4.1 Universal subtraits exhibited by macrobenthic communities in Johor Straits
SIMPER analyses toward three major macrobenthic groups (POL, BIV, MIX) identified burrower, upward-downward conveyor and vermiform as universal subtraits, i.e. available in all stations regardless taxa composition. Burrowers and upward-downward conveyor traits are common in most if not all, macrobenthic taxa. These traits are very prevalent in annelids, echinoderms, mollusks and sipunculids but not limited to arthropods too (Bremner et al. 2006; Huang et al. 2012; Tullos et al. 2009; Kasihmuddin & Cob 2021b). Vermiform subtrait is exclusive to worm-shaped benthic groups, namely annelids and sipunculids (Fauchald 1977; Buruaem et al. 2015; Faulwetter et al. 2014). This subtrait became extremely significant all due to highest individual counts of annelids in this stations, and readily available in all but stations J5 to J9 in the strait. These three subtraits are essential for most macrobenthic taxa, especially polychaetes, as these taxa fully rely on resources in sediment to thrive and survive. Macrobenthos exhibiting these subtraits would burrow downwards and traverse between sediment particles to obtain food particles (Kristensen et al. 2012; van der Meer 2017). These subtraits are deemed very universal, what actually differed POL, BIV and MIX groups was merely the percentage differences of these three subtraits rather than other subtraits assessed this study.
Meanwhile, POL (J1, J3, and J4) and BIV (J2) communities are differentiated by SIMPER analysis through interstitial and filter feeder subtraits, respectively. Interstitial subtrait is exhibited by Sedentaria polychaetes, but more prevalent from Families Capitellidae, Cirratulidae and Spionidae, which were mostly found in these locations (Cho et al. 2013; Gholizadeh et al. 2015; Dauvin et al. 2018). On the other hand, filter feeder subtrait is exhibited by various arthropods and mollusks in this study, but more prevalent in J2 due to larger presence of Asian Date Mussels (Arcualuta sp.) in the area. Higher abundance of these taxa are what made POL and BIV groups significantly different to each other. This was otherwise different in MIX group, where myriads of subtraits assessed in this region were identified owing to diverse phyla group thriving in this region.
4.2 Driving environmental factors behind spatial variation of macrobenthic ecological functioning in Johor Straits.
BIOENV identified pH level, Chl-a, clay sediment and TOC as main environmental factors behind spatial subtrait variation in this study. Stations in central region, namely J3 and J4, contained higher levels of organic carbon and clay sediments, and consequently also recorded very high counts of Sedentaria polychaetes from Family Capitellidae, Cirratulidae and Spionidae. The advent of Sedentaria polychaetes in conjunction to noticeably increasing organic carbon and clay sediments were previously observed in Northern England’s dredging areas (Bolam et al. 2016) and China’s Bohai Sea (Rui et al. 2021), both of which were notable for environmental degradation concerns due to massive reclamation activities occurring in the regions. Large presence of these polychaete families in these regions corresponded to higher percentages of subtraits related to these groups, namely vermiform, interstitial, surface deposit feeder, asexual, direct development and upward-downward conveyors (Kristensen et al. 2012; Faulwetter et al. 2014; Kasihmuddin & Cob 2021b). Carvalho et al. (2013) and Rehitha et al. (2017) reported a distinct correlation between dominant Sedentaria subtraits in coastal waters owing to higher percentages of smaller-sized sediment particles. These subtraits enable Sedentaria polychaetes to not only thrive easily in TOC-rich sediments, but even assist in increasing the carbon enrichment rate in sediments via upward-downward conveyor subtraits (Kristensen et al. 2012; Dai et al. 2015; Bolam et al. 2016).
Higher pH levels and Chl-a in BIV group (J2) and MIX group (J10 to J13) were marked with greater multitude of macrobenthic subtraits recorded in these stations. Many of these subtraits, notably epifauna, were found on these stations rather than in POL group, contributed by amphipods, bivalves, Errantian polychaetes, brittle stars and assortment of minor benthic groups such as octopus, hermit crab and lamp shell in the area. Water acidity and chlorophyll-a are linked to one another; higher chlorophyll-a in water is attributed to higher presence of phytoplankton, by which the said plankton requires slightly higher pH (7.50) in water in order to photosynthesize properly (Scholz 2014). Higher concentration of Chl-a in water indicates higher presence of phytoplankton in water, thereby promotes better foraging spots for macrobenthos with grazer subtrait such as Cymadusa amphipod, Arenicola polychaete and Cerithium snail, which then be consumed by macrobenthos with predator subtrait such as Diogenes hermit crab, Histoctopus octopus and Glycera polychaete. This leads to variation of phyla in the area, and hence promote to varied subtraits to prevail in these regions (Hale et al. 2011). Otherwise, lower pH in water attributes highly toward smaller-sized macrobenthos rather than larger ones. Acidified water may render exoskeletal integrity and several life processes difficult for most benthic phyla, making the environment unsuitable for all but annelids to thrive, (Verissimo et al. 2012; Tripole et al. 2018).
