Burrowing crab effects on the properties and functions of coastal soft sediments

Burrowing ecosystem engineers, such as termites, crabs, marmots, and foxes, can profoundly affect the biological structure and ecosystem functions of their environments. However, the relative importance of burrowing engineers on sediments are challenging to predict and are expected to be influenced by engineer density, engineer functional traits (e.g., burrow morphology), and environmental conditions (e.g., geomorphology, vegetation presence). To develop robust hypotheses predicting the impacts of burrowing ecosystem engineers, we conducted a systematic meta-analysis evaluating the effects of burrowing crabs on sediment properties, nutrient stocks, and ecosystem functions in coastal soft-sediment habitats (e.g., salt marshes, mangrove forests, tidal flats). The data set includes 1422 effect size calculations for the effects of burrowing crabs on sediments collected from 59 total manuscripts. The data suggest that burrowing crabs rework and oxygenate sediments and accelerate rates of nutrient cycling (i.e., nitrification and CO2 flux). However, the magnitude and direction of burrowing crab effects depend on burrowing crab superfamily, the presence of vegetation, and their interaction. Crab burrow density does not consistently predict burrowing engineer effects on sediments. 

Methods
Search string development and literature survey.

To develop our search string, we consulted the preferred reporting items for systematic reviews and meta-analyses (PRISMA; Moher et al. 2009, Page et al. 2021) and implemented a modified version of the Population, Intervention, Comparison, Outcome (PICO) approach (Foster and Jewell 2017). We defined our populations as burrowing crab communities located within soft-sediment tidal ecosystems. Our variable was broadly defined and included all known pathways by which burrowing crab communities may influence sediments and their functions (e.g., bioturbation, excavation, burrowing, particle reworking, herbivory, facilitation). The outcome was any change in edaphic conditions or sediment functions. The final search string is as follows (the string is presented in sections to specify the intent of each group of search terms, underlined headings were not included in the Boolean string):

Crab Engineer Populations: ((burrowing NEAR/0 crab) OR crab OR (ecosystem NEAR/0 engineer)) OR (uca OR leptuca OR  minuca OR (fiddler NEAR/0 crab) OR ocypodid) OR (sesarm OR grapsid OR purple marsh crab) OR (neohelice OR chasmagnathus) OR (pachygrapsus OR ("lined shore" NEAR/0 crab))

AND

Crab Engineer Effect Pathways: ((bioturbation OR bio-irrigation OR bioengineering OR excavation OR burrow OR biomixing OR (particle NEAR/0 rework) OR ventiliat OR morphodynamic OR geomorphic) OR (sediment OR soil OR (intertidal NEAR/0 sediment*)) OR (herbivory OR mutualism OR "top-down control" OR (ecosystem NEAR/0 engineer) OR consum OR graz OR facilitat))

AND

Crab Engineering Outcomes for Sediments: (carbon OR "organic matter" OR decompos OR decay OR respira OR efflux OR (methane OR (CH4)) OR ("carbon dioxide" OR (CO2)) OR fixation OR carbon NEAR/0 flux) OR (nitrogen OR denitrification OR nitrification OR anammox OR DNRA OR nitrate OR ammonium OR nitrite) OR ((sediment NEAR/0 biogeochemistry) OR biogeochemistry OR (sediment NEAR/0 chemistry) OR (soil NEAR/0 chemistry) OR redox OR reduction OR oxygenation OR oxidation OR iron OR sulfur OR sulfate OR manganese) OR (erosion OR erod* OR sediment* OR accret* OR deposit* OR accumulat* OR import* OR export*) OR (nutrient cycling OR nutrient*)

AND

Focal Burrowing Crab Habitats: ((salt NEAR/0 marsh) OR saltmarsh OR marsh OR (salt NEAR/0 panne) OR Spartina OR Juncus OR Phragmities OR Salicornia OR Sarcocornia) OR (mangrove OR (mangrove NEAR/0 tree) OR Avicennia OR Rhizphora) OR (mudflat OR (mud NEAR/0 flat)) OR (tidal OR coastal)

NOT

Exclude: (dune OR freshwater) OR (metal OR pesticide OR pollut) OR (larva OR embryo) OR (seagrass OR eelgrass).

We input our Boolean search string into Web of Science (WoS) Core Collection (http://isiknowledge.com/) on 03 September 2021 and restricted the search to journal articles only. This search yielded 1424 articles. To capture as much of the literature as possible, we also input our Boolean search string into the WoS BIOSIS Previews, WoS Biological Abstracts, and Zoological Record databases on 03 September 2021. The four database searches were merged, and duplicates removed using Endnote (https://endnote.com/). This yielded a merged RIS file containing 1424 unique articles.

