Population scarcity of an estuarine crab (Chiromantes dehaani) caused by intertidal reclamation from the perspective of reduced salinity

https://doi.org/10.1016/j.rsma.2020.101386Get rights and content

Highlights

  • Why C. dehaani population scarcity occurs in reclaimed wetlands is unclear.

  • All C. dehaani disappeared in fully-enclosed area with zero salinity.

  • No crabs died directly from osmotic stress caused by freshwater exposure.

  • Reproduction barriers were a key factor causing the scarcity of crab population.

Abstract

Decreased salinity is one of the main abiotic factors causing macrobenthic degradation in reclaimed intertidal wetlands. However, our knowledge of the mechanism(s) underpinning this degradation remains surprisingly scanty. To fill this gap, here we used the crab Chiromantes dehaani as a study subject. First, we investigated differences between C. dehaani populations in fully- and semi-enclosed wetlands in 2018. Then, in controlled experiments, we exposed female C. dehaani to freshwater (salinity of 0) and two salinity levels (3 and 12) for 12, 24, and 48 days to explore the effects of reduced salinity on the osmoregulation and lipid materials of C. dehaani. Then, the surviving crabs mated with mature male crabs, and the spawning rate, fecundity, and abortion rate of female crabs quantified to reveal the effects of lower salinity on reproduction in this species. Our results revealed that no crabs could be found in the fully-enclosed zone, where the salinity level closely matched that of freshwater. In controlled experiments, the C. dehaani showed the ability of osmoregulation under freshwater condition, but it consumed more lipid materials to maintain stable osmotic pressure. Moreover, the ovary development of C. dehaani was significantly inhibited in the freshwater group, which resulted in no spawning crabs. In contrast, the breeding success of female crabs in salinities of 3 and 12 reached 90.5 ± 4.8% and 79.4 ± 6.9%, respectively. The abortion rate of embryos increased significantly after spawning crabs were exposed to the freshwater environment. Collectively, the reproduction barriers caused by salinity’s decrease may be a critical causal factor driving the scarcity of C. dehaani population in reclaimed wetlands of Yangtze estuary. These findings are expected to provide new insights into the effects of reclamation on macrobenthos.

Introduction

In recent decades, many coastal cities have had to address the pressing problem of sustaining an increasing human population with limited land resources. Wetland reclamation is widely considered as providing an effective way to solve this problem of land shortage. However, such reclamation may interfere with ecosystems processes and undermine the ecological integrity of intertidal wetlands (Yim et al., 2018). On a global scale, intertidal wetlands, namely 50% of salt marshes, 35% of mangroves, 30% of coral reefs, and 29% of seagrasses, have been heavily degraded or lost entirely due to reclamation projects and other human activities (Barbier et al., 2011). Moreover, reclamation activities may weaken or impair the ecological functions and services that intertidal wetlands provide for many aquatic animals and migrating birds.

Macrobenthos are major secondary producers in intertidal wetlands (Lv et al., 2018). Due to their sedentary life history and high environmental sensitivity, macrobenthos are considered as potentially powerful bio-indicators for the reliable monitoring of environmental change (Zhou et al., 2019, Vassallo et al., 2020). Previous studies have shown that reclamation projects may cause species loss and community degradation of macrobenthos, because of the changes of abiotic (elevation, sediment characteristics and water salinity) and biotic (vegetation) factors (Yuan and Lu, 2001, Yang et al., 2018). However, the knowledge on why this community degradation occurs is rather sparse, because too few studies have investigated the altered physiological traits of macrobenthos caused by environmental changes that occur when wetlands are reclaimed.

According to many researchers, reduced water salinity is a major environmental characteristic that is affected after wetlands are enclosed by seawalls (Lv et al., 2016, Matsuda and Kokubu, 2016, Liu et al., 2018). The irregular change of water salinity may significantly disturb the growth and reproductive performance of macrobenthos, because water salinity is usually characterized by interannual periodic changes in estuarine area, due to the complex interaction between freshwater flow and tidal currents (Chen et al., 2012, Hu et al., 2014). Macrobenthos usually complete their life cycle in the process of water salinity changes. In the laboratory, much research suggests that osmoregulation (Romano and Zeng, 2006, Gomes et al., 2019, Lu et al., 2019), energy metabolism (Chen et al., 2014, Huang et al., 2019), gonadal development (Long et al., 2017), mating behavior (Wu et al., 2013, Ikhwanuddin et al., 2014) and embryonic development (Rotllant et al., 2015, Urzúa et al., 2018, Wang et al., 2019) of economically important macrobenthos are easily affected by changes to salinity.