4.3 Overview of macrobenthic communities in Johor Straits with reference to dominant subtraits
The POL community is comprised of stations J1, J3, and J4. The taxa composition of these locations was dominated by smaller-sized (< 1 mm), incomplete parapodia and sedentary-lifestyle Sedentaria polychaetes (Fauchald 1977). Cirriformia, Mediomastus, Minuspio, and Prionospio are known Sedentaria polychaetes to possess these traits (Carvalho et al. 2013; Faulwetter et al. 2014; Hochstein et al. 2019). These four taxa were wholly abundant and major contributors to interstitial, vermiform, deposit feeder, burrower, asexual, and upward-downward conveyor subtraits in these regions. Although many of these subraits were found readily in all stations, they were rather found in higher percentages in these regions than the others. While the entire set of stations in this study indicated a lower FD index in reproductive strategy, it was otherwise for these stations. The four taxa mentioned earlier all reproduced asexually; hence, they contributed further to the asexual subtrait and thereby, increasing the category’s FD index (Gerwing et al. 2015). Among these communities, J1 has deeper water, higher silt counts and dissolved oxygen. Higher silt content in J1 was proportionate with higher Sedentaria polychaete counts, particularly Capitellids (Mediomastus) and Spionids (Minuspio and Prionospio). In J1, taxa contributors for polychaete-related subtraits were mostly not from the four taxa but those from other Sedentaria polychaetes such as Poecilochaetus and Sternaspis and Errantia polychaetes such as Micronepthys and Sigambra (Bremner et al. 2006; Bolam et al. 2016). Many Errantia polychaetes too exhibit similar polychaete subtraits as their Sedentarian counterparts, hence further contributing to the percentages (Kristensen et al. 2012; Quieros et al. 2013; Bolam et al. 2016; Rui et al. 2020; Kasihmuddin & Cob 2021b). Although J1 is considered a polychaete-dominated community, a higher oxygen level in the water but lower organic carbon in the sediment guarantees better survivability for non-polychaete taxa to thrive in the sediments, leading to notable percentages of non-polychaete subtraits in this station and a slightly higher FD index in almost all trait categories overall. This means that J1, despite being dominated by Sedentaria polychaetes, persisted with an almost similar environmental background as MIX communities, as evidently shown in the nMDS graph (Fig. 4). Meanwhile, J3 and J4 have higher organic carbon in sediment and higher turbidity in water, but lower depths and oxygen levels. Silt percentages in J3 were similar to those in J1, but sands were higher in J4 than silts. Similar to J1, non-polychaete taxa were present in J3, notably due to the location’s proximity to smaller mangrove enclaves off Skudai estuary, hence contributing to noticeable non-polychaete subtraits in J3, albeit the percentages were lower than J1. Capitellid, Cirratulid, and Spionid polychaetes dominate J3 and J4 en masse, with J4 consisting of nothing but just polychaetes. Lower oxygen levels in water, coupled with a lower pH but higher turbidity, altogether promote settlement for Sedentaria polychaetes but otherwise for other organisms (Zang et al. 2011; Villnäs et al. 2012). Levin et al. (2013) suggested that water mixing is vital for the macrobenthic community to thrive and survive. Unfortunately, the geographical barrier of the Causeway, coupled with the constant flux of dredged materials from mainland Malaysia, has rendered potential water mixing impossible, yet organic enrichment and other pollutants’ concentrations have increased tenfold over decades (Koh et al., 1991; Nordin & Ali, 2013; Maznah et al., 2016; Yap et al. 2021). This made the environment unsuitable for all but Sedentaria polychaetes, which seemingly are not only capable of surviving an ecologically stressed environment but even benefit from organic enrichment in sediment due to their interstitial, deposit feeding, asexual, direct development, and upward-downward conveyor subtraits (Selck et al. 2012; Carvalho et al. 2013; Kristensen et al. 2012; Faulwetter et al. 2014).
BIV community was comprised of only station J2, which was located within seagrass patches, close to Malaysia’s Merambong Island and Adang Cape, and Tuas industrial zone in Singapore (Wong et al. 2014; Cob et al. 2014; Guan et al. 2014). The higher presence of Arcuatula mussels in this region has led to increased percentages of bivalve-related subtraits such as globose body shape and filter feeding mode (Gosling 2021). Similar to the three Sedentaria polychaete families, this mussel also performs upward-downward conveyor as a bioturbation mode in sediment. In addition to dominating mussel numbers, other significant macrobenthic taxa present in the region included Histoctopus octopus, Acanthomysis mysid shrimp, and Arenicola polychaetes, many of which are common in seagrass ecosystems and share similar subtraits as the mussels, albeit only showing miniscule individual counts compared to the mussels. Akin to most known seagrass biotopes, organic carbon in J2’s sediment was very low, yet the level of Chl-a in the water was very high. Lower organic carbon in sediment was often associated with constant usage by seagrass’ roots in the vicinity, while higher Chl-a in water was associated with a higher number of phytoplankton in the water (Scholz 2014; Samper-Villareal et al., 2016; Alsaffar et al., 2020; Ashikin et al., 2020; Asha et al., 2021). Higher sand percentages in this area could be associated with heightened symbiotic activities between the bivalves and the seagrasses, where the bivalves readily perform the upward-downward conveyor as a bioturbation method, hence helping the seagrass’ root propagation and further increasing the sedimentation rate in the region (van der Heide et al. 2012; Schultz et al. 2015). The formation of seagrass networks eventually leads to increased oxygen levels via photosynthesis, which further benefits not only the bivalves but also other macrobenthic taxa (Dolbeth et al. 2013). Consequently, the resultant environment offers more viable foraging zones and better mobility for not only the bivalves but also larger-sized macrobenthos such as molluscs and arthropods (Cardini et al. 2019; Bedulli et al., 2020; Valdez et al., 2020). Previous records by Hadibarata et al. (2012), Wong et al. (2014), Guan et al. (2014), and Cob et al. (2014) all reported very diverse taxa compositions of macrobenthos in these regions. These numbers, however, may have become comparatively smaller due to the potentially greater loss of seagrass volumes affected by increased sedimentation activities in the nearby Forest City development (Hossain et al. 2019; Ashikin et al. 2020).