Literature screening.

We input our merged RIS files into Rayyan (https://rayyan.ai/; Ouzzani et al. 2016). In Rayyan, each article (n = 1424) was randomly allocated to two blind reviewers. Reviewers evaluated the title and abstract of each article to determine if it should be included, excluded, or reconsidered (i.e., “maybe” in Rayyan software). Included articles needed to evaluate the relationship between burrowing crab density (relative or absolute) on edaphic conditions and sediment functions in a soft-sediment tidal ecosystem. Articles were excluded if they did not include burrowing crabs, quantify sediment properties and functions, or perform the study in a soft-sediment tidal habitat. We also excluded articles that were 1) qualitative with no primary data, 2) modeling or meta-analyses with no primary data, or 3) a graduate thesis where the data was also in a published article. Reviewers could also mark the article for reconsideration if they felt the title and abstract did not provide enough information to include or exclude the article.

Our first review of articles yielded 102 included articles, 112 ‘maybe’ articles, and 1210 excluded articles. We did a secondary review of all included and ‘maybe’ articles (n = 214). This secondary review involved a single reviewer reading the article in its entirety and determining if the article was eligible for inclusion based on the same criteria used during the first review in Rayyan. Our second review resulted in 87 articles that we considered for data collection. After reviewing these 87 articles, we decided to focus on articles that used comparative methodologies to assess edaphic conditions and sediment functions in habitats with high vs. low relative burrowing crab density. We chose to focus on articles that used comparative approaches, rather than articles that took a strictly correlative approach, because studies used a variety of burrowing crab density proxies (e.g., individual crab vs. burrow counts) and standardizing measurements of edaphic conditions and sediment functions across studies limited our sample sizes. Ultimately, we had 56 articles that we used for data collection. We also added three additional articles (Walker et al. 2021, Rinehart et al. 2023, Rinehart et al. in prep) that were close to publication at the time of the search. This resulted in our data set containing 59 total articles.

Data collection.

From each article, we collected data on sediment physical conditions, nutrient stocks, and ecosystem functions in habitats with relatively high vs. relatively low burrowing crab activity. We extracted data from tables, text, and figures (using Web Plot Digitizer; Rohatgi 2022). For each relevant study, we extracted the sample size, mean, and variance (standard error or standard deviation). Because the mean was not reported for all data in five articles (Martinetto et al. 2011, Escapa et al. 2015, Alvarez et al. 2018, Giorgini et al. 2019, Wang et al. 2020), we extracted the sample size, minimum, first quartile, median, third quartile, and maximum values of sediment characteristics and functions for these studies. We used this information to estimate the means and standard deviations for these studies (n = 50; Wan et al. 2014). If articles included multiple relevant independent studies, we extracted each individual study. This process resulted in 1422 total studies evaluating the relative effect of burrowing crabs on coastal soft-sediments and their functions. For each extracted study, we also recorded the following potential covariates: (1) ecosystem type (categorical: tidal flats, tidal marsh, mangrove forest), (2) Crab burrow density (continuous: density per m2), (3) vegetation (categorical: vegetated, unvegetated), (4) burrowing crab superfamily (categorical: Grapsoidea, Ocypodoidea, mixed community), and (5) methodology (categorical: manipulative, observational). 

Effect size calculations.

We conducted our meta-analysis using OpenMEE software (Build date: 26 July 2016; Wallace et al. 2017). We calculated the Hedges’ d (hereafter, d) to evaluate the effects of burrowing crabs (present/absent) on coastal sediment characteristics and functions (Hedges 1981). The Hedges’ d represents the relative difference between ‘Crab Present’ treatments and ‘Crab Absent’ treatments divided by the pooled standard deviation (Hedges 1981). If manuscripts included multiple ‘Crab Present’ treatments (e.g., Moore 2019), an individual Hedges’ d calculation was performed for each ‘Crab Present’ treatment relative to the ‘Crab Absent’ treatment. We used d because it is less sensitive to small sample sizes than other effect size calculations (Osenberg et al. 1997, Lajeunesse and Forbes 2003). A positive effect size indicates that burrowing crabs increased the response variable, while a negative effect size indicates that burrowing crabs decreased the response variable.

Variability and publication bias

We tested for potential publication bias by calculating Kendall’s Rank Correlations (Tb) between effect size and pooled variance within each dataset (Begg and Mazumdar 1994).

References

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