Histological characterization and morphological alterations in gill and digestive gland in non-native bivalve from the Province of Buenos Aires: spatial and seasonal evaluation

doi:10.21203/rs.3.rs-3126138/v1

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Histological characterization and morphological alterations in gill and digestive gland in non-native bivalve from the Province of Buenos Aires: spatial and seasonal evaluation

https://doi.org/10.21203/rs.3.rs-3126138/v1

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The objective of this study was to characterize and evaluate morphological alterations and cell and tissue composition of the gill and digestive gland in Magallana gigasfrom urbanized areas with different degrees of human activity over one year. For that, the height of the plicas and filaments of the gill and the tubule epithelium area were measured, the ratio of cell-type and tissue composition analyzed of the digestive gland as well as alterations in the pattern of structural organization in these organs were assessed. The specimens were collected in November 2021, and February, May and August 2022 from two representative sampling sites of distinct anthropic pressures in the coastal area of Buenos Aires Province: Arroyo Parejas (AP, 38° 55’ S, 62° 04’ W) and Pehuén-Có (PC, 39° 01’ S; 61° 32’ W). The results of the morphological parameters, ratio of cell-type, tissue composition and histological alterations of Magallana gigas showed difference between the studied urbanized areas and seasons, suggesting a negative relationship between intense human activity and the health of the gills and digestive gland of the Pacific oyster. Understanding the gill and digestive gland morphology of Pacific oysters, as well as their response to varying levels of human activity in the study region, could help mitigate the impacts of this non-native species.

Biomarkers

Crassostrea

Invasive

Pacific oyster

South Atlantic

Anthropogenic activities have caused a significant increase in pollution levels in the marine environment globally, which poses a serious threat to the biodiversity of marine ecosystems (Rivadeneira et al. 2013). The harmful effects of this pollution are numerous, including multiple toxic effects in exposed organisms. This may cause a variety of physiological and morphological alterations in animals, including changes to organ morphology and functionality. There is an international inclination of complementing chemical analysis with the appropriate use of “biomarkers-species” (Arrighetti et al. 2019). Biomarkers provide valuable insight into the presence of pollutants in the environment by measuring molecular, cellular, and tissue levels responses in sentinel organisms (Au 2004; Aarab et al. 2008; Aarab et al. 2011; Izagirre et al. 2014). Bivalves are widely used as sentinel species in environmental monitoring programs due to their wide distribution, sedentary lifestyle, and tolerance to a large range of environmental conditions. In addition, their feeding habit, filter feeders, allow them to accumulate and reflect the levels of contaminants in the environment (Au 2004; Lowe et al. 2006).

The Pacific oyster Magallana gigas (Thunberg 1793), also known as Crassostrea gigas, is native to Southeast Asia and it is one of the most commercialized species in the world (FAO 2023). In 2020, the world production of this oyster was more than 600,000 tonnes and the majority of global production was in China (FAO 2023). The transfers of marine organisms by seafaring plus the high ability to adapt to various environmental conditions (tolerant to high temperature and salinity variations), allow this specie to establish and spread outside of cultivation farms (Miossec et al. 2009). Besides that, they have the potential to displace native species and modify habitats and ecosystems (Herbert et al. 2016). M. gigas have been introduced in many countries outside their native range, resulting from aquaculture (Ruesink et al. 2005). In Argentina, this species was introduced in Bahía Anegada (Buenos Aires Province) for aquaculture in 1982 (Orensanz et al. 2002). Since then, it has expanded its distribution area in the last decade to estuarine systems and beaches as well as highly urbanized, industrialized and tourist areas (Dos Santos and Fiori 2010). The concentration of contaminants in filter-feeding can indicate the consumption risks as well as the health of coastal waters, thus, the broad spread of the Pacific oyster and its popularity as a food make it a useful sentinel (Talley et al. 2022).

