The final spawning ground of Tachypleus gigas (Müller, 1785) on the east Peninsular Malaysia is at risk: a call for action Bryan Raveen Nelson1,2, Behara Satyanarayana3,4,5, Julia Hwei Zhong Moh1, Mhd Ikhwanuddin1, Anil Chatterji6 and Faizah Shaharom7 1 Institute of Tropical Aquaculture (AKUATROP), Universiti Malaysia Terengganu—UMT, Kuala Terengganu, Terengganu, Malaysia 2 Horseshoe Crab Research Group (HCRG), Universiti Malaysia Terengganu—UMT, Kuala Terengganu, Terengganu, Malaysia 3 Mangrove Research Unit (MARU), Universiti Malaysia Terengganu—UMT, Institute of Oceanography and Environment (INOS), Kuala Terengganu, Malaysia 4 Laboratory of Systems Ecology and Resource Management, Université Libre de Bruxelles—ULB, Brussels, Belgium 5 Laboratory of Plant Biology and Nature Management, Vrije Universiteit Brussel—VUB, Brussels, Belgium 6 Biological Oceanography Division, National Institute of Oceanography (NIO), Goa, India 7 Institute of Kenyir Research (IPK), Universiti Malaysia Terengganu—UMT, Kuala Terengganu, Terengganu, Malaysia ABSTRACT Tanjung Selongor and Pantai Balok (State Pahang) are the only two places known for spawning activity of the Malaysian horseshoe crab - Tachypleus gigas (Müller, 1785) on the east coast of Peninsular Malaysia. While the former beach has been disturbed by several anthropogenic activities that ultimately brought an end to the spawning activity of T. gigas, the status of the latter remains uncertain. In the present study, the spawning behavior of T. gigas at Pantai Balok (Sites I-III) was observed over a period of thirty six months, in three phases, between 2009 and 2013. Every year, the crab's nesting Submitted 20 March 2016 activity was found to be high during Southwest monsoon (May–September) followed Accepted 17 June 2016 Published 19 July 2016 by Northeast (November–March) and Inter monsoon (April and October) periods. In the meantime, the number of female T. gigas in 2009–2010 (Phase-1) was higher Corresponding authors Bryan Raveen Nelson, (38 crabs) than in 2010–2011 (Phase-2: 7 crabs) and 2012–2013 (Phase-3: 9 crabs) for [email protected] which both increased overexploitation (for edible and fishmeal preparations) as well as Behara Satyanarayana, anthropogenic disturbances in the vicinity (sand mining since 2009, land reclamation [email protected] for wave breaker/parking lot constructions in 2011 and fishing jetty construction in Academic editor 2013) are responsible. In this context, the physical infrastructure developments have María Ángeles Esteban altered the sediment close to nesting sites to be dominated by fine sand (2:5X' ) with Additional Information and moderately-well sorted (0.6–0.7σ '), very-coarse skewed (−2:4SK '), and extremely Declarations can be found on page 25 leptokurtic (12:6K ') properties. Also, increased concentrations of Cadmium (from 4.2 to 13.6 mg kg−1) and Selenium (from 11.5 to 23.3 mg kg−1) in the sediment, and DOI 10.7717/peerj.2232 Sulphide (from 21 to 28 mg l−1) in the water were observed. In relation to the monsoonal Copyright changes affecting sheltered beach topography and sediment flux, the spawning crabs 2016 Nelson et al. have shown a seasonal nest shifting behaviour in-between Sites I-III during 2009–2011. Distributed under However, in 2012–2013, the crabs were mostly restricted to the areas (i.e., Sites I and Creative Commons CC-BY 4.0 II) with high oxygen (5.5–8.0 mg l−1) and moisture depth (6.2–10.2 cm). In view of the OPEN ACCESS How to cite this article Nelson et al. (2016), The final spawning ground of Tachypleus gigas (Müller, 1785) on the east Peninsular Malaysia is at risk: a call for action. PeerJ 4:e2232; DOI 10.7717/peerj.2232 sustained anthropogenic pressure on the coastal habitats on one hand and decreasing horseshoe crabs population on the other, it is crucial to implement both conservation and management measures for T. gigas at Pantai Balok. Failing that may lead to the loss of this final spawning ground on the east coast of P. Malaysia. Subjects Aquaculture, Fisheries and Fish Science, Conservation Biology, Marine Biology Keywords Anthropogenic disturbance, Conservation and management, Living fossil, Monsoonal impact, Nest shifting behaviour, Seasonal nesting INTRODUCTION The surviving horseshoe crab species, three Asian—Tachypleus gigas (Müller, 1785), Tachypleus tridentatus (Leach, 1819), Carcinoscorpius rotundicauda (Latreille, 1802), and one American—Limulus polyphemus (Linnaeus, 1758) persist from the Ordovician period (Rudkin & Young, 2009). Its body with armour-like carapace, degener- ated spines (adult), appendages with setae, spine-like telson, etc., shows their prehistoric appearance clearly (Walls, Berskson & Smith, 2002; Ruppert, Fox & Barnes, 2004; Smith, Millard & Carmichael, 2009). Of the four species, only C. rotundicauda breeds in the muddy areas near mangroves while the rest spawn along the intertidal beaches of the estuarine coasts (Cartwright-Taylor et al., 2011; Nelson et al., 2015). The selective nesting behaviour of the crabs is usually facilitated