Widespread crab burrows enhance greenhouse gas emissions from coastal blue carbon ecosystems

You are undoubtedly familiar with the butterfly effect, where the flutter of a butterfly’s wings can ultimately alter the course of the wind…But have you ever wondered about the impact that a fiddler crab, waving its pincers, might have on greenhouse gases? 
​The fiddler crab, renowned as an ecological engineer of coastal wetlands, inhabits a vast majority of coastal ecosystems, excluding the polar regions. This intriguing creature exhibits a remarkable rhythm in its activities, intricately tied to the rise and fall of tides. During the high tide, they retreat to their burrows, while as the tide recedes, they emerge onto the tidal flats to forage, feed, and repair their burrows. Furthermore, their body hue undergoes a remarkable transformation in harmony with the diurnal cycle, lightening at nightfall and deepening into a more vivid shade during daylight hours. Studies have revealed that this exquisitely regulated daily pattern is orchestrated by an intricate biological clock, a testament to millions of years of evolutionary refinement. Fiddler crabs, as burrow-inhabiting creatures, thrive abundantly in environments such as mangrove forests, salt marshes, and expansive mudflats. They have complex burrows, and the depth of their burrows is related to the groundwater table. Generally, the burrow bottom needs to reach moist mud. Because of their feeding and mating behaviors, their burrows are replaced every few days, which plays a significant role in controlling the sediment in the intertidal zone from above down. 
In 2018, I successfully earned a PhD in hydrogeology from China University of Geosciences (Beijing). Prior to that, in 2017, I had the privilege of being sponsored by my esteemed advisor, Professor Hailong Li, to undertake a visit to the Department of Earth, Ocean, and Environment at the University of South Carolina in the United States. During this visit, I was fortunate to be mentored by Professor Alicia Wilson, a renowned coastal wetland hydrogeologist, who imparted invaluable training and guidance to me. While conducting a survey of the hydrological processes in salt marshes along the East Coast of the United States, we found that fiddler crabs were everywhere on the tidal flats during low tides. Using numerical simulations in the lab, we explored the impact of vertical crab burrows on the hydrological cycle of coastal wetlands, and found that these burrows significantly changed the path of groundwater circulation and the transport of dissolved salts. 
Upon my return to China in 2018, the esteemed Belle W. Baruch Foundation in the United States acknowledged the significance of our research investigating the influence of fiddler crabs on salt marsh hydrology. Recognizing my contributions, they honored me with a Visiting Scientist Award, inviting me to undertake a two-month fieldwork stint at the Baruch Marine Field Laboratory, situated in Georgetown, South Carolina. This endeavor aimed to delve deeper into the intricate relationship between fiddler crab burrowing activities and their implications on the carbon cycle.
The title of my research project was “Impacts of crab burrow on exchanges of inorganic and organic carbon across the interface of water column and sediments in salt marshes”. I got a lot of help from the University of South Carolina, such as carbon expert Prof. Susan Lang, isotope expert Prof. Willard Moore, and field station staff (Dr. Erik Smith, Dr. Matthew Kimball, etc.). Specifically, Professor Isaac Santos, a renowned blue-carbon expert, learned of my impending trip to the United States to conduct research on fiddler crabs. In response, he kindly dispatched Rogger Correa, a PhD student from Australia, to assist me with my fieldwork endeavors. I also want to thank my wife for working with me in the field in the salt marsh wetlands of South Carolina, where we not only measure CO2 in hundreds of fiddler crab burrows every day, but also fight against the dreaded mosquitoes. With the help of so many people, I became more interested in fiddler crab research. In the next five years, I conducted a lot of research on fiddler crabs burrow’ role in hydrological processes and element cycles based on field monitoring, numerical simulation and laboratory experiments. 
