Sage Journals: Discover world-class research

Abstract

In northern Peru, the mangrove crab Ucides occidentalis is of great importance due to its ecological, economic, and social role. In this study, we reported for the first time the presence of microplastics in the gills and digestive tract of the mangrove crab U. occidentalis derived from local markets in Tumbes. Microplastics were identified in 100% of the crabs analyzed with a total of 921 items, 475 items (52.57%) found in the gills, and 446 (48.43%) found in the digestive tract. The size range was established in 2 to 250 µm, 250 to 500 µm, 500 to 1 mm, and 1 to 5 mm, microplastics with sizes between 2 and 250 µm were the most common with 53.79% in the digestive tract and 90% in the gills. A total of six different types of microplastic were recorded; The highest percentages for each tissue were fibers (59.64%–61.05%) and films (19.28%−36.63%), with clear fibers being the most prevalent microplastic type in both tissues. Microplastics with less than 250 µm size were found 90% in the gills and 53.79% in the crab digestive tract. Although the present study is a baseline for rapid identification of microplastics in mangrove crab, we suggested that these findings provided more information on the state of contamination as well as food security alert for local markets.

Keywords

Mangrove crab fibers gills digestive tract food security

Background

Marine litter is mainly made up of plastic (90%) (Crawford & Quinn, 2017), with land-based sources contributing 80% of that plastic litter, associated with the fastest-growing size population and the lack of waste management infrastructure (Jambeck et al., 2015). Furthermore, direct input such as aquaculture, fisheries (loss of nets), maritime transport, and tourism (loss of litter) (Barboza et al., 2018), contributed large amounts of plastic that through currents within the Humboldt Current System (HCS) transfer floating plastic into the South Pacific Subtropical Gyre (SPSG) with highest concentration in the Oceanic and Polynesian sector (Thiel et al., 2018).

Due to its persistence for centuries and its ability to absorb chemical pollutants such as polycyclic aromatic hydrocarbons (PAH), polychlorinated biphenyl (PCB), organochlorine pesticides (OCP), diphenyl-dichloro-ethane (DDT), brominated diphenyl ethers (BDE), and organophosphorus flame retardants (OPFR) (Camacho et al., 2019; De-la-Torre, 2020) resulting in a cockatiel of contaminants (Rochman, 2015) plastic is considered a risk to the global environment, socioeconomic well-being, and an impact on food security (Botterell et al., 2019; Walkinshaw et al., 2020). However, the main concern is on any plastic particles between 1 µm and 5 mm denominated microplastic, which are created at microscale (primary microplastics) or derived through degradation in the environment (secondary microplastics) (Crawford & Quinn, 2017; Watts et al., 2014) bioavailable to wildlife (Rochman, 2015); morphological properties, including shape, size, and color of the plastic are also important for the rapid identification of main sources of contamination, exposure to biota and their fate in the environment (Rodríguez-Seijo & Pereira, 2017).

These plastic particles can interact with different species through trophic levels by ingestion; including marine mammals (Zhu, Yu et al., 2019), seabirds (Provencher et al., 2018), fish (Pannetier et al., 2020), crustaceans (Cau et al., 2019), mollusks ( Li et al., 2018), echinoderms (Plee & Pomory, 2020), corals (Rotjan et al., 2019), and zooplankton (Botterell et al., 2019); moreover, microplastics can accumulate organisms on their surface (biofouling) being able to represent potential pathogens (Kooi et al., 2017). The presence of microplastics has also been detected in commercial seafood consumed by humans (Walkinshaw et al., 2020); fish (eg, peruvian anchovie), bivalves, crustaceans (eg, blue crab), and echinoderms (Baechler et al., 2020; Li et al., 2015; Ory et al., 2017; Waddell et al., 2020). Microplastics have been shown to accumulate in the gills or gastrointestinal tract, with human exposure to plastics occurring where the whole organism is consumed (Baechler et al., 2020).

Microplastic pieces have been found in different ecosystems (Pauna et al., 2019) including coastal mangroves (Garcés-Ordóñez et al., 2019). This ecosystem functions as a natural biological filter for waste from marine and land-based sources (Martin et al., 2019); they trap marine plastic debris for years, especially when they are geographically close to maritime routes and have a large amount of pneumatophores (Cordova et al., 2021). They remove and degrade different types of contamination in water and sediment (plastic, pesticides, and heavy metals) (Moroyoqui-Rojo et al., 2015), allowing the presence of microplastics in the sediment, water column, and local aquatic organisms (including fish production from wild or aquaculture fisheries and commercial crabs) (Barasarathi et al., 2014; Cordova et al., 2021; Moroyoqui-Rojo et al., 2015).

As mentioned before, microplastic have the ability to interact with different mangrove species through trophic levels, especially in commercial seafood that may have implications for food security (Cordova et al., 2021). In Peru, the mangrove crab Ucides occidentalis plays an important role in this ecosystem, promoting the retention of nutrients, the reduction of organic matter to increase nitrogen recycling in mangrove soils, and the oxygenation and fertilization of muddy soil through the construction of its burrow (Nordhaus & Wolff, 2007; Solano & Moreno, 2009; Zambrano & Meiners, 2018). These crabs are considered ecosystem engineers, as they change the availability of resources for associated organisms by modifying the physical structure, transport conditions, and the chemistry of the substrate (Advíncula, 2017). As a commercially-exploited, edible species, its main wholesale centers are in Tumbes (El Tumpis) and Zarumilla (Puerto 25 and El Bendito), with 2,204,585 kg (70.62%) landed each year compared to the black shell (34.3%), hollow shell (3.82%), and striped shell (5.79%) (Ordinola et al., 2013). Through seafood, humans can ingest 37 microplastics annually (Baechler et al., 2020). Although humans can remove 90% of microplastics through feces, they may have an adverse effect on human health (disturbance of the gut microbiome, transfer of pollutant, and inflammatory responses) (Wright & Kelly, 2017).

In Tumbes, the mangrove receives the waters of the Tumbes River (INRENA, 2007). In the river, the city sewage is discharged directly without prior treatment, as the wastewater treatment system is not optimal and has been malfunctioning since 2007 (SUNASS, 2010). Lebreton et al. (2017) considered rivers as a main source of microplastics input. Additionally, human activities in the mangrove ecosystem: tourism, recreational activities, and marine industries (aquaculture) can affect the abundance of microplastics (Andrady, 2011). In the mangroves of Tumbes, the tourist and recreational zone comprises a total area of 137.5 ha, where U. occidentalis is located (INRENA, 2007). Also, the aquaculture of shrimp in mangrove zones (INRENA, 2007) produced microplastics that could enter directly into the mangrove environment by currents or tides (Cole et al., 2011; Deng et al., 2021). Although microplastics have been identified in a variety of edible shellfish species, (Deng et al., 2021; Walkinshaw et al., 2020), there have been no studies on the mangrove crab U. occidentalis, one of the most important crustaceans for the mangrove ecosystem in Tumbes.

Since 2022 knowledge, and practices related to the extraction of the mangrove crab U. occidentalis is considered Cultural Heritage of the Nation in Peru (R. VM N° 000036-2022-VMPCIC/MIC). This activity is carried out by 450 families in Tumbes belonging 72% to Tumbes district and 28% to Zarumilla district (PNIPA, 2018). Being the only economic activity of the crabbers, with a maximum extraction of 64 crabs per person per day, they receive the minimum wage apart from closed season when they do not carry out the activity (PNIPA, 2018). The possible absence and/or decrease of the mangrove crab would generate not only an economic loss for the families that dedicate themselves exclusively to this activity, but also a cultural one, since this activity is learned from generation to generation.

Therefore, the objective of this study is to characterize and morphologically classify the presence of microplastics in the gills and digestive tract of the mangrove crab (U. occidentalis) sourced from the main local markets in Tumbes city, Peru. The study will contribute to the development of ideas for future research in the Peruvian mangrove ecosystem, as well as for its use in integrated management plans in the marine coastal areas of Tumbes.

