one of the major stressors of marine ecosystems in addition to overfishing, coastal development, climate change, and ocean acidification. The results from all the recommended studies are important as a feedback mechanism to fine-tune response protocols. The availability of such information, and alerts to decision-makers and managers in a timely fashion, is crucial to threatened marine ecosystems. Land-air-sea connectivity is a less obvious issue for policy-makers when considering biomass burning and haze. Even though both the atmosphere and the sea are open systems, the impact of the haze to the atmosphere is more visually apparent when compared with the lagged and obscured responses of the marine ecosystems. In addition, because the end impacts of biomass burning and haze are similar to common marine impacts from other anthropogenic activities (for example, sediment run-off from coastal development), the sources of these impacts during a haze episode may not have been seriously considered. Biomass burning and haze episodes are expected to increase in severity and we anticipate future episodes to worsen. Marine ecosystems in Southeast Asia already face multiple anthropogenic stressors. Taking the critical steps towards gathering vital baseline information and understanding the direct and indirect impacts from biomass burning will ensure greater preparedness to manage the effects from increasingly severe burning and haze events on threatened marine ecosystems in Southeast Asia and other regions of the world. The authors thank the following: Ria Tan for her comments on the initial draft, Lynne Parenti and Joseph Pawlik for editing and discussions on the revised versions of the manuscript, as well as the four anonymous reviewers and the subject editor whose suggestions improved the manuscript. The authors declare no conflict of interest.