Chiromantes dehaani is a typical crab that mainly lives in estuarine areas of East Asia. This crab has similar ecological importance to other intertidal crabs. Many studies have demonstrated that the bioturbation by crabs, e.g., ingestion and excretion, can promote biogeochemical cycling in wetlands (Thongtham et al., 2008, Chandler et al., 2015, Abdullah and Lee, 2016). Because it figures prominently in ecosystem dynamics, C. dehaani is often called an “ecosystem engineer” (Lee, 1998). Moreover, crabs and their larvae are one of the most important food resources for birds and fishes. In Yangtze estuary, C. dehaani is often used to indicate environmental degradation, because it is easy to collect and sensitive to environmental changes. Hence, to better understand the reasons behind the degradation of macrobenthic communities in reclaimed wetlands, it is pertinent to not only consider population-level changes but also how the growth and reproductive measures of C. dehaani are affected under different levels of water salinity.

In this study, we assessed the number of C. dehaani in two reclaimed wetlands of the Yangtze estuary to detect the effect of reclamation on C. dehaani populations. Then, in the laboratory, we simulated the changes in water salinity characterizing reclaimed wetlands and measured the concentrations of Na+ and K+ in the hemolymph and the activity of Na+/K+ ATPase (NKA) in the gills of C. dehaani. We also analyzed the levels of triglyceride (TG) and total cholesterol (TCHO) in hemolymph, as well as lipid contents in the ovary and hepatopancreas. Going further, we examined the impact of different salinity levels on the crab’s reproductive metrics, including gonadal development and embryonic development. The primary objective of this study was to detect the mechanism(s) of salinity decrease in reclaimed wetlands on the C. dehaani population.

Section snippets

Experiment 1

In experiment 1, we compared the water salinity and number and weight of C. dehaani between a fully-enclosed wetland (i.e., east shoal of Hengsha Island) and semi-enclosed wetland (i.e., the east shoal of Chongming Island).

The east shoal of Hengsha Island was fully enclosed from the sea by dikes in 2012. Thus, natural seawater cannot enter into its enclosed area. The vegetation types here include Phragmites australis, Scirpus mariqueter, as well as emerging terrestrial vegetation. The east

Results

Effects of reduced salinity on C. dehaani population in reclaimed wetlands

In this investigation, the fully-enclosed wetland in the Yangtze estuary had an extremely low level of water salinity (0.2–0.5)in its reclaimed zone in which no C. dehaani crabs were found. By contrast, the crab’s number and weight were similar between reclaimed and natural zones in the semi-enclosed wetland. Moreover, we found a significant positive correlation between the number of C. dehaani and water salinity. These above results suggest reduced salinity may cause the decrement or

Conclusion

Our comprehensive study used both field and laboratory data to explore the reasons for the scarcity of C. dehaani population under lowered salinity conditions in reclaimed wetlands. In the investigation, no crabs were found in the fully-enclosed wetland, which had an extremely low water salinity (0.2–0.5).​ Female C. dehaani were exposed to freshwater and salinity conditions in a laboratory setting. Results showed that the crabs possessed the ability of hypertonic regulation in a freshwater

CRediT authorship contribution statement

Weiwei Lv: Writing - original draft, Methodology, Software. Qiang Chen: Data curation. Quan Yuan: Visualization, Investigation. Wenzong Zhou: Supervision. Yunlong Zhao: Conceptualization, Validation, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This study was supported by the Shanghai Municipal Science and Technology Commission, China [grant number 19ZR1436900]; and the SAAS Program for Excellent Research Team, China [nong ke chuang 2017 (A-03)].

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