Methods

Sample site

U. occidentalis (Ortmann 1897) has a distribution from Isla Espiritu Santo (Mexico) to San Pedro de Vice mangrove, Sechura (Peru) (Alemán & Ordinola, 2017). In the present study, the principal city local markets were selected: El Tumpis and Tumbes Market (Figure 1).

Figure 1.

(A) Location of Peru and (B) Tumbes region. (C) Local Markets in Tumbes city: El Tumpis and Tumbes Market.

Thirty crabs were purchased from local markets in the city of Tumbes fulfilling the minimum landing size (MLS) according to Peruvian Article No. 3 of RM 445-2014-PRODUCE with a cephalothorax width (CW) greater than 65 mm, the measurements were taken once with the crab alive (Table 1 and Figure 2). According to Zambrano et al. (2018), this size range is consistent with the age of 2 years in the mangrove crab U. occidentalis. The samples were transported in a cooler to the Universidad Nacional de Tumbes laboratory. There they were sexed according to Carbajal Enzian and Santamaría (2017), all samples were male crabs due to the Peruvian Article No. 5 of RM 445-2014-PRODUCE prohibiting the extraction and commercialization of ovigerous females.

Table 1.

Ucides occidentalis (mangrove crab) Average Width and Length (±SD) From Local Markets (n = 30).

Sites	Size (mm)
Sites	Cephalothorax width (CW)	Cephalothorax length (CL)
El Tumpis	82.61 ± 4.64	57.39 ± 3.05
Tumbes Market	78.58 ± 6.23	55.79 ± 4.92

Figure 2.

Mangrove crab (Ucides occidentalis).

The gills and digestive tract were dissected and stored in individual falcon tubes prior to digestion and characterization. To prevent airborne contamination, the falcon tubes were covered in aluminum foil and stored in a hermetical cooler at 0°C (Naji et al., 2018) to be transported to the laboratory at the Instituto del Mar del Peru (IMARPE) in Lima until further treatment.

Quality assurance

The laboratory was kept clean, all work surfaces were wiped with 70% ethanol, and all windows and doors were closed to avoid air movement.

To avoid potential contamination in treatment, KOH was filtered through a support membrane filter with a pore size of 0.2 µm and the distilled water was vacuum filtered on a cellulose membrane with a pore size of 0.45 µm (Merck) prior to use. Then, all the apparatus (falcon tubes, glass beakers, Petri dishes), were rinsed with distilled water four times before use. Air movement during filtration was minimized using a “transparent PVC vinyl protector” in the laminar flow cabinet.

Soft tissue digestion

According to Protocol 1b with a modification by Dehaut et al. (2016) approximately 50 ml of 10% KOH were added to each falcon tube to digest the organic matter and placed in an incubator at 60°C for 48 hours.

Due to its habitat in muddy areas (Alemán & Ordinola, 2017), the digested material in the digestive tract had a lot of sediments, so the sediment protocol of Coppock et al. (2017) was used to extract microplastics from the sediments found in the crab digestive tract. Therefore, 30 beakers (100 ml) were sterilized where the digestive tract and 450 ml of water were added with 83 g of NaCl and 9 g of ZnCl₂. A magnetic stirrer was used to mix them for 5 minutes at 70 rpm and kept in an incubator at 30°C to avoid evaporation.

Filtration and Characterization

The supernatant in the samples was vacuum filtered over a support membrane filter (hydrophilic polyethersulfone—PES) with a pore size of 0.2 µm (Support^® 100, Gelman Sciences) in a laminar flow cabinet.

The number and type of microplastics were recorded for the gills and digestive tract. Six categories were identified to classify microplastics according to their shape: foam, film, fragment, pellet, fiber, and microbead using a digital camera with the Motic Images Plus 3.0 program for visual identification and classification described by Kovač Viršek et al. (2016). There is currently no FTIR- situated in Peru limiting the capacity for verification.

FTIR-ATR analysis

The polymer characterization was performed by a FTIR-MIR-ATR Perkin Elmer Frontier Dual Range at the Department of Sciences-Chemical Section from Pontificia Universidad Catolica del Peru.

Fibers (4) were randomly chosen for the analysis. Each sample was placed on the Universal Attenuated Total Reflectance Accessory (UATR) crystal, pressed, and the spectrum was collected. Each result is the average of 64 scans, with a precision of 4 cm⁻¹, in the mid infrared range (MIR: 380–4000 cm⁻¹). The obtained spectra were compared with De Frond et al. (2021) polymer spectra library, the type of microplastic was determined when the correlation rate was higher than .70. The final results were processed in the program OriginPro 2022b (Origin (Pro), 2022).

Statistical analysis

To compare the abundance of microplastics between the gills and the digestive tract of the mangrove crab. First, normality (Shapiro-Wilk’s test) and homogeneity of variance (Levene’s test) were calculated. To be considered statistically significant, the p-value was established at 0.005. Data did not meet the parametric statistics criteria (Shapiro-Wilk normality test and Levene’s homogeneity test p-values < .005). Consequently, the Mann Whitney-Wilcoxon test was used to compare differences in microplastic abundance between gills and digestive tracts. No blank correction was applied; we used an air filter to avoid microplastic contamination in the laboratory fume hood. All analyzes were performed with Microsoft Excel and RStudio (R Core Team, 2016).

Results

We identified a total of 921 microplastics and established them in four ranged sizes: 2, 250, 250, 500,and 500 µm to 1, 1, and 5 mm, with 475 (52.57%) found in the gills and 446 (48.43%) found in the digestive tract. Fibers were the most common microplastic type in the gills (61.07%) and digestive tract (59.54%). The color of each type of microplastics related to the tissue was described: In the gills, a greater number of clear fibers 125 (13.57%) and black films 77 (8.36%) were found; instead, in the digestive tract clear fibers 192 (20.84%) and black fragments 81 (8.79%) were the most predominated (Figure 3). The median abundance of microplastics was significantly different (p = .0045) between the gills and digestive tract. The higher percentages of microplastics types for each tissue were fibers and films (Table 2).

Table 2.

Total Percentage (%) of Microplastics Type for Each Tissue (gills and digestive tract) in U. occidentalis..

Tissue	Type	Number of items	Percentage (%)
Gills	Fiber	290	61.05
	Film	174	36.63
	Fragment	1	0.21
	Pellet	7	1.47
	Foam	3	0.63
	Microbead	0	0
	Total	475	52.57
Digestive tract	Fiber	266	59.64
	Film	86	19.28
	Fragment	90	20.18
	Foam	3	0.67
	Microbead	1	0.22
	Pellet	0	0
	Total	446	48.43

Figure 3.

Microplastic abundances according to their color type and examined tissue.

The size of the microplastic ranged from 2 to 5 mm in the gills and digestive tract of the mangrove crab. Microplastics less than 250 µm were the most common, consisting of 90% for the gills and 53.79% for the digestive tract (Figure 4). The digestive tract (46.21%) had microplastics larger sizes (0.25–5 mm) than the gills (10%) (Figure 4).

Figure 4.

Composition of the different sizes found in the gills and digestive tract.

The spectra obtained from the randomly chosen microplastics is illustrated in Figure 5. FTIR-ATR analyses indicated that the microplastics found are made of two main polymers due to the correlation matching ratio with the standard spectrum from De Frond et al. (2021): Polyester ([polyethylene terephthalate, PET] :1714,1243,1097,726 cm⁻¹) with a correlation rate between .91 and .96, and Polyethylene-vinyl acetate (PEVA:2243,1737,1452,1238 cm⁻¹) with a correlation rate around .89 (Figure 5).

Figure 5.

