Recent Trends of Demersal Marine Fish and Invertebrate Production in Southeast Asia – A Hypothesis-based Analysis

Demersal marine fish and invertebrate production data for Southeast Asia (1996–2007) obtained from the Southeast Asian Fisheries Development Center (SEAFDEC) statistical bulletin indicated a reduced production by Thailand largely due to over-exploitation and altered coastal ecosystems. In contrast, increased production by Philippines, Indonesia and Malaysia was due to an increase in mechanised fishing fleets. Moreover, marginal increases in the ecosystem indicators were attributed to increased exploitation of high and mid trophic level organisms suggesting the development of “top-down” cascade effect in the future. In this bioregion, land use pattern affecting water quality coupled with altered monsoonal sequences and rising sea surface temperatures interfere with biological processes. The most apparent manifestations of these disturbances are recurrences of extensive algal blooms and coral bleaching events. Fish mortality as a result of these events threatens to weaken the native biota and facilitate invasions that would modify the trophic dynamics of the coastal habitats.


INTRODUCTION
The biologically diverse coastal seas in Southeast Asia (Figure 1), endowed with myriad faunal assemblages (Kathiresan and Rajendran 2005;Keesing and Irvine 2005;Mazlan et al. 2005), are aptly regarded as the epicentre of global marine biodiversity.The coastal wetlands in this region harbour 75 species of mangrove trees (Son and Thuoc 2003), and some 700 scleractinian coral species in reefal habitats (Hutomo and Moosa 2005;Keesing and Irvine 2005).These ecosystems, besides being natural barriers to tropical storms and tsunamis, support approximately 40% of the marine fish species found in the region with high levels of endemicity (Keesing and Irvine 2005).However, the utility of mangroves and corals as construction material, conversion of wetlands into aquaculture farms, coastal pollution (Hutomo and Moosa 2005), land reclamation for human settlements, and destructive fishing activities (Burke et al. 2002) are potentially perilous to these fragile ecosystems.
On the other hand, recent shifts in monsoonal sequences and increasing sea surface temperature associated with the El Niño and La Niña phenomena have wreaked havoc through frequent tropical cyclones, coral bleaching events (Mazlan et al. 2005) and harmful algal bloom formations (Wang et al. 2008), thereby potentially altering ecosystem functions like fisheries.Stocks of large demersal and small pelagic fish, as well as benthic invertebrates are threatened owing to demand-driven uninhibited fishing by mechanized fishing vessels and other destructive techniques in coastal and deeper waters (Armada 2004;Barut et al. 2004;Hutomo and Moosa 2005;Morgan and Staples 2006).The above events could potentially alter the life cycles and ecology of the resident faunal assemblages with long-lasting effects on the biological processes including feeding, migration and reproduction, with disastrous consequences for commercially exploitable fish and invertebrate stocks in the region.
In view of above, the present study seeks to provide a synoptic view of the demersal marine fisheries trends of the Southeast Asian region during 1996-2007.Further, we take a holistic approach to determine the causes of decline of marine fisheries in this region during the above period with due consideration on the roles of both natural and anthropogenic factors.

Data collation
Marine capture fishery and aquaculture production datasets of nine Southeast Asian countries (Brunei Darussalam, Cambodia, Indonesia, Malaysia, Myanmar, Philippines, Singapore, Thailand and Vietnam; Figure 2) for the period from 1996-2007 were obtained from the SEAFDEC (2013).Subsequently, available datasets of 53 demersal (and bentho-pelagic) fishery groups from only four out of the nine countries (Thailand, Indonesia, Malaysia and Philip-pines) were obtained from SEAFDEC (2013), clumped into three broad categories namely demersal fishes (37 groups/species), crustaceans (eight groups) and molluscs (eight groups), and their trends were examined.Additionally, certain bentho-pelagic fishes such as carangids and hairtails were also included in the analysis due to their occurrence in the demersal trawl hauls.Moreover, 18 pelagic fish groups (Appendix 1) were included to aid in hypothesizing ecological responses of both demersal and pelagic fish and invertebrate assemblages to climate change and anthropogenic interference.
In addition, datasets indicating the size of the marine fishing fleets and categories of vessels (available for only three countries namely Indonesia, Malaysia and Thailand) were obtained from SEAFDEC (2013).Altogether, available data for 10 types of vessels were classified into five categories namely Non-powered, Outboard powered, Small inboard powered (including < 5 tons, 5-10 tons, 20 tons, 20-50 tons), Medium inboard powered (including 50-100 tons, 100-200 tons) and Large inboard powered (including 200-500 tons, 500 tons and over) vessels.

Fish stock assessment
Stock status of all 53 demersal fisheries of the above four countries (considering the year 1996 as the base/initial year) was examined separately following the criteria (Table 1) provided by Froese and Kesner-Reyes (2002).