by appendage setae (chemoreceptors) which can sense and detect suitable sandy/muddy substratum for their egg incubation and hatching (Botton, 2009). Horseshoe crabs are encountered only when they come ashore to shallow and surf- protected beaches for nesting. A male crab attached to the rear end of a female crab (using their pedipalps) is distinguished as one mating pair or amplex (Brockmann, 2003; Duffy et al., 2006; Brockmann & Smith, 2009). In addition, satellite males - single and available close to the amplexed pairs to fertilize their eggs and, solitary females - if they are alone, are also visible on the beaches (Mattei et al., 2010; Nelson et al., 2015). A female crab is capable of laying 200–300 eggs (Chatterji & Abidi, 1993) in varying depths (10–20 cm) below the sand (Botton, Tankersley & Lovel, 2010). However, its spawning activity is largely governed by season and local environmental (sediment and water) conditions (Smith, 2007; Weber & Carter, 2009). Despite the increased scientific attention on the horseshoe crabs globally (Smith, Millard & Carmichael, 2009; Chatterji & Shaharom, 2009; Mattei et al., 2010; Cartwright-Taylor et al., 2011; Srijaya et al., 2014), their population is consistently decreasing over the years due to natural (e.g., coastal erosion) as well as anthropogenic disturbances (e.g., pollution, overexploitation, etc.) (Jackson, Nordstrom & Smith, 2005; Ngy et al., 2007; Faurby et al., 2010; Nelson et al., 2015). In addition, the delayed maturity (between 9 and 11 years) and longer embryogenesis period (up to 42 days) (Coursey et al., 2003; Chabot & Watson, 2010) are making these crabs vulnerable to recent changes in the coastal environments (Botton et al., 2006; Chatterji & Shaharom, 2009; Nelson et al., 2015). In fact, Nelson et al. (2016), PeerJ, DOI 10.7717/peerj.2232 2/32 L. polyphemus is recognised as `near threatened' species, while the remaining three Asian horseshoe crabs are under ``data deficient'' category in the IUCN red list (IUCN , 2016). In Malaysia, all three Asian horseshoe crabs are available. While T. gigas and C. rotundicauda are present in the coastal areas of Peninsular Malaysia, the distribution of T. tridentatus is restricted to East Malaysia (i.e., Sabah and Sarawak) (Chatterji et al., 2008). Although several researchers in P. Malaysia have worked on T. gigas, most of their findings are based on short-term investigations (e.g., Zaleha et al., 2010; John et al., 2011; Kamaruzzaman et al., 2011; Tan, Christianus & Satar, 2011; John, Jalal & Kamaruzzaman, 2013). The only long-term (2009–2011) study that examined the nesting behaviour of T. gigas was carried out by Nelson et al. (2015) from Tanjung Selongor. In fact, Tanjung Selongor and Pantai Balok (in State Pahang) are the only two places known for T. gigas spawning on the east coast of P. Malaysia. According to Nelson et al. (2015), the physical infrastructural developments such as jetty and road/bridge constructions at Tanjung Selongor have already brought an end to the spawning activity of T. gigas. In the case of Pantai Balok, Zaleha et al. (2012), Tan et al. (2012), and John et al. (2012) have observed the spawning populations and nesting behaviour of T. gigas, but for different months in 2009–2010 with no seasonal cross-checking. Therefore, an assessment on the seasonal impact as well as state-of-the-art information on T. gigas is necessary and still to be ascertained from Pantai Balok. The present study was aimed at investigating the relationship between the nesting activity of T. gigas and the environmental (water/sediment) conditions noticed at Pantai Balok. In specific, identification of major environmental factors predisposed by lunar and monsoonal changes that support T. gigas spawning formed the main forte of this study. In recent years, several anthropogenic activities such as sand mining (2009 - to present), land reclamation (2011), and construction of a fishing jetty (2013) also appeared to influence T. gigas population. At the end, a few recommendations were offered for possible conservation and management of T. gigas at Pantai Balok. MATERIALS AND METHODS Study area We recall that Pantai Balok, in State Pahang, is one of the two spawning grounds for T. gigas on the east coast of P. Malaysia (Lat: 3◦56016.5800-3◦55039.3300N; Long: 103◦22032.7400- 103◦22027.1200E) (Fig. 1A). River Balok and its tributaries opens here into South China Sea and provide a regular exchange of water (Fig. 1B). The climate of Pantai Balok is influenced by Northeast (NE) (November–March) and Southwest (SW) monsoons (May– September), separated by two Inter-monsoon (IM) periods (April and October). The weather—with a temperature varying between 20 and 36 ◦C, is generally hot and humid (WU , 2014). The annual (average) rainfall is about 1710.5 mm and occurs mostly during September-December. The tides with a range of 0.1–3.4 m are mixed in nature (NHC, 2013). Pantai Balok is under sustained human intervention over the last few decades. In addition to the sand mining since 2009 (Fig.