FTIR-MIR-ATR spectra of the main polymers found in the microplastics ingested by U. occidentalis: Polyethylene terephthalate (PET), and ethylene-vinyl acetate (PEVA). The value in parenthesis is the correlation matching ratio with the standard spectrum for each polymer.

Discussion

The present study represents the first report of microplastics in the gills and digestive tract of the mangrove crab U. occidentalis of Tumbes. Our study evidenced the presence of microplastics in 100% of the evaluated organisms. This could be due to the origin of the crab; the local markets commercialize mangrove crabs from the high intertidal zone (INRENA, 2007), and plastic pollution in this area is directly related to the number of habitants in its zone (Yin et al., 2020). Furthermore, the intertidal zone, where the crab makes it burrows, is composed of the root system of the mangrove Rhizophora mangle (Garcés-Ordóñez et al., 2019; Zambrano & Meiners, 2018); studies showed a great abundance of microplastics in the roots of the mangrove, which act like litter traps (Garcés-Ordóñez et al., 2019; Martin et al., 2019).

Crab ingestion and ventilation systems are the pathways of microplastic entry into crabs (Daniel et al., 2021). All Infraorder-Brachyura commercial crabs (Table 3) reported the presence of microplastics in edible tissue. The highest average of microplastic intake (327.56 MPs) was recorded by Patria et al. (2020), for the crab Metopograpsus quadridentatus, which as an opportunistic omnivorous- scavenger consumes a wide variety of invertebrates allowing the presence of microplastics in its food (Torn, 2020). Not et al. (2020) found 90% of the microparticles (>10 µm) inside the stomach of Parasesarma bidens, Metopograpsus frontalis and Thalamita crenata suggesting that ingestion system is the main path of microplastic intake. In our results, U. occidentalis hat 15.83 ± 4.38 (items/individual) in the gills and 14.86 ± 3.59 (items/individual) accumulating more microparticles less than 250 µm (Figure 4). Based on the results, even though it has a feeding behavior as a detritivorous species, consuming decaying mangrove leaves (Forgeron et al., 2021; Zambrano & Meiners, 2018), the ventilation system is the main path of intake for microparticles less than 250 µm.

Table 3.

Comparison of Microplastics Abundance and Their Morphological Properties Between Commercial Crabs of the Same Infraorder: Brachyura.

Location	Species	Abundances (item/individual)	%Types of MPs	Tissue/Organ studied	Most common color	Common size	References
Florida, USA	Panopeus herbstii	3.1 ± 2.4 (Highest value)	Fibers (85%)		Blue (87%)		Waite et al. (2018)
Hong Kong, China	Parasesarma bidens	Average: 60.5	Fragments (80%), Beads (13%)			>10 µm	Not et al. (2020)
	Paraleptuca splendida		Fibers (Not specify)
	Metopograpsus frontalis		Fragments (80%), Beads (13%)	Gills and stomach
	Thalamita crenata		Mixture Fragments, beads, and fibers
Jakarta Bay, Indonesia	Metopograpsus quadridentatus	Average: 327.56	Fibers (68.72%), Films (29.34%), Fragments (0.71%), Pellets (1.22%)	Body Tissue			Patria et al. (2020)
Beibu, China	Chiromantes dehaani	Small MPs: 0.39–2.83Large MPs: 0.74–4.96	Fibers (59.15%), Pellets (20.53%), Films (9.6%)	Gills and Gastrointestinal tract	White (36.75%), Transparent (27.67%)	Small MPs: 1–20 µmLarge MPs: 20–500 µm	Zhang et al. (2021)
Thames Estuary, United Kingdom	Carcinus maenas	October: 6.14 ± 5.33 (Highest value)December: 11.35 ± 7.91 (Highest value)	Fibers (78%), Films (9.6%)	Gastric mill, gastrointestinal tract, and gills	Clear (25.1%), white (21.9%)	54 µm to 34 mm	McGoran et al. (2020)
Thames Estuary, United Kingdom	Eriocheir sinensis*		Fibers (78%), Films (9.6%)	Gastric mill, gastrointestinal tract, and gills	Clear (25.1%), white (21.9%)	34 µm and 32 mm	McGoran et al. (2020)
Bahia Blanca, Argentina	Neohelice granulata*	0.7 ± 0.15 (Highest value)	Fibers (60%), Fragments (40%)	Gills and Digestive tract	Blue	500–1500– µm	Villagran et al. (2020)
Kerala, India	Portunus pelagicus	0.14 ± 0.44	Fragments (80%), Fibers (20%)	Edible tissue	White- Transparent (50%)	100–200 µm	Daniel et al. (2021)
Tumbes, Peru	Ucides occidentalis*	Gills: 15.83 ± 4.38Digestive tract: 14.86 ± 3.59	Gills: Fibers (61.05%), Films (36.63%)Digestive tract: Fibers (59.64%), Films (19.28%)	Gills and Digestive tract	Clear (>50%), Black (⩾20%)	2–250 µm	This study

Burrowing crabs.

Gills as a mode of uptake

In this study, microplastic was significantly found in the gills than in the digestive tract (p = .0045). Detritivorous mangrove crab P. bidens, filter sediment pellets and water employing different mechanisms to store it into gills chambers (Not et al., 2020). The microplastic recovered from the gills of U. occidentalis (52.57%) (Table 2) and Neohelice granulata (77%–91%) (Villagran et al., 2020) associated with plastic particles in the water column may have been retained during gills irrigation (Villagran et al., 2020; Watts et al., 2014). This suggest that the fine structures of the gills allow microplastics to be trapped and accumulate (Brennecke et al., 2015). However, only 10% of microplastics were found in the gills of the mangrove crabs P. bidens, M. frontalis, and T. crenata, dismissing the ventilation system as a possible route of microplastic intake (Not et al., 2020). This is due to the blockage of the opening of the gastrointestinal tract caused by the microplastics, preventing their egestion, therefore it produces an increase in the retention of microplastics in the digestive system (McGoran et al., 2020).

The presence and accumulation of microplastic in gills may reduce osmoregulatory and respiratory capability due to the gas exchange that is generated in the gill’s chambers (Miller, 1961; Villegas et al., 2021). The water in the gill chamber is recycled and evaporated trickling down to the top of the legs, allowing more concentration of microplastic in the gill chamber (Villegas et al., 2021).

Digestive gland as a mode of uptake

The abundance and type of microplastic in the digestive tract are related to the crab’s feeding behavior and its role in the food web (Not et al., 2020). Crabs with opportunistic feeding behavior can consume microplastic with their food (Torn, 2020). Only microplastic with too large sizes are expelled from the digestive tract through feces (Torn, 2020).

This study showed that U. occidentalis and Eriocheir sinensis have 14.86 ± 3.59 (digestive tract) and 11.35 ± 7.91 microplastic per individual ±SD, respectively (Table 3). Both being burrowing crabs remove decaying plant material—mangrove leaves from the sediment and dragged it into their burrows for 2 weeks before its consumption (Forgeron et al., 2021; Nordhaus et al., 2011). This behavior increases their exposure to plastic waste during their burying and storing activity (Forgeron et al., 2021; McGoran et al., 2020 ). Also, this activity allowed the presence of mud in the stomach of many crabs (Clark et al., 1997). McGoran et al. (2020), evidenced 1.9% of mud in the stomach of E. sinensis and 16.0% in Carcinus maenas. As well, we evidence the presence of mud in every digestive tract of each crab. U. occidentalis is a detritivorous species that mainly ingest Rhizophora mangle leaves and organic sediment on the mangrove floor (Zambrano & Meiners, 2018).