Ecosystem health assessment
Ecosystem indicators such as MTI (Pauly et al. 1998) and FiB (Pauly et al. 2000) were computed using the catch data to assess the status of marine demersal capture fisheries of four countries and their effects on the coastal ecosystems.For these analyses, trophic levels of the demersal species examined were obtained from Fishbase (Froese and Pauly 2013) and Sea Around Us Project (Pauly 2013).Subsequently, demersal species/groups examined were segregated into three trophic levels namely HTL (>3.51),MTL (2.51-3.50)and LTL (< 2.51) after modifications in trophic level criteria provided by Vivekanandan et al. (2005).

Country-wise comparison of catch trends among trophic levels
Catch figures of individual species obtained from published data (SEAFDEC 2013) within a particular trophic level group (HTL, MTL or LTL) were summed up and their trends were compared for the period from 1996-2007.

Overview of catastrophic events
Review of literature on HAB and coral bleaching events that occurred during 1996-2007 was undertaken to collate information on these catastrophic events, in order to assess their effects on the marine fisheries production trends throughout Southeast Asia.

Overall trends: marine capture fisheries and aquaculture
Marine fish (and invertebrate) production through marine capture fisheries and aquaculture sectors in Southeast Asia displayed an increasing trend from 1996-2007.However, during the above period, production through capture fisheries increased only 41.8%, as compared to 285.3% through aquaculture (Figure 2A).

Marine demersal capture fisheries: country-wise trends
Datasets from only four countries namely Indonesia, Malaysia, Philippines and Thailand were selected for the analysis due to availability of continuous data from 1996-2007.The numbers of fishery groups analyzed for the above countries were 41, 41, 45, and 36, respectively (Table 2).The combined trends of marine demersal species production in these countries revealed an 18.0% increase during the above period.Country-wise trends for the period from 1996-2007 are provided below.

Indonesia
Total demersal landings increased from 1.901 MMT in 1996to 2.611 MMT in 2007 (37.3% increase).Landings of demersal fishes, crustaceans and molluscs increased by 37.6%, 52.8% and 2.0%, respectively, during the above period (Figure 3B).Out of the 41 fishery groups assessed, stocks of five groups were overfished, 29 fully exploited, whereas fisheries of seven groups were developing (Table 2).

Malaysia
Total demersal landings increased from 0.851 MMT in 1996 to 1.027 MMT in 2007 (21.68% increase).Landings of demersal fishes and molluscs increased by 25.6% and Table 1.Criteria for determining the status of exploitable fish stocks.( 52.2% respectively.In contrast, crustacean landings decreased by 26.0%, over the same period (Figure 3C).Out of the 41 fishery groups assessed, stock of one group had collapsed, three groups were overfished, 35 fully exploited, whereas fisheries of two groups were developing (Table 2).

Philippines
Total demersal landings increased from 0.790 MMT in 1996 to 1.370 MMT in 2007 (73.4% increase).Landings of demersal fishes, crustaceans and molluscs increased by 40.5%, 457.32% and 6.7%, respectively, during the above period (Figure 3D).Out of the 45 fishery groups assessed, stocks of 11 groups were overfished, 33 groups fully exploited, whereas fishery of one group was developing (Table 2).

Thailand
Total demersal landings decreased from 1.944 MMT in 1996 to 1.463 MMT in 2007 (24.8% reduction).Landings of demersal fishes, crustaceans and molluscs decreased by 21.4%, 51.8%, and 26.9% respectively during the above period (Figure 3A).Out of the 37 fishery groups assessed, stocks of 16 groups were overfished, 20 fully exploited, whereas fishery of one group was developing (Table 2).

Overall trends of fishing fleet size
Available datasets for the number of marine fishing vessels from four countries for the period from 1996 to 2007 revealed a substantial increase in the size of the Indonesian (40.7%; Figure 2F) and Malaysian (25.3%; Figure 2G ).However, fishing effort for Singapore was not considered as the fishery fleet for marine capture fisheries of this nation is very small (less than five vessels), and fishery yield is generated mostly by private fishermen (Figure 2H).Segregated datasets for size categories of marine fishing vessels revealed that traditional/artisanal nonpowered boats dominated the fishing fleets of Indonesia (Figure 4A) and Malaysia (Figure 4B).On the other hand, small-capacity inboard-powered vessels (up to 50 tons) dominated the Thai fishing fleet (Figure 4C).

Catch trends at various trophic levels: A comparison
In the case of Thailand and Malaysia, the mean MTL catches for the period from 1996-2007 were higher than HTL and LTL species (Figure 5A-B), whereas mean HTL catches in Indonesia and Philippines far exceeded MTL and LTL catches (Figure 5C-D).