As a well-established and sensitive biomarker of stress, changes in the morphological parameters in the gill and digestive gland of bivalves have been used to investigate the effect of the contaminants (Bignell et al. 2011; Nogarol et al. 2016; Arrighetti et al. 2019). Gills play an important role in the feeding process and it is the main entry of pollutants into the body of bivalves (Arrighetti et al. 2019). Oyster gills consist of two V-shaped demi-branches in which each is composed of an ascending and a descending lamella linked by interlamellar junctions. Each lamella is composed of a sequence of folded structures, called plicas, which are made of a succession of tubular structural units called filaments (Jemaà et al. 2014). The development of both right and left gills is symmetrical, via a cavitation–extension process from the gill buds (Cannuel and Beninger 2006).

The digestive gland is considered the center of metabolic regulation, acting in the process of immunological defense and homeostatic regulation of the internal medium, and also in the detoxification and elimination process of xenobiotics (Moore and Allen 2002). The digestive epithelium consists of two main cell types, digestive and basophilic cells. The basophilic cells are secretory cells that contribute to extracellular digestion and metabolic regulation and the role of the digestive cells is intercellular food digestion (Marigómez et al. 1998). Usually, digestive cells are much more abundant than basophilic cells; however, under conditions of exposure to pollutants, an increase in the numbers of basophilic cells and alterations of the epithelium area can occur (Zaldibar et al. 2007; Marigómez et al. 2006; Arrighetti et al. 2019).

Exposure to pollutants in the marine environment can influence the morphology of the gills and digestive tubules as size, shape, area, and cell type composition of the epithelium. In this way, this study aims to characterize and evaluate morphological alterations in the gill and digestive gland in M. gigas oysters through the morphometric analysis of these organs from urbanized areas with different degrees of human activity - harbors and tourist zones along the one year. Thus, we expect to observe a larger size of the filaments and plica of gills as well as a smaller tubule epithelium area and more basophilic cells of the digestive tubules in oysters under more human activity than less human activity. Also, we expect to observe a variability of these morphological parameters along seasons. Understanding the gill and digestive gland morphology of Pacific oysters, as well as their response to varying levels of human activity in the study region, could help mitigate the impacts of this non-native species.

2.1. Study areas and oyster collection

The study area is located in the southwest of Buenos Aires Province, Argentina and includes two representative sampling sites with distinct anthropic pressures: Arroyo Parejas (AP, 38° 55’ S, 62° 04’ W) and Pehuén-Có (PC, 39° 01’ S; 61° 32’ W) (Fig. 1). AP is a protected area located in Bahía Blanca Estuary (BBE) that receives significant pressure from ports activities and chemical industries, and it is located next to an oil pumping and shipping plant (Tombesi et al. 2018; Quintas et al. 2019; Fiori et al. 2020). The BBE is a mesotidal coastal plain estuary that extends over approximately 2300 km² and is formed by several tidal channels, extensive tidal flats with patches of low salt marshes, and islands (Piccolo et al. 2008). This area has significant industrial activity and is considered one of the main agricultural export zones in the country. It also has a complex port system as a military base (Base Naval Puerto Belgrano) as well as a commercial harbor, which receives large vessels for navigation (Puerto Rosales) (Melo 2021). Thus, this coastal area is in a periodic activity of dredging with the removal of bottom sediments that can carry contaminants and potentially impact the local marine fauna. In addition, this area also receives urban waste without treatment, from nearby cities, such as Bahía Blanca (with a population of 335,190 INDEC 2021), and Punta Alta (with a population of 60,943 INDEC 2021). Heavy metals, organochlorine pesticides and organotin compounds were detected in surface water, sediment and soil in the study area and surroundings (Botté et al. 2007; Botté et al. 2010; Tombesi et al. 2018; Quintas et al. 2019; Fiori et al. 2020). PC is primarily a tourist destination, which has a permanent population of 681 inhabitants according to the National Institute of Statistics and Census of Argentina (INDEC 2021), and experiences significant anthropogenic pressure during the summer season due to the influx of approximately 600,000 visitors between December and March. Besides that, PC is exposed to the direct action of the waves, backed by extensive dunes (Carcedo et al. 2017). It is situated approximately 80 km from the innermost zone of the BBE. Both sampling sites are connected by an estuarine plume that acts as the main source of turbidity and suspended sediment that is diluted towards the adjacent beaches. The influence of the estuarine plume also causes a rise in the temperature of the coastal water up to the Pehuén-Có beach (Delgado et al. 2016).