The sediment on the mangrove floor has a great abundance of plastic particles that can be accumulated for a long time near the vegetation and possibly settle to greater depths, were crabs carry out the burying and storing activity (Maghsodian et al., 2022; McGoran et al., 2020). In the southern mangrove’s sediments of China, a total of 3,520 ± 107 microplastic per kg were reported (Zhang et al., 2020a,b), in Colombia 540 ± 137 microplastic number per hectare were collected (Garcés-Ordóñez et al., 2019). The average number of particles isolated from mangrove sediments around the world depends on the levels of human activity (Nor & Obbard, 2014). In Tumbes, recreation and aquaculture activities may affect the number of microplastic in the Peruvian mangrove’s sediment and its exposure to U. occidentalis.

Types of microplastics found

Fibers were the most common microplastic morphotype in U. occidentalis for the gills (61.05%) and the digestive tract (59.64%). The predominance of fibers is consistent with the reports of Panapeus herbstii (85%) (Waite et al., 2018), Chiromantes dehaani (59.15%) (Zhang et al., 2020a,b), N. granulata (60%) (Villagran et al., 2020), C. maenas and E. sinensis (78%) (McGoran et al., 2020). Organisms such as bivalves allow the presence of fibers during their ventilation process (Li et al., 2015, 2018; Not et al., 2020). Furthermore, the low density of fibers allows their abundance on the water surface, which is in direct contact with the crab ventilation system (Dai et al., 2018). Horn et al. (2020) found that with an increasing number of fibers in crab organs or tissue, crab mortality increased severely.

The study conducted by Syakti et al. (2017) indicated that 71% of floating microplastics with sizes between 0.33 and 5 mm are white or clear (71%), blue (19%), green (11%), red (5%), black (2%), and yellow (1%). A wide range of species such as seabirds, sea turtles and the planktivorous pelagic fish Decapterus muroadsi showed selectivity to blue (40%) microplastics ranging from 0.2 to 5 mm, resembling their copepod prey ( Ory et al., 2017). However, in our study, clear, black, and blue microplastics were the most common with sizes below 0.25 mm (Figures 3 and 4). Other studies also reported that the clear or white color is the most predominant (Daniel et al., 2021; McGoran et al., 2020; Zhang et al., 2020a), as shown in Table 3. Organisms will eat microplastics colors that resemble their natural food (Ory et al., 2018), especially light colors (clear, white, and grey) and some black colors (Engler, 2012).

Mangrove crabs feed on decaying leaves of the mangrove family trees Rhizophoraceae (Forgeron et al., 2021). Mangrove crab U. occidentalis removed Rhizophora mangle (red mangrove) leaves from the sediment and stores them in its burrow (Holguin & Bashan, 2007). Rhizophora mangle decaying leaves colors are brown and black sometimes they are covered with a thin film of detritus (Hopper et al., 1973). The microplastic color clear and black found in this study (Figure 3) resemble the mangrove crab’s food.

Microplastics with a smaller size range of 0.002 to 0.25 mm constituted 90% in the gills and 53.79% in the digestive tract of U. occidentalis (Figure 4); this is also shown in the crab Portunus pelagicus with a maximum microplastic size of 200 µm (Table 3); the presence of gastric mills apparatus in the digestive tract of crabs, function as a down food breaker (McGaw & Curtis, 2013). Microplastic agglomeration is caused by the contraction of the gastric mill and foregut muscles, tangling the fibers (Torn, 2020). The crab Nephrops norvegicus showed that the microplastic filaments are unable to be excreted and some of them are shredded into smaller fibers (Andrade & Ovando, 2017; McGoran et al., 2020).

The most common polymers ingested by crabs are polyethylene terephthalate (PET), polystyrene (PS), polyethylene (PE), polypropylene (PP), and polyamide (PA) (Yi et al., 2021). PET is the most abundant polymers found in the digestive tract of crabs (Yi et al., 2021), due to their large annual global production and their prevalence as clothing fibers,bottles for water, plastic films, food jar, microwavable packaging, etc.(Jones et al., 2020). As these polymers are denser than water (>1.35 g cm⁻³) they precipitate and settle down in the underlying sediments where the mangrove crabs makes its burrow (Yi et al., 2021; Zambrano et al., 2018). The polyethylene-vinyl acetate (PEVA) is originated from adhesive, foam padding, foam floats, fishing rods handles, etc. (Jones et al., 2020), in Tumbes mangroves, recreational activities include the use of plastic items that can be ingested by U. occidentalis. This study adds the first dot in the Equatorial Eastern South Pacific Ocean of the world map revision of microplastics presence in mangrove crabs of the characterize with PET and PEVA (Maghsodian et al., 2022).

Crab health and food security

The presence of microplastics in the gills and digestive tract of U. occidentalis could cause serious harm to the crab, the fine particles can block the glands of the digestive system disturbing body functions such as the absorption of nutrients, the storage of energy reserves, and the segregation of digestive enzymes (Brennecke et al., 2015). Discontinuation of these functions can lead to a decrease in the performance of the organism and in the ecosystem services it provides as the bioecological dynamic balance of the mangrove ecosystem (Brennecke et al., 2015; Zambrano & Meiners, 2018). Additionally, the retention of microplastics in the digestive tract may affect the organism’s health by giving the crab a feeling of false satiety, affecting its feeding behavior (Walkinshaw et al., 2020).

Although, the plastic particle can be detoxified on day 21 and this may result from a decapod behavior called “gill grooming,” crabs counteract microbe colonization in their gills since their habitat is exposed to microbial fouling (Farrell & Nelson, 2013; Waite et al., 2018). Waite et al. (2018), considered the possible use of this behavior to expel a large amount of microplastic from the mud crab gills Panopeus herbstii.

The translocation of plastic particles to crab organs and tissues has been identified (Brennecke et al., 2015; Crooks et al., 2019; Farrell & Nelson, 2013; Watts et al., 2014). Smaller plastic particles from Necora puber, C. maenas, and Uca rapax were found to enter the brain, ovary, gills, stomach, and hepatopancreas (Brennecke et al., 2015; Crooks et al., 2019; Watts et al., 2014).

Morphologically, the surface of the microplastics evidenced a lower degree of degradation (Figure 6). The edges of microplastics films and fragments were fractured (Figure 6B and C), and the surface of microplastics pellets had a cracked texture (Figure 6D). The surface morphology of plastic is affected by physical, biological, and chemical processes in the coastal environment producing degradation (Li, Zhang et al., 2019). Dai et al. (2018) also observed that irregular surfaces and edges in microplastics may increase the probability of attachment and adhesion of contaminants or microorganisms (biofouling), decreasing their buoyancy. Microplastic act as pollutant vector of organophosphate pesticides, found in the sediment and water of Leptuca festae and Minuca ecuadoriensis habitats, being able to enhance toxicological effects on crabs, including DNA damage, metabolic, AchE inactivation, histological, physiological damage, especially in acute and chronic exposure to this pollutant (Knapik & Ramsdorf, 2020; Villegas et al., 2021).

Figure 6.

Different types of microplastics in mangrove crab. Fiber (A), Film (B), Fragment (C), Pellet (D), Foam (E), and Microbead (F).

The plastic association with the microbial community (plastisphere) is present in intertidal zones, and bacteria pathogens for humans and animals such as Vibrio sp., Leptolyngbya sp., and Pseudomonas spp. were attached to microplastic samples taken from the Yangtze estuary in China (Jiang et al., 2018). This can have implications for food security, especially for those species that are in direct contact with plastic particles and live in areas with no sanitary management (Walkinshaw et al., 2020). Mangrove crab meat (U. occidentalis) can be contaminated with microbial agents: Escherichia coli, Pseudomonas spp., and Salmonella spp. (Guaman Quishpi & Renteria Minuchi, 2012). The presence of microplastics in the mangrove crab shown in this study and the lack of a wastewater treatment system in the Tumbes region (SUNASS, 2010) increases the risk of contracting pathogens that could affect the organism and human health.