Coral bleaching and HAB events
A review of published literature pertaining to catastrophic marine events such as large-scale coral bleaching and extensive HAB formations during 1996-2007 revealed that these events were largely associated with the El Niño phenomenon that originated in the Eastern Pacific region (Table 3).

DISCUSSION
Analysis of recent trends (1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007) of marine fish and invertebrate production throughout Southeast Asia indicated 41% growth in the marine capture fisheries sector.Contemporary global marine capture fisheries trends indicated an overall drop of 10% in landings (FAO, 2011).A noteworthy boom was witnessed in the mariculture sector throughout Southeast Asia, which was concurrent with recent global trends (FAO, 2011).Further analysis of available data on total seafood production (including pelagic and demersal fisheries) in four countries, namely Indonesia, Malaysia, Philippines and Thailand (data combined) suggested a very slow growth rate (18.1%) during 1996-2007.Contemporaneously, demersal (and benthopelagic) fish production increased by 17.8%.However, there was a marginal decrease in MTI of Southeast Asian demersal fisheries (concurrent with global trends) largely due to a surge in the exploitation of HTL and MTL species.Analysis of the seafood production trends by country suggested that there were disparities in the growth rates of marine fisheries of individual countries and the same has been discussed here on the basis of a trophic web hypothesis.
It is well established that in a generalized marine ecosystem, anthropogenic removal (fishing) of a particular trophic level would have broad implications for the entire marine food web (Steneck 1998).For example, the removal of top predators and HTL species would cause: (A1) lowering of predation pressure on the MTL species (Sala et al. 1998); (A2) proliferation of MTL species would facilitate the creation of an "omnivore niche" resulting in significant loss of LTL species including planktivorous The removal of MTL species would cause: (B1) decline in HTL species owing to absence of prey (Pauly et al. 1998); (B2) proliferation of LTL species due to decreased predation pressure (Pauly et al. 1998); (B3) suppression of plankton standing crop due to uncontrolled grazing.

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The removal of LTL species would: (C1) release predation pressure from phytoplankton causing extensive blooms; (C2) cause "bottom-up trophic cascade" i.e., reduction of MTL, and consequently HTL species, resulting in a diminished marine fish community.
Alterations in trophic structure of marine communities would be greatly influenced by the geographical and bathymetric setting of that ecosystem.In an open ocean environment with a stratified water column, the regenerated nutrients are not transported to the subsurface waters owing to a strong pycnocline, indicating absence of benthicpelagic coupling.Moreover, in the absence of an external nutrient source, the subsurface waters become oligotrophic.In such an event, ephemeral small sized cells dominate the phytoplankton community, and the phytoplankton biomass so generated is inadequate to sustain primary pro-  ductivity (Kiørboe 2008).Simultaneously, anoxic or hypoxic conditions in the bottom waters would induce anaerobic catabolism of the organic matter accumulated at the sediment-water interface.Additionally, low dissolved oxygen concentrations would interfere with the physiological processes of the benthic faunal communities either causing mortality or forcing emigration.On the other hand, in coastal waters with well-mixed water column prone to cyclonic wind circulation, the regenerated nutrients in the bottom waters would be transported to the subsurface waters, indicating prevalence of benthic-pelagic coupling.Moreover, nutrient loading from terrestrial sources would render these waters eutrophic, and the phytoplankton com-munity may become dominated by long-lived large sized cells (Kiørboe 2008).Simultaneously, well-oxygenated bottom waters would support myriad communities of benthic fishes and invertebrates.
In view of the above hypothesis, it is noteworthy that the major bulk of the Southeast Asian demersal marine fisheries are restricted to the shallow coastal waters, whereas both coastal and deeper water fisheries exploit pelagic species.However, demersal deep-sea fisheries of the individual countries are evolving rapidly (Saharuddin 1995;Flores 2004;Morgan and Staples 2006).
A significant reduction in LTL species production by Thailand along with marginal reduction in MTL and HTL