Magallana gigas oysters were collected in November 2021, and February, May and August 2022 at AP and PC sites. In each sampling site, the oysters were manually collected from intertidal zones during the lowest tide. The oyster samplings were transported to the laboratory in polyethylene bags and immediately preserved at -20°C. After, the samplings were fixed in formaldehyde (4%) for 24 h at 4°C and subsequently stored in 70% ethanol. Each specimen had its shell measured using a caliper, opened using a knife and the soft tissue was removed with a scalper for the histological and morphometric analysis.

2.2. Histological procedure

Ten adult specimens of M. gigas from each sampling site and seasons were randomly selected for the histological procedure. A cross-section was cut from each individual's gills and digestive gland, always in the same place on the body. Posteriorly, the gills and digestive gland tissue were dehydrated using an ascending series of ethanol concentrations and then embedded in paraffin. Sections were cut at 7 µm with a rotary motorized microtome (Leica RM 2155). The tissue sections were stained with hematoxylin-eosin to identify the nucleus and cytoplasm components. Also, alcian blue and periodic acid of Schiff histochemical techniques were applied to verify the chemical composition of tissue as acid and neutral polysaccharidae, respectively. The tissue sections were observed with a Zeiss Axiostar microscope, integrated into a Canon PowerShot G-10 digital camera and all image analyses to obtain morphometric parameters were recorded with Axiovision Rel 4.4.

2.3. Morphometric analysis of gill and digestive gland epithelium

The shifts in shape and size of the gill and digestive gland structures that may occur in response to pollutants were quantified using 3 morphometric parameters. With the aid of an image analyzer program (Axiovision Rel 4.4), the height of the plicas and filaments of the gill and the tubule epithelium area was measured for each M. gigas specimen. Both gill measurements were taken from the upper to down region. A total of 5 plicas per individual (400) and 6 filaments (3 from the upper zone and 3 from the middle zone) per plica (2400; 30 per individual) were obtained. For the digestive gland, the tubule epithelium area was taken by the difference between the total epithelial area and the digestive lumen area. A total of 20 tubular profiles per individual (1600) were analyzed.

2.4. Gill and digestive gland histological alterations

Tissue sections stained with hematoxylin-eosin, alcian blue and periodic acid of Schiff were used to evaluate possible histological alterations in the gill and digestive gland of M. gigas. The condition of the gill tissue was assessed by the alterations in the pattern of structural organization of the plica and fusion of the filaments. The condition of the digestive gland was assessed by the presence of tubule necrosis and the alterations in the pattern of structural organization of digestive and basophilic cells. Also, the volume density of basophilic cells (VvBas) and the connective-to-diverticula ratio (CTD) were determined by the STEPanizer software (Tschanz et al. 2011) in order to evaluate the cell-type replacement occurred and the integrity of the digestive gland, respectively. For the both, a test system with 100 points was used for each histological image, in which the number of points hitting a basophilic cell (b), a digestive cell (d), (l) diverticular lumen and (c) interstitial connective tissue were counted and related by: VvBas = b/(d + b) and CTD ratio = c/(b + d + l). Cells and tissues counted were made in 3 fields per oyster (5 oysters per sampling site/season) at 400× magnification.

2.5. Data analysis

In order to evaluate the influence by of the different degrees of human activity in the morphology of gills and digestive glands, test t was performed to compare the mean values of the morphometric parameters (e.g., height of plica and filaments of gill and tubule epithelium area of the digestive gland) and the between sampling sites. The same statistical test was applied to compare the cell type composition and tissue integrity between sampling sites. Analysis of variance (one-way ANOVA) followed by a Tukey-HSD post-hoc was performed to compare the mean values of the morphometric parameters and the cell type composition and tissue integrity among seasons. Previously, the data were tested for normality with the Shapiro-Wilk test and homogeneity of variance was assessed through the Levene test. A value of p ≤ 0.05 was regarded as statistically significant. All statistical analyses were performed using the Software R (v. 3.4.3, R Core Team 2017).

