Effects of rubble zones from oyster cultivation on habitat utilization and foraging behaviour of the endangered tri-spine horseshoe crab: An implication for intertidal oyster cultivation practices

Highlights

• Horseshoe crabs are ecologically significant in coastal and estuarine ecosystems.

• Intertidal oyster rubbles affected foraging behaviour of juvenile horseshoe crabs.

• Laboratory studies confirmed the localized effects of physical structure additions.

• On-bottom oyster culture not recommended on nursery habitats of horseshoe crabs.

Abstract

Estuarine structured habitats, including benthic cultivation structure, are widely cited as substantial nursery and feeding grounds for fish and macroinvertebrates. Activities such as locomotion and foraging behaviour of sediment-dwelling species, however, may be hindered in the presence of the obstacles. In this study, collected field evidence demonstrated that habitat utilization of the juvenile tri-spine horseshoe crab Tachypleus tridentatus, an iconic and endangered macroinvertebrate, was adversely affected by high-density intertidal oyster rubble zones. Despite the fact that the utilization area of individual juvenile horseshoe crabs was independent of the presence of these obstacles, the abundance and number of positional fixes of tagged juveniles in these areas were lower. The effects of these obstacles and their associated topographic changes on the movement of the juvenile horseshoe crabs was investigated in a simulated laboratory experiment. Both the simulated oyster cultches and hummocks formed between the cultches reduced the total distance and displacement of the feeding trail, and less juveniles preferred to forage on elevated, dry hummocks (dry at low tide) formed between the cultches. Our findings suggested that oyster cultches and rubbles reduced the habitat quality for juvenile horseshoe crabs. On-bottom oyster cultivation activities seeking to conserve horseshoe cabs by avoiding nursery habitats should instead consider off-bottom or offshore cultivation methods.

Introduction

In the past three decades, the global aquaculture production of marine and brackish species increased at an average rate of 8% per annum, partly driven by the need for food security (FAO, 2012). Mariculture production worldwide has consistently been dominated by mollusks, primarily bivalves since 1970, which account for more than 70% by weight (Campbell and Pauly, 2013). In terms of geographic distribution, China is responsible for 85% of the global production of marine bivalves, primarily Pacific oyster Crassostrea gigas (Wijsman et al., 2019).

Oyster farming in intertidal and subtidal zones employs various techniques ranging from on-bottom (i.e., laying rock, concrete tile or post) to off-bottom (i.e., using rack, longline or mesh bag) culture methods. Collecting spat by laying concrete tiles, poles or rocks on intertidal areas has been practicing worldwide since the 1970s (Nell, 1993; Joseph, 1998; Nair, 2001; Taylor and Bushek, 2008; Robert et al., 2013; Mao et al., 2019). In China, the on-bottom culture produced more than five million tons of shellfish that accounted for one-third of the total production in 2015 (Mao et al., 2019). The addition of farming infrastructure on the seabed may result in localized changes in sediment topography (Everett et al., 1995; Kwan et al., 2018a), grain size, organic content, redox potential (Mitchell, 2006; Forrest and Creese, 2006), and/or associated infaunal assemblages (Castel et al., 1989; Nugues et al., 1996; Spencer et al., 1997). A number of studies have demonstrated a decrease in the abundance of macrofauna (Castel et al., 1989; Heral et al., 1986; Simenstad and Fresh, 1995) and seagrass (Bulmer et al., 2012) in extensive intertidal oyster farms. Disturbance caused by farming activities such as walking personnel and vessel movement between cultivation structures (De Grave et al., 1998), as well as shell rubbles and other farm debris (Escapa et al., 2004; Kwan et al., 2018a) also have profound influences on benthic habitats beneath cultivation sites. Since oyster cultivation can occupy a large portion of the intertidal area, the associated physical structures and activities may decrease the habitat quality for spawning, nursery and foraging of resident species (Davidson and Rothwell, 1993; Kwan et al., 2018a) as well as wading birds (Davidson and Rothwell, 1993). These structures, however, can provide fish and macroinvertebrates refuges from predation (Moksnes et al., 1998) and potential food sources from farmed shellfish (Bowling, 1994) and organisms associated with the structures (Seaman, 2000; Brickhill et al., 2005; Nielsen et al., 2016).

Asian horseshoe crabs are the iconic and ecologically important macroinvertebrates in coastal and estuarine ecosystems along the west coast of Pacific Ocean (Chen et al., 2004; Kwan et al., 2018b). Among the three extant species in Asia, the tri-spine horseshoe crab, T. tridentatus, was classified recently as an endangered species under the IUCN Red List (Laurie et al., 2019). Adult horseshoe crabs live on the seabed but migrate to intertidal flats and spawn during summertime. The juveniles inhabit intertidal areas for approximately nine years or longer before reaching sexual maturity (Sekiguchi, 1988; Hu et al., 2009, 2015). Their slow-growing life-history characteristics render them vulnerable to habitat loss and degradation (Chen et al., 2015; Nelson et al., 2016). Juvenile horseshoe crabs burrow in the sediment on the rising tide to protect them from predator such as rays and other fishes (Mikkelsen, 1988). When the tide is receding, they emerge and forage on the sand surface with a layer of water embracing the underlying vulnerable body to reduce body temperature and for gaseous exchange (Rudloe, 1981; Chiu and Morton, 2004), leaving behind a characteristic feeding trail. During foraging, they intermittently stop crawling at the front of their track, possibly because they encounter an appropriate prey and are feeding (Chiu and Morton, 2004). The preferred prey include bivalves, insect larvae, crustaceans and polychaetes (Zhou and Morton, 2004; Kwan et al., 2015b). Several reports have recorded the occurrence of horseshoe crabs near the intertidal oyster beds (SCMP , 1998; Morton and Lee, 2010; Lee and Morton, 2016; Yao, 2018). The spatial interaction between the on-bottom oyster cultivation structure and foraging behaviour of juvenile horseshoe crabs, therefore, raises considerable research interest for management and conservation purposes. In a field manipulation experiment using bricks to simulate oyster cultches, Kwan et al. (2018a) showed that the population density of juvenile horseshoe crabs reduced and the distance and displacement of foraging trails were shorter in the area with bricks.

In the present study, we quantified habitat utilization by T. tridentatus on the Hai Pak Nai mudflat, a critical nursery habitat which overlaps with the on-bottom oyster cultivation area. This habitat is the most important nursery ground of T. tridentatus, housing more than half of the juveniles found in Hong Kong (Kwan et al., 2016). Our study addressed the following questions: (1) What is the impact of oyster rubble zones generated from oyster culture activities on nursery habitat use of T. tridentatus? (2) How do the associated changes in sediment topography affect their foraging behaviour? The recommendations derived from this study may be beneficial to the development of environmental and ecologically sound management for the intertidal oyster farming industry.