Through seafood, humans can ingest microplastic, especially in organisms that are consumed whole (Smith et al., 2018). In Peru, U. occidentalis consumption can be whole crab or only claws depending on the dish. The effect of microplastic in humans is based on the frequency, exposure, concentration, and chemical and/or additive adsorption in the microplastic surface (GESAMP, 2015). Also, microplastic toxicity is related to the nature, size, porosity, and hazard of the toxin (Wright & Kelly, 2017). Nevertheless, certain microplastic characteristics allow translocation through cells in the mammalian systems that affect cell health (Smith et al., 2018). Wright and Kelly (2017), explained that microplastic ingestion is a pathway for harmful bacteria that compromise immune cells.

Subsequently, microplastics in the environment can be transported throughout the food web and biomagnified (Maghsodian et al., 2022). This may affect the natural predators for U. occidentalis such as the crab raccoon (Procyon cancrivorus), estuarine fishes, the bare-throated tiger heron (Trigrisoma mexicanum), the great egret (Ardea alba) and the little blue heron (Egretta caerulea) (Diele & Koch, 2010) since these carnivorous predators could indirectly introduce microplastics into their bodies (Maghsodian et al., 2022). The bioaccumulation of microplastics in top predators can cause internal and external deleterious effects due to the concentration and/or absorption of chemicals in the microplastic surface (Capparelli et al., 2022; GESAMP, 2015). Hence, further research is needed to assess the biomagnification of these emerging pollutants in the mangrove ecosystem.

Conclusion

Our research reported the first evidence of microplastics in the gills and the digestive tract of the mangrove crab U. occidentalis. The plastic litter in the mangrove and the local markets allowed the presence of microplastics in all organisms. Being the gills the main pathway of microplastics intake in the mangrove crab, accordingly to its retention mechanisms. Although the present study is a baseline for rapid identification of microplastics in the mangrove crab, we suggested that these findings provided more information on the state of contamination as well as food security alert for the local markets of Tumbes city.

Footnotes

Acknowledgements

This study was carried out with the support of Universidad Científica del Sur, Instituto del Mar del Peru (IMARPE) and Universidad Nacional de Tumbes. Special thanks to Dr. Matthew Cole for the language and structure revision, to Dr. Betty Galarreta for the FTIR-MIR-ATR analysis, and to Consorcio Manglares del Noroeste del Peru for the information provided.

Author Contributions

AAS: Conceptualization, software, formal analysis, investigation, data curation, writing-review & editing, visualization. SP: Conceptualization, methodology, validation, resources, supervision, writing-review & editing, visualization. AGI: Conceptuali-zation, validation, resources, supervision, writing-review & editing, visualization.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Research Ethics and Patient Consent

This research was carried out according to an ethic committee “Reglamento del Comite Institucional de ética en investigación con animales y biodiversidad” from the Universidad Científica del Sur.

Clinical Trials

Not applicable

ORCID iDs

Angelica Aguirre-Sanchez

Sara Purca

Aldo G. Indacochea

References

Advíncula

(2017). Variación temporal de la estructura comunitaria de la infauna macrobentónica en los bancos del cangrejo Ucides occidentalis (Ortman, 1987), en los manglares del río Zarumilla, Tumbes, Perú (Tesis para optar el grado académico de Magíster en Ecosistemas y Recursos Acuáticos con mención en Ecosistemas Acuáticos). Universidad Nacional Mayor de San Marcos, Lima, Perú. http://hdl.handle.net/20.500.12816/966

Alemán

Ordinola

(2017). Ampliación de la distribución sur de Ucides occidentalis (Decapoda: Ucididae) y Cardisoma crassum (Decapoda: Gecarcinidae). Revista Peruana de Biología, 24(1), 107–110. https://doi.org/10.15381/rpb.v24i1.13110

Andrade

Ovando

(2017). First record of microplastics in stomach content of the southern king crab Lithodes santolla (Anomura: Lithodidae). Anales del Instituto de la Patagonia, 45(3), 59–65. https://doi.org/10.4067/S0718-686X2017000300059

Andrady

A. L.

(2011). Microplastics in the marine environment. Marine Pollution Bulletin, 62(8), 1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030

Baechler

B. R.

Stienbarger

C. D.

Horn

D. A.

Joseph

Taylor

A. R.

Granek

E. F.

Brander

S. M.

(2020). Microplastic occurrence and effects in commercially harvested North American finfish and shellfish: Current knowledge and future directions. Limnology and Oceanography Letters, 5(1), 113–136. https://doi.org/10.1002/lol2.10122

Barasarathi

Periathamby

Fauziah

S. H.

Emenike

(2014). Microplastic abundance in selected mangrove forest in Malaysia. Proceeding of the ASEAN Conference on Science and Technology, 5(2014), 18–20.

Barboza

L. G. A.

Dick Vethaak

Lavorante

B. R. B. O.

Lundebye

A.-K.

Guilhermino

(2018). Marine microplastic debris: An emerging issue for food security, food safety and human health. Marine Pollution Bulletin, 133, 336–348. https://doi.org/10.1016/j.marpolbul.2018.05.047

Botterell

Z. L. R.

Beaumont

Dorrington

Steinke

Thompson

R. C.

Lindeque

P. K.

(2019). Bioavailability and effects of microplastics on marine zooplankton: A review. Environmental Pollution, 245, 98–110. https://doi.org/10.1016/j.envpol.2018.10.065

Brennecke

Ferreira

E. C.

Costa

T. M.

Appel

da Gama

B. A.

Lenz

(2015). Ingested microplastics (>100 μm) are translocated to organs of the tropical fiddler crab Uca rapax. Marine Pollution Bulletin, 96(1–2), 491–495. https://doi.org/10.1016/j.marpolbul.2015.05.001

10.

Camacho

Herrera

Gómez

Acosta-Dacal

Martínez

Henríquez-Hernández

L. A.

Luzardo

O. P.

(2019). Organic pollutants in marine plastic debris from canary Islands beaches. The Science of the Total Environment, 662(22–31), 22–31. https://doi.org/10.1016/j.scitotenv.2018.12.422

11.

Capparelli

M. V.

Martínez-Colón

Lucas-Solis

Valencia-Castañeda

Celis-Hernández

Ávila

Moulatlet

G. M.

(2022). Can the bioturbation activity of the fiddler crab Minuca rapax modify the distribution of microplastics in sediments? Marine Pollution Bulletin, 180, 113798. https://doi.org/10.1016/j.marpolbul.2022.113798

12.

Carbajal Enzian

Santamaría

. (2017). Guía ilustrada para reconocimiento de crustáceos braquiuros y anomuros con valor comercial del Perú. Boletin Instituto del Mar del Peru 150, 1–22 [online]. Retrieved from: http://biblioimarpe.imarpe.-gob.pe/handle/123456789/3202

13.

Cau

Avio

C. G.

Dessì

Follesa

M. C.

Moccia

Regoli

Pusceddu

(2019). Microplastics in the crustaceans Nephrops norvegicus and Aristeus antennatus: Flagship species for deep-sea environments? Environmental Pollution, 255, 113107. https://doi.org/10.1016/j.envpol.2019.113107

14.

Clark

P. F.

Rainbow

F. S.

Robbins

Smith

Dobson

Byrne

Lowe

Morgan

(1997). The Chinese mitten crab in the Thames catchment. A report for the environment agency (Myles Thomas and Willie Yeomans) in three parts. Part 1 A report for the environment agency. Limnology and Oceanography, 1, 1–75.

15.

Cole

Lindeque

Halsband

Galloway

T. S.

(2011). Microplastics as contaminants in the marine environment: A review. Marine Pollution Bulletin, 62(12), 2588–2597. https://doi.org/10.1016/j.marpolbul.2011.09.025

16.

Coppock

R. L.

Cole

Lindeque

P. K.

Queirós

A. M.

Galloway

T. S.

(2017). A small-scale, portable method for extracting microplastics from marine sediments. Environmental Pollution, 230, 829–837. https://doi.org/10.1016/j.envpol.2017.07.017

17.