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Table 4. Years of peak production of fishery groups (or species) exploited by four Southeast Asian countries (which were followed by decline in production) over the period 1996-2007.species production partially suggested the occurrence of a partial "top down" trophic cascade effect (involving A1, A2, A3).This effect was attributed to multiple factors, but primarily due to the long-term negative effects of large scale bottom trawling in the Gulf of Thailand and Andaman Sea since the 1960's.Secondly, the decline in catches of mangrove crabs, penaeid and non-penaeid prawns as well as myriad trash fish species after 1996-1998 was attributed to large scale mariculture and urbanization that destroyed some of the vital mangrove habitats.Thirdly, the massive coral bleaching event of 1998 probably caused a gradual decline in HTL reef fishes (Table 4).Further, anthropogenic nutrient enrichment of the coastal waters of Gulf of Thailand resulted in frequent plankton blooms (Wattayakorn 2006).
In the case of Indonesia and Malaysia, the ecological implications of removal of considerable quantities of fish biomass across the trophic spectrum could not be explained explicitly.Increase in seafood production at all trophic levels roughly corresponded with increase in the size of the fishing fleets (particularly artisanal nonpowered boats and inboard powered mechanized vessels), and the geographical expansion of fishing grounds (Pauly 2013).Marine basins across Southeast Asia, with the exception of the Gulf of Thailand, were not exploited intensively to depletion levels prior to 1996, and many of their coral reefs, although at very high risk from anthropogenic disturbances, were in marginally better conditions (Burke et al. 2002).This probably explained why, despite the widespread coral bleaching event of 1998, the coral reefs could withstand fishing pressure, thereby returning marginally higher yields in terms of seafood production.Moreover, the increased use of artisanal fishing vessels might have minimized destruction of bottom reef structures.However, caution must be exercised while interpreting these trends as 71 and 85% of the demersal fisheries (including reef-associated species) of Indonesia and Malaysia, respectively were fully exploited and another 10% were overfished.Furthermore, production of a few HTL species declined strongly after 1998-1999 (Table 4) mostly due to the 1998 coral bleaching event.Another factor affecting the coastal marine habitats of the South China Sea was nutrient enrichment and sedimentation of coastal waters from domestic sewage and highly dense aquaculture farms (Wang et al. 2008).Circulation of these enriched waters was affected due to seasonal changes of winds and current patterns thus facilitating long distance transportation of HAB-causing species (Azanza et al. 2005).Therefore, it is conjectured that the marine basins exploited by these countries could be heading towards a "top down" trophic cascade effect (involving A1-5; see above).
In the Philippines, production of a few HTL species declined strongly after 1996 (Table 4) due to targeted exploitation and destructive fishing practices (Gomez et al. 1994).In addition, production of mangrove-associated crustaceans and molluscs declined after 1996 (Table 4) probably due to habitat loss.However, decline in their catches did not have any significant effect on the total seafood production trends during 1996-2007 largely due to maximized fishing effort coupled with geographical expansion of fishing areas.It is conjectured that continuous increase in fishing effort and use of destructive fishing techniques coupled with changes in land use pattern would potentially endanger most coastal ecosystems (Burke et al. 2002) and lead to a "top down" trophic cascade effect in the near future.A few manifestations of this ecological effect such as recurrent phytoplankton blooms (A3) were prevalent dur-ing this period, which frequently resulted in massive fish kills (Relox and Bajarias 2003;Azanza et al. 2005).
It is apparent from above that the marine living resources of Southeast Asia are afflicted by demand-driven overexploitation (Mamauag 2004;Ochavillo et al. 2004), and the consequences of ecosystem alteration (Burke et al. 2002).Intensive exploitation of coastal and offshore living resources throughout Southeast Asia has resulted in the overexploitation of most HTL and MTL species.Furthermore, unrestrained alterations of land-use pattern as well as coastal habitats to serve the increasing demands of the ever-growing demographic pressure have also caused immense damage to these ecosystems (Burke et al. 2002).In the light of this scenario, excessive anthropogenic sedimentation and eutrophication may cause hypoxic (or anoxic) conditions, thereby accelerating anaerobic decomposition and compelling HAB-forming species to switch to mixotrophic (combined phototrophy and heterotrophy) mode of nutrition (Burkholder et al. 2008).Moreover, in tropical waters, elevated temperature regimes intensify decomposition, but also stratify the water column as well as stimulate excessive planktonic growth (Hallegraeff 2010).The most apparent manifestations of these disturbances during the last few decades were the recurring HABs (Wang et al. 2008;Lim et al. 2012) those are responsible for large scale fish mortality (Relox and Bajarias 2003;Azanza et al. 2005), as well as potential hazards to the coastal human population (Backer and McGillicuddy 2006).
A rapidly changing global climate has intensified the El Niño phenomenon resulting in higher SST, altered monsoonal sequences, and increased rates of CO 2 dissolution those interfere with the biological processes of the symbiotic zooxanthellae, whose mortality has resulted in mass coral bleaching events (Reaser et al. 2000).Climate change also accelerates speciation and extinction of native fauna through changes in thermal (Sanciango et al. 2013) and pH regimes of the ambient ecosystems and creates opportunities for the establishment of resilient opportunistic (Mohamed et al. 2013) and invasive species (Occhipinti-Ambrogi 2007) that would further modify the trophic dynamics of the coastal habitats.

Figure 1 .
Figure 1.Map of Southeast Asia indicating the geographical extent of the study area.

Table 3 .
Catastrophic events in the coastal waters off four Southeast Asian countries during 1996-2007; abbreviations used: CB -Coral bleaching; HAB -Harmful Algal Bloom formation.