The MIX group, comprising stations J10 to J13, was located on the east side of the strait. The stations had no dominant macrobenthic groups and persisted in very diverse macrobenthic taxa. Taxa composition in J10 recorded the fewest macrobenthic individual counts in this study, of only five polychaetes, two amphipods, and one gastropod. Despite showing a higher Chl-a and dissolved oxygen level in water as well as higher clay contents in the sediment. Subtraits that are considered universal such as upward-downward conveyor, vermiform and interstitial were present in these locations, but in lesser percentages compared to POL community. As seen in J3 and J4, annelids, particularly Sedentaria polychaetes, prefer silt and sand contents for easier mobility and forage (Dauvin 2018; Hochstein et al. 2019; Shafie et al. 2021). Higher clay contents render most macrobenthic movements harder and hence unsuitable for settlement for most macrobenthic taxa, especially the non-polychaete ones (Bolam et al. 2016). Next, J11 to J13 altogether contained significant numbers of annelids, arthropods, echinoderms, and molluscs, with no dominant groups detected in these locations overall. Higher sand contents allow various larger-sized macrobenthos to settle and thrive due to the higher permeability of sand particles compared to silts and clay (Lv et al. 2018). Coupled with lower organic carbon and silt content but higher dissolved oxygen and chlorophyll-A, many macrobenthos that are not Sedentaria polychaetes can be easily found in this region, with each benthic group contributing specific subtraits that led to higher FD indices in almost all trait categories in this region. Unlike J2, which was dominated by bivalves, many of these taxa possess subtraits that reflect wider and more well-balanced food web structures. Variations of amphipods contributed to hyperbenthic, brooding, epifauna, and regenerator subtraits; Errantia polychaetes exhibited vermiform, endobenthic, upward-downward conveyors, deposit feeders, and crawlers; echinoderms’ ophiuroids showed scavenger, surficial modifier, and hermaphrodite subtraits; and finally, gastropods gave out globose and non-motile subtraits (Vickery et al. 2001; Bremner et al. 2006; Pagenelli et al. 2012; Quieros et al. 2013). Many of these taxa were previously recorded in the Santi estuary (Affendi et al., 2005), Tekong Island (Siang et al. 2012), and even throughout the entirety of the eastern side of the Johor Straits itself (Wan-Muda et al., 2013).
Despite presenting varied benthic groups, a concerning trend was noticed. While sand contents were higher, silt contents and organic carbon increased significantly from J11 to J13. Despite this, the percentages of subtraits related to Sedentaria polychaetes were miniscule, even in J13, where organic carbon was higher. Only Mediomastus polychaete was found in the sediments of J13, but the number was lower compared to those in J3 and J4. A subtrait related to Sedentaria polychaetes, namely surface and subsurface deposit feeders, was detected in this region, although the subtrait was also shared by other polychaete taxa in J13. While J11 and J12 are both situated close to regions with lesser anthropogenic traffic, J13 is located close to Pengelih Cape, where a massive land reclamation project is underway to make way for the development of the Pengerang Integrated Complex, or PIC (Brelsford 2016; Rezayee et al. 2020). The increasing reclamation activities highly reflected the increasing organic carbon and silt contents in sediment in J13. If this persists, increasing sediment content may restrict macrobenthic taxa movement and foraging activities (Egres et al. 2012; Ceia et al. 2013). Oxygen level and chlorophyll-a might decrease due to disruption of water mixing, worsening the situation by rendering the locations unsuitable for most macrobenthos to thrive, leading to a reduction of various benthic traits (Villnäs et al., 2012; Levin et al., 2013; Gerwing et al., 2015; Bolam et al., 2016). Conversely, with lesser macrobenthic taxa, smaller-sized Sedentaria polychaetes would settle unhindered, and in conjunction with heightened organic carbon percentages and silt contents from nearby reclamation activities, these polychaetes could utilize their traits to not only multiply faster but also further increase the organic enrichment process in the sediment under a lower oxygen environment, and only taxa that have traits similar to those of Sedentaria polychaetes could thrive (Linares et al. 2015; Dauvin 2018).