Cordova

M. R.

Ulumuddin

Y. I.

Purbonegoro

Shiomoto

(2021). Characterization of microplastics in mangrove sediment of Muara Angke Wildlife Reserve, Indonesia. Marine Pollution Bulletin, 163, 112012–112012. https://doi.org/10.1016/j.marpolbul.2021.112012

18.

Crawford

C. B.

Quinn

(2017). Microplastic pollutants (1st ed.). Elsevier. https://doi.org/10.1016/C2015-0-04315-5

19.

Crooks

Parker

Pernetta

A. P.

(2019). Brain food? Trophic transfer and tissue retention of microplastics by the velvet swimming crab (Necora puber). Journal of Experimental Marine Biology and Ecology, 519, 151187. https://doi.org/10.1016/j.jembe.2019.151187

20.

Dai

Zhang

Zhou

Tian

Chen

Luo

(2018). Ocurrence of microplastic in the water column and sediment in an inland affecting by intensive anthropogenic activities. Environmental Pollution, 242, 1557–1565. https://doi.org/10.1016/j.envpol.2018.07.131

21.

Daniel

D. B.

Ashraf

P. M.

Thomas

S. N.

Thomson

K. T.

(2021). Microplastics in the edible tissues of shellfishes sold for human consumption. Chemosphere, 264(Pt 2), 128554. https://doi.org/10.1016/j.chemosphere.2020.128554

22.

De Frond

Rubinovitz

Rochman

C. M

. (2021). μATR-FTIR spectral libraries of plastic particles (FLOPP and FLOPP-e) for the analysis of Microplastics. Analytical Chemistry, 93(48), 15878–15885.

23.

Dehaut

Cassone

A.-L.

Frère

Hermabessiere

Himber

Rinnert

Rivière

Lambert

Soudant

Huvet

Duflos

Paul-Pont

(2016). Microplastics in seafood: Benchmark protocol for their extraction and characterization. Environmental Pollution, 215, 223–233. https://doi.org/10.1016/j.envpol.2016.05.018

24.

De-la-Torre

G. E.

(2020). Microplastics: An emerging threat to food security and human health. Journal of Food Science and Technology, 57, 1601–1608.

25.

Deng

Feng

Zhao

Sun

(2021). Microplastics pollution in mangrove ecosystems: A critical review of current knowledge and future directions. The Science of the Total Environment, 753, 142041. https://doi.org/10.1016/j.scitotenv.2020.142041

26.

Diele

Koch

(2010). Comparative Population Dynamics and life histories of North Brazilian mangrove crabs, genera uca and Ucides (Ocypodoidea). In Saint-Paul

Schneider

(Eds.), Mangrove dynamics and management in North Brazil. Ecological Studies (vol.211). Springer, Berlin, Heildelberg. pp 275–285.

27.

Engler

R. E.

(2012). The complex interaction between marine debris and toxic chemicals in the Ocean. Environmental Science & Technology, 46(22), 12302–12315. https://doi.org/10.1021/es3027105

28.

Farrell

Nelson

(2013). Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environmental Pollution, 177, 1–3. https://doi.org/10.1016/j.envpol.2013.01.046

29.

Forgeron

S. J.

Quadros

A. F.

Zimmer

(2021). Crab-driven processing does not explain leaf litter-deposition in mangrove crab burrows. Ecology and Evolution, 11, 8856–8862. https://doi.org/10.1002/ece3.77182021.

30.

Garcés-Ordóñez

Olaya

Granados

Blandón Garcia

Espinosa

. (2019). Marine litter and microplastic pollution on mangrove soils of the Ciénaga Grande de Santa Marta, Colombian Caribbean. Marine Pollution Bulletin, 145, 455–462. https://doi.org/10.1016/j.marpolbul.2019.06.058

31.

GESAMP. (2015). “Sources, fate and effects of microplastics in the marine environment: A global assessment”. ( Kershaw

P. J.

, ed.) (IMO/FAO/UNESCO-IOC/UNIDO/WMO/IAEA/UN/UNEP/UNDP Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection). Rep. Stud. GESAMP, No. 90, p.96.

32.

Guaman Quishpi

F. M.

Renteria Minuchi

. (2012). Estudio de la calidad microbiologíca y organoleptíca de pulpa de cangrejo rojo Ucides occidentalis bachelor thesis. Universidad Técnica de Machala. Ecuador.

33.

Holguin

Bashan

(2007). La importancia de los manglares y su microbiología para el sostenimiento de las pesquerías costeras. In: Ferrera-Cerrato, R., & Alarcon, A. (eds.) Microbiología agrícola: Hongos, bacterias, micro y macrofauna, control biológico, planta organismo. México City, México, Editorial Trillas, pp. 239–252.

34.

Hopper

B. E.

Fell

J. W.

Cefalu

R., C

. (1973). Effect of temperature on life cycles of nematodes associated with the mangrove (Rhizophora mangle) detrital system. Marine Biology, 23(4), 293–296. https://doi.org/10.1007/bf00389336

35.

Horn

D. A.

Granek

E. F.

Steele

C. L.

(2020). Effects of environmentally relevant concentrations of microplastic fibers on Pacific mole crab (Emerita analoga) mortality and reproduction. Limnology and Oceanography Letters, 5(1), 74–83. https://doi.org/10.1002/lol2.10137

36.

INRENA. (2007). Plan Maestro del Santuario Nacional Los Manglares de Tumbes 2007-2011. Lima.

37.

Jambeck

J. R.

Geyer

Wilcox

Siegler

T. R.

Perryman

Andrady

Narayan

Law

K. L.

(2015). Marine pollution. Plastic waste inputs from land into the ocean. Science, 347(6223), 768–771. https://doi.org/10.1126/science.1260352

38.

Jiang

Zhao

Zhu

(2018). Microplastic-associated bacterial assemblages in the intertidal zone of the Yangtze Estuary. The Science of the Total Environment, 624, 48–54. https://doi.org/10.1016/j.scitotenv.2017.12.105

39.

Jones

J. I.

Vdovchenko

Cooling

Murphy

J. F.

Arnold

Pretty

J. L.

Spencer

K. L.

Markus

A. A.

Vethaak

A. D.

Resmini

(2020). Systematic analysis of the relative abundance of polymers occurring as microplastics in freshwaters and estuaries. International Journal of Environmental Research and Public Health, 17(24), 9304. https://doi.org/10.3390/ijerph17249304

40.

Knapik

L. F. O.

Ramsdorf

(2020). Ecotoxicity of malathion pesticide and its genotoxic efects over the biomarker comet assay in Daphnia magna. Environmental Monitoring and Assessment, 192(5), 1–9. https://doi.org/10.1007/s10661-020-8235-0

41.

Kooi

Nes

E. H.

Scheffer

Koelmans

A. A.

(2017). Ups and downs in the ocean: Effects of biofouling on vertical transport of microplastics. Environmental Science & Technology, 51(14), 7963–7971. https://doi.org/10.1021/acs.est.6b04702

42.

Kovač Viršek

Palatinus

Koren

Š.

Peterlin

Horvat

Kržan

. (2016). Protocol for microplastics sampling on the sea surface and sample analysis. Journal of Visualized Experiments: JoVE, 118, e55161. https://doi.org/10.3791/55161

43.

Lebreton

L. C. M.

Van Der Zwet

Damsteeg

J.-W.

SLat

Andrady

Reisser

(2017). River plastic emissions to the world’s oceans. Nature Communications, 8(1), 15611. https://doi.org/10.1038/ncomms15611

44.

H.-X.

L.-S.

Lin

Z.-X.

X.-R.

Shi

H.-H.

Yan

Zheng

G.-M.