3.1. Morphometric analysis of gill and digestive gland epithelium

Concerning the alterations in the morphometric parameters for the oysters by sampling sites, a significant difference between the height of gill filaments was observed (t = -11.067, p < 0.05), being greater in AP than PC. Still in the gills, no significant difference was observed between the height of the plicas and sampling sites (t = 1.0199, p = 0.3084). The tubule epithelium area of the digestive gland was significantly different (t = 4.5713, p < 0.05), being greater in PC than in AP. Regarding the seasons, the morphological parameters showed variability and significant differences over time (filament, F = 106.41, p < 0.05; plica, F = 13.88, p < 0.05; digestive gland, F = 99.510, p < 0.05). In general, the values observed for gills decreased from winter to autumn (Fig. 2A, B), and the opposite for the values of the digestive gland, which increased from winter to autumn (Fig. 2C).

3.2. Gill and digestive gland histological alterations

In general, tissue organization and size and type of cells in the gill and digestive gland were different between individuals at the sampling sites (Fig. 3A, B; 4A, B) and there was no macro and microscopic evidence of pathogens, including bacteria, protozoans and metazoans. In relation to the gill, alteration of the pattern of structural organization and size of the plica (although it was not significantly different) and fusion of the frontal and abfrontal filaments as well as irregular folders structure were observed with more frequency in AP (Fig. 3C, D) than PC (Fig. 3E, F). For the digestive gland, a narrow cell layer with atrophied digestive tubules characterized by a reduction of the epithelial cell thickness as well as an enlargement of the lumen were observed in PA individuals (Fig. 4C). In contrast, the relationship between basophilic and digestive cells showed a similar proportion in PC oysters (Fig. 4F). The VvBas and CTD ratio results were also significantly different between sampling sites, which both value parameters were higher in oysters from AP compared to oysters from PC (VvBas, t = 12.336, p < 0.05; CTD ratio, t = 5.4903, p < 0.05). In both organs, the presence of acid and neutral polysaccharidae was greater and more distributed in tissue from AP. Regarding the seasons, VvBas was significantly higher in winter than the other seasons for both sampling sites (AP, F = 5.782, p < 0.05; PC, F = 9.964, p < 0.05) (Fig. 5A). The CTD ratio was significantly higher in the summer than the other seasons for oysters from AP and a significant difference was observed in the CTD ratio between winter and spring for oysters from PC, with higher values in the spring (Fig. 5B).

The results of the morphological parameters, ratio of cell-type, tissue composition and histological alterations of M. gigas showed a difference between the studied urbanized areas and the no evidence of the pathogens in the organs studied suggest a negative relationship between intense human activity and the health of the gills and digestive gland of the Pacific oyster.