Specifically, in August 2021, the National Natural Science Foundation of China (NSFC) granted me a four-year funding for a research endeavor under the project titled “The Influence of Fiddler Crab Bioturbation on the Groundwater Cycle and Dissolved Inorganic Carbon Fluxes in Mangrove Wetlands.” This funding enabled me to delve into the intricate relationship between the disruption caused by fiddler crabs and its impact on the carbon cycle. Collaborating with a team of enthusiastic young scientists in China, who share a profound interest in the behavior and ecology of fiddler crabs, we embarked on this ambitious project. For example, Dr. Feng Pan of Xiamen University, who is very good at using high-resolution in-situ monitoring to investigate the biogeochemical processes of fiddler crab burrows, Dr. Yan Liu of Southern University of Science and Technology and Dr. Maosheng Yin of Eastern Institute of Technology in Ningbo, are particularly good at using numerical simulations to investigate the effects of irregular crab burrows on groundwater circulation. However, after carrying out a lot of research work, I found that these studies are fixed-point case studies, and how to carry out the influence of fiddler crab perturbations on carbon cycle in different climatic zones at larger spatial scales is a scientific problem to be solved urgently. 
To answer the above scientific question, I have collaborated may colleagues in China, particularly Dr. Hebo Peng and his team at Guangdong University of Technology, have been extremely helpful in conducting extensive sampling along nearly 18,400 km of China’s coastline. We collected paired samples of crab burrow walls and adjacent sediment substrates from different ecosystems (salt marshes, mangroves, bare mudflats and tidal creek banks) at 21 study sites along continental coastlines. After we obtained these samples, we did a lot of testing work, including sediment particle size analysis, hydrochemical indicators and carbon-related indicators. In particular, we conducted culture experiments on the samples for a month to detect differences in the rate and flux of greenhouse gas production. 
Through the integration of changes in organic carbon and humus components in sediments under the disturbance of fiddler crabs, it was found that the heavy fraction of organic carbon (HFOC) in fiddler crab burrow sediments had a higher enrichment ratio compared to the light fraction of organic carbon (LFOC). The influence of fiddler crab burrowing on humus components was relatively complex, with humin content in burrow sediments higher than in the matrix in salt marshes and tidal creeks, but the opposite trend occurred in mudflats and mangroves. Compared to sediment matrixes, the emission rates of CO2, CH4, and N2O from burrow sediments increased by 23%, 120%, and 30% respectively, with CO2 emissions increasing by 17%-30%, CH4 by 49%-141%. Analysis of the relationships between organic carbon composition, enzyme activity, climate gradients, and greenhouse gas emissions indicated: (1) Fiddler crab burrows enhanced oxygen penetration, leading to increased soil organic carbon consumption and thus promoting greenhouse gas production; (2) CO2 emissions were primarily influenced by organic carbon content and soil enzyme activity, while CH4 emissions were controlled by enzyme activity and humus content. However, the overall correlation between N2O emissions and environmental indicators was not significant; (3) Greenhouse gas emissions within fiddler crab burrows were indirectly constrained by HFOC and LFOC, while greenhouse gas emissions in sediment matrix were directly related to climate conditions. Finally, statistical results showed that increased greenhouse gas emissions from fiddler crab burrows in mangroves and salt marshes could offset 35%-134% of sediment carbon sequestration. Burrows in mangroves generated more CO2 and CH4 emissions than those in salt marshes.

Effects of fiddler crab burrows on carbon cycle fluxes and carbon components in sediments

In summary, the carbon sequestration potential of coastal blue carbon ecosystems may be lower than expected due to disturbances to benthic organisms. Nevertheless, intricate relationships intertwine crab burrows, habitat diversity, and climatic factors. Crab burrows may also increase carbon storage by increasing organic matter accumulation and improving plant primary productivity. Future research needs to be conducted on a larger spatial and temporal scale to study the impact of fiddler crab disturbance on the blue carbon cycle in coastal ecosystems, further discussing the complex mechanisms of biological disturbance on the system’s carbon sequestration. This study brings new insights into the role of coastal ecosystems in the global carbon cycle and provides new evidence for coastal management and protection. This work is titled as “Widespread crab burrows enhance methane emissions from coastal blue carbon ecosystems” and published in the latest issue of Communications Earth & Environment (https://doi.org/10.1038/s43247-024-01621-2).
 
I dedicate this piece to express my heartfelt gratitude to those who have assisted me on my journey of scientific research.

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