Rittschof

(2018). Microplastics in oysters Saccostrea cucullata along the Pearl River estuary, China. Environmental Pollution (Barking, Essex: 1987), 236, 619–625. https://doi.org/10.1016/j.envpol.2018.01.083

45.

Yang

Jabeen

Shi

(2015). Microplastics in commercial bivalves from China. Environmental Pollution, 207, 190–195. https://doi.org/10.1016/j.envpol.2015.09.018

46.

Zhang

Xue

Wang

(2019). Abundance and characteristics of microplastics in the mangrove sediment of the semi-enclosed Maowei Sea of the south China sea: New implications for location, rhizosphere, and sediment compositions. Environmental Pollution (Barking, Essex), 244, 685–692. https://doi.org/10.1016/j.envpol.2018.10.0891987.

47.

Maghsodian

Sanati

A. M.

Tahmasebi

Shahriari

M. H.

Ramavandi

(2022). Study of microplastics pollution in sediments and organisms in mangrove forests: A review. Environmental Research, 208, 112725–112725. https://doi.org/10.1016/j.envres.2022.112725

48.

Martin

Almahasheer

Duarte

C. M.

(2019). Mangrove forests as traps for marine litter. Environmental Pollution, 247, 499–508. https://doi.org/10.1016/j.envpol.2019.01.067

49.

McGaw

I. J.

Curtis

D. L.

(2013). A review of gastric processing in decapod crustaceans. Journal of Comparative Physiology B: Biochemical, systemic, and environmental physiology, 183(4), 443–465. https://doi.org/10.1007/s00360-012-0730-3

50.

McGoran

A. R.

Clark

P. F.

Smith

B. D.

Morritt

(2020). High prevalence of plastic ingestion by Eriocheir sinensis and Carcinus maenas (Crustacea: Decapoda: Brachyura) in the Thames Estuary. Environmental Pollution, 265, 114972. https://doi.org/10.1016/j.envpol.2020.114972

51.

Miller

D. C.

(1961). The feeding mechanism of fddler crabs, with ecological considerations of feeding adaptations. Zoologica, 46, 80–101.

52.

Moroyoqui-Rojo

Flores-Verdugo

Escobedo-Urias

D. C.

Flores-De-Santiago

González-Farías

(2015). Uso potencial de dos especies de mangle subtropical (Laguncularia racemosa y Rhizophora mangle) para la remoción de nutrientes en sistemas de recirculación cerrados. Ciencias Marinas, 41(4), 255–268. https://doi.org/10.7773/cm.v41i4.2521

53.

Naji

Nuri

Vethaak

A. D.

(2018). Microplastics contamination in molluscs from the northern part of the Persian Gulf. Environmental Pollution, 235, 113–120. https://doi.org/10.1016/j.envpol.2017.12.046

54.

Nordhaus

Wolff

(2007). Feeding ecology of the mangrove crab Ucides cordatus ( Ocypodidae ): Food choice, food quality and assimilation efficiency. Marine Biology, 151(5), 1665–1681.

55.

Nordhaus

Salewski

Jennerjahn

T.C.

(2011). Food preferences of mangrove crabs related to leaf nitrogen compounds in the Segara Anakan Lagoon, Java, Indonesia. Journal of Sea Research, 65(4), 414–426. https://doi.org/10.1016/j.seares.2011.03.006

56.

Nor

N. H.

Obbard

J. P.

(2014). Microplastics in Singapore’s coastal mangrove ecosystems. Marine Pollution Bulletin, 79, 278–283. https://doi.org/10.1016/j.marpolbul.2013.11.025

57.

Not

Lui

C. Y. I.

Cannicci

(2020). Feeding behavior is the main driver for microparticle intake in mangrove crabs. Limnology and Oceanography Letters, 5(1), 84–91. https://doi.org/10.1002/lol2.10143

58.

Ordinola

Alemán

Montero

(2013). Biología y pesquería de cuatro especies de invertebrados marinos de importancia comercial. Región Tumbes, II etapa -2007, 40, 21. Inf Inst Mar Perú, Vol. 40 / Nos. 3-4 / Julio-Diciembre 2013.

59.

Origin(Pro). (2022). Version 2022b. OriginLab Corporation. https://www.originlab.com/2022b

60.

Ory

Chagnon

Felix

Fernández

Ferreira

J. L.

Gallardo

Garcés-Ordóñez

Henostroza

Laaz

Mizraji

Mojica

Murillo Haro

Ossa Medina

Preciado

Sobral

Urbina

M. A.

Thiel

(2018). Low prevalence of microplastic contamination in planktivorous fish species from the southeast Pacific Ocean. Marine Pollution Bulletin, 127, 211–216. https://doi.org/10.1016/j.marpolbul.2017.12.016

61.

Ory

N. C.

Sobral

Ferreira

J. L.

Thiel

(2017). Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island) in the South Pacific subtropical gyre. The Science of the Total Environment, 586, 430–437. https://doi.org/10.1016/j.scitotenv.2017.01.175

62.

Pannetier

Morin

Le Bihanic

Dubreil

Clérandeau

Chouvellon

Van Arkel

Danion

Cachot

(2020). Environmental samples of microplastics induce significant toxic effects in fish larvae. Environment International, 134, 105047. https://doi.org/10.1016/j.envint.2019.105047

63.

Patria

Santoso

Hanifah

(2020). Microplastic ingestion by periwinkle snail Littoraria scabra and mangrove crab Metopograpsus quadridentata in Pramuka Island (Vol.49, pp. 2151–2158). Pramuka Island, Jakarta Bay, Indonesia.

64.

Pauna

V. H.

Buonocore

Renzi

Russo

G. F.

Franzese

P. P.

(2019). The issue of microplastics in marine ecosystems: A bibliometric network analysis. Marine Pollution Bulletin, 149, 110612. https://doi.orssssssg/10.1016/j.marpolbul.2019.110612

65.

Plee

T. A.

Pomory

C. M.

(2020). Microplastics in sandy environments in the Florida Keys and the panhandle of Florida, and the ingestion by sea cucumbers (Echinodermata: Holothuroidea) and sand dollars (Echinodermata: Echinoidea). Marine Pollution Bulletin, 158, 111437. https://doi.org/10.1016/j.marpolbul.2020.111437

66.

PNIPA. (2018). Desarrollo de metodologías de producción de semillas de cangrejo de manglar (Ucides occidentalis) con fines de repoblamiento en el Santuario Nacional los Manglares de Tumbes y su zona de amortiguamiento, distrito y provincia de Zarumilla, Tumbes cofinanciado por el Programa Nacional de Innovación en Pesca y Acuicultura (PNIPA). Report: PNIPA-PES-SIADE-PP-000031-2018-LB-01

67.

Provencher

J. F.

Vermaire

J. C.

Avery-Gomm

Braune

B. M.

Mallory

M. L.

(2018). Garbage in guano? Microplastic debris found in faecal precursors of seabirds known to ingest plastics. The Science of the Total Environment, 644, 1477–1484. https://doi.org/10.1016/j.scitotenv.2018.07.101

68.

R Core Team. (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/

69.

Rochman

C. M.

(2015). The complex mixture, fate and toxicity of chemicals associated with plastic debris in the marine environment. In Bergmann

Gutow

Klages

(Eds.), Marine anthropogenic litter (1st ed., pp. 117–140). Springer.

70.

Rodríguez-Seijo

Pereira

(2017). Morphological and physical characterization of microplastics. Comprehensive Analytical Chemistry, 75, 49–66. https://doi.org/10.1016/bs.coac.2016.10.007

71.

Rotjan

R. D.

Sharp

K. H.

Gauthier

A. E.

Yelton

Lopez

E. M.

Carilli

Kagan

J. C.

Urban-Rich

(2019). Patterns, dynamics and consequences of microplastic ingestion by the temperate coral, Astrangia poculata. Proceedings of the Royal Society B Biological Sciences, 286(1905), 20190726. https://doi.org/10.1098/rspb.2019.0726

72.