The histological and morphological alterations in tissues are a useful tool for evaluating the ecosystem’s health status (Au 2004). These tissue alterations can reflect disturbances at lower biological organization levels (e.g., molecular and cellular) and may persist even after the cessation of the pollutant inputs (Garmendia et al. 2011). In this study, morphological alterations were more prominent in the oyster gills of AP individuals suggesting that anthropic activity is more intense in this site than in PC. The highest size of filaments, fusion of filaments, irregular folder structure, and disorganization of the gill pattern of the individuals from PA can be associated with stress factors and constant pollutant inputs from the intense activities of the harbors activity and the discharges of sewage waters at this site. The morphological alterations such as those reported here and hyperplasia and increased mucous secretory activity can decrease gas exchange efficiency on gills and can be associated with the proliferation of mucocytes, suggesting stress response to contaminants’ presence (Valdez Domingos et al. 2007). AP is located near one of the most urbanized and industrialized coastal areas of Argentina (Arias et al. 2010) and has suffered several anthropic perturbations as a consequence of growing industrial activity and demographic expansion (Botté et al. 2007; Botté et al. 2010). A greater exposure to metals in AP than PC has been suggested, since a decreasing trend in the content of some metals in the body of M. gigas was reported from within the BBE towards adjacent beaches (Colla et al. 2018). As here, Zanette et al. (2006) observed an increase in the presence of morphological changes in the gills of Crassostrea rhizophorae with an increase in sources of pollution by human activity. Similar results were observed in oyster gills exposed in the presence of different pollutants as field works with Crassostrea sp. exposed to high values of heavy metals in estuarine harbor regions (Noleto et al. 2021)d rhizophorae exposed to areas impacted by anthropogenic activities (Valdez Domingos et al. 2007), as well as, experiment works with Crassostrea angulata exposed to a higher concentration of copper (Rodríguez-Rúa et al. 2005)d gigas exposed to a toxic dinoflagellate diet (Noleto et al. 2021). Also, similar gills alterations were observed in mussels Brachidontes rodriguezii from harbor areas of Buenos Aires Province (Arrighetti et al. 2019).

The morphology of the digestive gland and its cellular composition are other parameters that can be used to assess the environmental status and can aid in understanding the impact of stress factors (Aarab et al. 2008). In this work, the tubule epithelium area of the digestive gland was smaller in individuals from AP when compared to individuals from PC. The opposite was observed in the cell-type composition and the integrity of the digestive gland tissue measured by VvBas and CTD ratio that were higher in AP. Atrophied digestive tubules characterized by an enlargement of the lumen and a reduction of the epithelial cell thickness were also observed in individuals from AP. These results could indicate higher cellular activity due to stress factors and/or pollutants found in this study region, corroborating that human activity is more intense in AP. Morphological alterations in the digestive glands similar to those observed in this study were also found in field oysters such as M. gigas, Magallana angulate (Pires et al. 2022) and Magallana bilineata (Joshy et al. 2022) as well as in the experiment works with antifouling biocide and toxic metals in Crassostrea brasiliana and M. gigas, respectively (Campos et al. 2022; Rementeria et al. 2016; Rementeria et al. 2017). Similar results were also observed in mytilid bivalves close to anthropized areas and under the port influence (Da Ros et al. 2000; Arrighetti et al. 2019; Aarab et al. 2011; Bignell et al. 2011; Sabatini et al. 2023). The change of the cell-type, also called cell-type replacement and the integrity of the digestive gland tissue, possibly occur through a loss of digestive cells and hypertrophy of basophilic cells (Marigómez et al. 2006; Zaldibar et al. 2007) and the extent of the interstitial connective tissue, can provoke disturbance in the metabolisms, accumulation of xenobiotics and in the food digestion (Marigómez et al. 1998). In reference sites, the VvBas of mussels is normally < 0.1µ³/µ³, but on exposure to pollutants the value of this parameter may reach about 0.2µ³/µ³ (Cajaraville et al. 1992). In this study, the values of the VvBas were ≥ 0.5 µ³/µ³ for both sampling sites, which can indicate high levels of stress (Fig. 5A). It is worth mentioning that the reference values cited are for mussels, not for oysters. Independently, these results are in agreement with the presence of histological alterations and size and shape changes of the digestive tubule as well as of the gills.

