Impacts of pollution, sex, and tide on the time allocations to behaviours of Uca arcuata in mangroves

Highlights

• Uca act as ecosystem engineers in mangroves by foraging and burrowing activities.

• Ten behaviours of Uca arcuata were observed in the Futian Nature Reserve, China.

• Fiddler crabs spent the most time on feeding and feeding while walking.

• Nutrient pollution and sex are factors that influence crab behaviour.

• Foraging and burrowing activities decreased with increasing nutrients.

Abstract

Fiddler crabs (Uca) are ecosystem engineers in coastal ecosystems. Many anthropogenic and natural factors can affect the time allocated to various behaviours in Uca. However, the behaviour of U. arcuata, a widely distributed fiddler crab in Asia, has not been studied in mainland China. Here, we used binoculars to record the time budget of ten behaviours of U. arcuata to investigate the potential effects of sex, tides, and pollution on these behaviours. We found that the crabs spent 42.3%, 27.0%, and 10.6% of their time on feeding, feeding while walking, and stationary respectively. The crabs spent <1.5% of their time on copulation and grooming. The total foraging time (feeding + feeding while walking) did not differ among the three polluted sites. However, crabs spent more time on feeding but less time on feeding while walking. The feeding rate and probability of burrowing and grooming decreased while the possibility of locomotion and stay in burrow increased with increasing nutrient concentration. Females spent 13.9% more time on feeding and fed 54.9% faster than males. Males had a higher tendency to grooming and combat while they were less likely to walk than females. Regarding to the influence of tide, fiddler crabs fed 11.2% faster at ebb tides than at flood tides, and they were more likely to walk and stay in burrows at flood tides than at ebb tides. Our results indicated that nutrient pollution had stronger impacts on the behaviours of crabs than sex and tide. In polluted mangroves, increasing nutrient concentration reduced the quantity of sediment processed by fiddler crabs due to their smaller feeding area, slower feeding rate, and reduced frequency of burrowing activities. These results imply that mitigating nutrient pollution in mangroves may benefit the restoration and management of coastal ecosystems through the enhanced engineering functions of fiddler crabs.

Introduction

Mangroves are plants that grow at the interface between terrestrial and marine ecosystems in tropical/subtropical areas and can also expand into temperate coastal regions due to climate warming (Guo et al., 2013; Kathiresan and Bingham, 2001). Mangroves are among one of the most valuable and productive coastal ecosystems and are referred to as “Blue Forests”. They provide essential ecosystem services and functions to human beings, such as watershed protection, food production, and air quality improvement (Himes-Cornell et al., 2018; Vo et al., 2012). Mangroves are important for global carbon accounting, with an estimated total global mangrove aboveground biomass of 2.83 Pg (Hutchison et al., 2014). It is estimated that mangroves can support >70 direct human activities, and the general mean value provided by mangroves worldwide is 2000–9000 US$/ha/year (Kathiresan, 2012). However, mangrove forests are declining worldwide due to intensive anthropogenic activities such as deforestation, urbanization, and pollution (Thomas et al., 2017). Global mangroves disappear at a rate of 1–2% every year, which is equal to or even higher than the disappearance rates of coral reefs and tropical rainforests (Duke et al., 2007). The estimated global mangrove forest area has decreased by ~50% (Macintosh and Ashton, 2002). Ecological restoration is acknowledged as a powerful method of recovering the biodiversity, ecosystem functions and services of impaired mangroves. A study conducted in Brazil indicated that the herbivory and bioturbation (e.g., burrowing) effects of crabs aided in forest restoration by increasing aboveground carbon stocks and biomass (Ferreira et al., 2019). In another study conducted in a restored Florida coastal marsh, the presence of fiddler crabs enhanced the typically poor sediment quality in restored mangroves through burrowing activities, resulting in positive effects on mangrove height, leaf production, and trunk diameter (Smith et al., 2009). Therefore, the study of burrowing crabs such as fiddler crabs that can have ecological engineering impacts on mangroves is promising for advancing our knowledge of how to better manage and restore these degraded coastal ecosystems.

Crabs are among the most important groups of epifauna in mangroves (Ngo-Massou et al., 2018). Crabs of the genus Uca are characterized by their strong sexual dimorphism; males have one greatly enlarged cheliped (Crane, 2015). Approximately 100 species of Uca have been investigated in terms of their ethology, population ecology, and physiology (Jiang et al., 2016; Nabout et al., 2010; Zhang et al., 2019). Fiddler crabs are recognized as ecosystem engineers due to their bioturbation activities, such as feeding activities and burrow construction (Penha-Lopes et al., 2009). In a mesocosm experiment, the daily dry weight of sediments processed by an active fiddler crab in a pristine environment was 13 g and 17–20 g for feeding and burrowing activities, respectively (Penha-Lopes et al., 2009; Zhang et al., 2010). In a review paper that focused on the engineering impacts of mangrove crabs on sediment processes, Kristensen (2008) illustrated three features of the engineering effects of fiddler crabs on biogeochemical activity and heterogeneity in sediment environments: (1) alteration of physical structures (e.g., burrows); (2) physical transport (e.g., material, fluid, and gas); and (3) changes in the chemical properties of substances (e.g., degradability and redox conditions). These bioturbation activities can benefit coastal ecosystems by stimulating the growth and production of plants (Smith et al., 2009) and controlling bacterial communities to increase ecological resilience (Booth et al., 2019). These effects are closely linked to the time that fiddler crabs allocate to foraging, burrowing, and other behaviours.

The behaviour of fiddler crabs and their time allocations to behaviours can be affected by many biotic and abiotic factors, such as sex, body size, tidal and daily rhythms, and pollution (Darnell et al., 2019). For example, fiddler crabs spent less time foraging in polluted sites than in nonpolluted sites due to the increased food resources (e.g., microphytobenthos); the crabs spent more time on other activities, such as courtship and territorial defence (Bartolini et al., 2009; Li et al., 2015a). Another study found that male and female crabs with smaller body sizes fed faster than larger ones, and the larger the feeding claw, the faster the feeding rate per feeding claw (Tina et al., 2015). Kim et al. (2004) found that male fiddler crabs spend most of their time feeding during spring tides and spend more time on courtship during neap tides. Clark and Backwell (2017) found that a new heterospecific neighbour fights at a higher frequency with resident crabs, but these fights are shorter than those between a resident and a new conspecific male. Although fiddler crabs have been studied in many of their natural distribution areas, the study of fiddler crabs in mainland China is almost non-existent. Most of the fiddler crab studies have been conducted in Hong Kong and Taiwan and were related to crab distribution, diversity, and burrow morphology (Li et al., 2018; Shih et al., 2010; Shih et al., 2012). The study of fiddler crabs in mainland China may help advance the protection and restoration of mangroves in China.

By investigating ten behaviours of the fiddler crab U. arcuata in three polluted sites (differing in nutrient conditions) in the Futian Nature Reserve, China, we aimed to test the effects of pollution, sex, and tide on the time budget of crabs for 10 behaviours. We hypothesized that (1) fiddler crabs would spend most of their time on foraging activities; (2) females would feed faster than males, probably because females have two feeding chelipeds, while males only have one, and males would spend less time foraging while spending more time on social activities (e.g., combat) than females; (3) fiddler crabs would spend less time foraging in polluted sites; and (4) crabs would spend more time feeding at ebb tides than at flood tides because when the crabs emerge from their burrows after the seawater retreats (i.e., ebb tide), feeding to satisfy their energy requirements is their first priority.