Smith

Love

D. C.

Rochman

C. M.

Neff

R. A.

(2018). Microplastics in seafood and the implications for human health. Current Environmental Health Reports, 5(3), 375–386. https://doi.org/10.1007/s40572-018-0206-z

73.

Solano

Moreno

(2009). Cangrejo rojo (Ucides occidentalis) un análisis durante el periodo de veda reproductiva, 2009. Boletín Científico y Técnico, 20(3), 37–45.

74.

SUNASS (Superintendencia Nacional de Servicios de Saneamiento). (2010). Plan Maestro optimizado de la empresa prestadora de servicios de Saneamiento S.A para el periodo 2010-2039. Recuperado 13 de noviembre de 2019, de SUNASS website: https://www.sunass.gob.pe/websunass/

75.

Syakti

A. D.

Bouhroum

Hidayati

N. V.

Koenawan

C. J.

Boulkamh

Sulistyo

Lebarillier

Akhlus

Doumenq

Wong-Wah-Chung

P., P

. (2017). Beach macro-litter monitoring and floating microplastic in a coastal area of Indonesia. Marine Pollution Bulletin, 122(1), 217–225. https://doi.org/10.1016/j.marpolbul.2017.06.046

76.

Thiel

Luna-Jorquera

Alvarez-Varas

Gallardo

Hinojosa

Luna Bravo

Miranda-Urbina

Morales

Ory

Pacheco

Portflitt Toro

Zavalaga

(2018). Impacts of marine plastic pollution from continental coasts to subtropical Gyres—Fish, seabirds, and other vertebrates in the SE Pacific. Frontiers in Marine Science, 5 (2018), 238. https://doi.org/10.3389/fmars.2018.00238

77.

Torn

(2020). Microplastics uptake and accumulation in the digestive system of the mud crab Rhithropanopeus harrisii. Proceedings of the Estonian Academy of Sciences, 69(1), 35. https://doi.org/10.3176/proc.2020.1.04

78.

Villagran

D. M.

Truchet

D. M.

Buzzi

N. S.

Forero Lopez

A. D.

Fernández Severini

M. D.

(2020). A baseline study of microplastics in the burrowing crab (Neohelice granulata) from a temperate southwestern Atlantic estuary. Marine Pollution Bulletin, 150, 110686. https://doi.org/10.1016/j.marpolbul.2019.110686

79.

Villegas

Cabrera

Capparelli

M. V.

(2021). Assessment of microplastic and organophosphate pesticides contamination in fiddler crabs from a ramsar site in the estuary of Guayas River, Ecuador. Bulletin of Environmental Contamination and Toxicology, 107, 20–28. https://doi.org/10.1007/s00128-021-03238-z

80.

Waddell

E. N.

Lascelles

Conkle

J. L.

(2020). Microplastic contamination in Corpus Christi Bay blue crabs, Callinectes sapidus. Limnology and Oceanography Letters, 5(1), 92–102. https://doi.org/10.1002/lol2.10142

81.

Waite

H. R.

Donnelly

M. J.

Walters

L. J.

(2018). Quantity and types of microplastics in the organic tissues of the eastern oyster Crassostrea virginica and Atlantic mud crab Panopeus herbstii from a Florida estuary. Marine Pollution Bulletin, 129(1), 179–185. https://doi.org/10.1016/j.marpolbul.2018.02.026

82.

Walkinshaw

Lindeque

P. K.

Thompson

Tolhurst

Cole

(2020). Microplastics and seafood: Lower trophic organisms at highest risk of contamination. Ecotoxicology and Environmental Safety, 190, 110066. https://doi.org/10.1016/j.ecoenv.2019.110066

83.

Watts

A. J. R.

Lewis

Goodhead

R. M.

Beckett

S. J.

Moger

Tyler

C. R.

Galloway

T. S.

(2014). Uptake and retention of microplastics by the Shore Crab Carcinus maenas. Environmental Science & Technology, 48(15), 8823–8830. https://doi.org/10.1021/es501090e

84.

Wright

S. L.

Kelly

F. J.

(2017). Plastic and human health: A micro issue? Environmental Science & Technology, 51(12), 6634–6647. https://doi.org/10.1021/acs.est.7b00423

85.

Yin

C. S.

Chai

Y. J.

Danielle

Yusri

Gallagher

J. B.

, (2020). Anthropogenic marine debris and its dynamics across peri-urban and urban mangroves on Penang Island, Malaysia. Journal of Sustainability Science and Management, vol. 15 (6), 36–60. https://doi.org/10.46754/jssm.2020.08.004

86.

Y. Z.

Azman

Primus

Said

M. I. M.

Abideen

M. Z.

(2021). Microplastic ingestion by crabs. In Abang

D. Z.

Mazlan

A. N.

Abd

N. H.

Haniffah

M. R. M.

Zardasti

Annammala

K. V.

Mohamed

M. Z.

Mohd

M. N.

Hafizi

(Eds.), The 6th proceeding of Civil Engineering. School of Civil Engineering (pp. 363–375). Universiti Teknologi Malaysia. https://www.researchgate.net/publication/359481086

87.

Zambrano

Galindo-Cortes

Aragón-Noriega

E. A.

(2018). Comparison of growth pattern of male Ucides occidentalis (Ortmann, 1897)(Brachyura: Ocypodidae) based on a combination of commercial catches and non-commercial data. Journal of Crustacean Biology, 38(4), 429–434. https://doi.org/10.1093/jcbiol/rux105

88.

Zambrano

Meiners

(2018). Notas sobre taxonomía, biología y pesquería de Ucides occidentalis (Brachyura: Ocypodidae) con énfasis en el Golfo de Guayaquil, Ecuador. Revista peruana de Biología, 25(1), 055–066. https://doi.org/10.15381/rpb.v25i1.13821

89.

Zhang

Wang

Sun

Pan

Zhou

Xie

Wang

Zou

(2020a). Microplastic pollution in surface water from east coastal areas of Guangdong, South China and preliminary study on microplastics biomonitoring using two marine fish. Chemosphere, 256 (2020), 1272202. https://doi.org/10.1016/j.chemosphere.2020.127202

90.

Zhang

Guo

Wang

(2020b). Dynamic distribution of microplastics in mangrove sediments in Beibu Gulf, South China: implications of tidal current velocity and tidal range. Journal of Hazardous Materials, 399(4),122849. https://doi.org/10.1016/j.jhazmat.2020.122849

91.

Zhang

Sun

Liu

(2021). Full size microplastics in crab and fish collected from the mangrove wetland of Beibu Gulf: Evidences from Raman tweezers (1-20 μm) and spectroscopy (20-5000 μm). The Science of the Total Environment, 759, 143504. https://doi.org/10.1016/j.scitotenv.2020.143504

92.

Zhu

Zhang

Tan

Yang

Wang

(2019). Cetaceans and microplastics: First report of microplastic ingestion by a coastal delphinid, Sousa chinensis. The Science of the Total Environment, 659, 649–654. https://doi.org/10.1016/j.scitotenv.2018.12.389

Microplastic Presence in the Mangrove Crab Ucides occidentalis (Brachyura: Ocypodidae) (Ortmann,1897) Derived From Local Markets in Tumbes,Peru

Abstract

Keywords

Background

Methods

Sample site

Quality assurance

Soft tissue digestion

Filtration and Characterization

FTIR-ATR analysis

Statistical analysis

Results

Discussion

Gills as a mode of uptake

Digestive gland as a mode of uptake

Types of microplastics found

Crab health and food security

Conclusion

Footnotes

Acknowledgements

Author Contributions

Declaration of Conflicting Interests

Funding

Research Ethics and Patient Consent

Clinical Trials

ORCID iDs

References