Concerning the seasons, there was a tendency for the gill parameters to decrease whereas the digestive gland parameters increase over time. The smallest value of the tubule epithelium area of the digestive gland was in summer and the highest was in winter, that is, a decrease in the epithelium of the digestive tubules in the warmer months. CTD ratio was higher in the warmer months indicating, once again, a poor histological integrity of the digestive gland. These results may come from a sum of intense port activities in the region and visitors, which increase considerably in warm seasons (Dirección de Turismo de Coronel Rosales 2012), and can also increase untreated sewage released in this region. The gill parameters varied more with the seasons, but an increase in the parameters could be observed in the warmer months, possibly due to the increase in the negative effects of the increase in human activities in the region. Valdez Domingues et al. (2007) also observed variability in the histopathology analysis of C. rhizophorae gills over seasons. The authors link some negative observations in gills with the intense traffic of boats and coastal visitors, which lead to an increase in domestic runoff and aggravation in the region contamination in the summer. Bignell et al. (2007) also observed seasonal variability in mussels and suggested that biomarkers are dynamic variables that also depend on factors imposed by the environment and seasons, and not only by genetic factors. Animals sampled at different times of the year have different life histories that must be taken into account when trying to compare biomarker data from groups of animals, even the same species, collected in different seasons or different locations (Bignell et al. 2007) However, in these studies, a tendency of the parameters was observed over the seasons. Besides that, the characteristics of the sampling sites can contribute to explaining the different results found between sampling sites and seasons, with minor values in the individuals from PC. PC is located in a more exposed coastal area and farther from port areas, which may have less influence on the morphological parameters. On the other hand, AP is located close to port areas and is a more sheltered area, favoring the deposition and concentration of pollutants in both water and sediment. In these environments, depositional processes are predominant and are considered the sink and transitional way of many chemical pollutants from the open sea and freshwater land (Botté et al. 2010).

The popularity of oysters in human consumption and the interest in its farmed, plus the expansion of invasive populations worldwide makes oysters an important focal organism for the assessment of levels of status environmental and potential consumption risk. In this study, the values of the morphological parameter analyzed were larger in the gills and smaller in the digestive gland from AP than in PC individuals. Likewise, VvBas and CTD ratio were higher in oysters from AP. Besides that, both the gill and digestive gland present alteration of the pattern of structural organization with fusion of filaments and irregular folders of plicas as well as thickness and atrophy of the epithelium, respectively, in more intensity in individuals from AP. Regarding the seasons, the morphological parameters showed variability over time, being more intense in the warmer months, possibly due to the increase in the number of visitors in the region. These results can indicate that there is a negative relationship between intense human activities and the effect on the gills and digestive glands of Pacific oysters. Thus, the use of M. gigas as a sentinel specie and evaluation biomarkers as histological aspects of this species becomes an important tool for population management in the south of Buenos Aires province, because besides being consumed and presenting possible issues for human health such as virus (Barbieri et al. 2019), heavy metals (Colla et al. 2018) and microplastics (Severini et al. 2019) in their bodies; this species can have a negative effect on the functioning of ecosystems, competing with native species such as B. rodriguezii. Besides that, the understanding of morphology is one of the first steps toward the establishment of strategies to control invasive species (Freitas et al. 2021). In this way, works such as presented here can increase the knowledge about M. gigas, and can contribute to the management and mitigation of the impacts of this invasive species and to assess the environmental status of the study area.

Acknowledgements

We are grateful to Dra. Ariadna Battista who helped us with histological techniques and the reviewers for their contributions and time for revision of the manuscript.

Funding

This work was supported by Universidad de Buenos Aires, UBACyT 008. Otegui, MBP was supported by grants from the Consejo Nacional de Investigaciones Científicas y Técnicas (Conicet-UBA).

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Authors’ contribution

All authors participated in the study conception, design, analysis and interpretation of the data, redaction of the manuscript and gave final approval for publication.

Conflicts of interest

The authors declare there are no conflicts of interest.

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Histological characterization and morphological alterations in gill and digestive gland in non-native bivalve from the Province of Buenos Aires: spatial and seasonal evaluation

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Abstract

Figures

1. Introduction

2. Materials and Methods

2.1. Study areas and oyster collection

2.2. Histological procedure

2.3. Morphometric analysis of gill and digestive gland epithelium

2.4. Gill and digestive gland histological alterations

2.5. Data analysis

3. Results

3.1. Morphometric analysis of gill and digestive gland epithelium

3.2. Gill and digestive gland histological alterations

4. Discussion

Declarations

References

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Journal Publication

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