INTRODUCTION
⌅The green crab, Carcinus maenas (Linnaeus 1758), has a wide native distribution on the Atlantic coast, extending from Europe to North Africa (Crothers 1968Crothers J.H. 1968. The biology of the shore crab Carcinus maenas (L.). 2. The Life of the Adult Crab. Field Studies 2: 579-614.). It is also distributed worldwide due to several successful introductions and spreading episodes arising from anthropogenic activities (Carlton and Cohen 2003Carlton J.T., Cohen A.N. 2003. Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aestuarii. J. Biogeogr. 30: 1809-1820. https://doi.org/10.1111/j.1365-2699.2003.00962.x ). This crab inhabits intertidal and subtidal areas such as rocky shores, estuaries, salt marshes and coastal lagoons, which demonstrates its tolerance to large fluctuations in salinity, temperature and oxygen (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434., Amaral et al. 2009Amaral V., Cabral H.N., Jenkins S., et al. 2009. Comparing quality of estuarine and nearshore intertidal habitats for Carcinus maenas. Estuar. Coast. Shelf Sci. 83: 219-226. https://doi.org/10.1016/j.ecss.2009.03.029 ). Despite this plasticity in habitat use, when environmental conditions change, the distribution of this species can also change (Almeida et al. 2008Almeida C., Coelho R., Silva M., et al. 2008. Use of different intertidal habitats by faunal communities in a temperate coastal lagoon. Estuar. Coast. Shelf Sci. 80: 357-364. https://doi.org/10.1016/j.ecss.2008.08.017 ), as it actively moves in search of better-quality habitats (Ameyaw-Akumfi and Naylor 1987Ameyaw-Akumfi C., Naylor E. 1987. Spontaneous and induced components of salinity preference behaviour in Carcinus maenas. Mar. Ecol. Prog. Ser. 37: 153-158. https://doi.org/10.3354/meps037153 ). The species plays an important role in trophic food webs (Baeta et al. 2006Baeta A., Marques J., Cabral H., Pardal M. 2006. Feeding ecology of the green crab, Carcinus maenas (L., 1758) in a temperate estuary, Portugal. Crustaceana 79: 1181-1193. https://doi.org/10.1163/156854006778859506 ), where it can be a prey for several fish species (Hampel et al. 2005Hampel H., Cattrijsse A., Elliott M. 2005. Feeding habits of young predatory fishes in marsh creeks situated along the salinity gradient of the Schelde estuary, Belgium and The Netherlands. Helgol. Mar. Res. 59: 151-162. https://doi.org/10.1007/s10152-004-0214-2 , Avignon et al. 2017Avignon S., Tastard E., Weston S., et al. 2017. Morphological identification and DNA barcoding used for diet analysis of gilthead seabream (Sparus aurata) in its expanding northerly range. Aquat. Living Resour. 30: 1. https://doi.org/10.1051/alr/2016034 ) and also an active benthic predator on shellfish, crustacea and polychaetes (Chaves et al. 2010Chaves M.L., Horta M.S., Chainho P.M., Costa J.L. 2010. New additions to the feeding ecology of Carcinus maenas (L., 1758) in a South-western Europe estuary (Portugal). Cah. Biol. Mar. 51: 229-238.), acting as an energy carrier in all systems (Glamuzina et al. 2017Glamuzina L., Conides A., Mancinelli G., et al. 2017. Population Dynamics and Reproduction of Mediterranean Green Crab Carcinus aestuarii in Parila Lagoon (Neretva Estuary, Adriatic Sea, Croatia) as Fishery Management Tools. Mar Coast Fish: Dynamics, Management, and Ecosystem Science 9: 260-270. https://doi.org/10.1080/19425120.2017.1310155 ). Although the species can reach a carapace width of 86 mm (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434.), in high-density populations the crabs tend to be smaller due to intraspecific competition and cannibalism (Moksnes 2004Moksnes P.-O. 2004. Interference competition for space in nursery habitats: density-dependent effects on growth and dispersal in juvenile shore crabs Carcinus maenas. Mar. Ecol. Prog. Ser. 281: 181-191. https://doi.org/10.3354/meps281181 ). Females can achieve sexual maturity at a carapace width of between 15 and 30 mm, and breeding can occur during the entire year (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434.). Despite the existence of specimens in all life cycle stages throughout the year (Baeta et al. 2005Baeta A., Cabral H.N., Neto J.M., et al. 2005. Biology, population dynamics and secondary production of the green crab Carcinus maenas (L.) in a temperate estuary. Estuar. Coast. Shelf Sci. 65: 43-52. https://doi.org/10.1016/j.ecss.2005.05.004 ), the abundance of ovigerous females is higher in late winter and spring, in deeper saline waters (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434., Queiroga et al. 1994Queiroga H., Costlow D., Moreira M.H. 1994. Larval abundance patterns of Carcinus maenas (Decapoda, Brachyura) in Canal de Mira (Ria de Aveiro, Portugal). Mar. Ecol. Prog. Ser. 111: 63-72. https://doi.org/10.3354/meps111063 ).
One of the aquatic systems inhabited by the green crab is that of coastal lagoons, which are among the most productive ecosystems in the world (Kennish and Paerl 2010Kennish M.J., Paerl H.W. 2010. Coastal Lagoons: Critical Habitats of Environmental Change. In: Kennish M.J., Paerl H.W. (eds), Coastal Lagoons: Critical Habitats of Environmental Change (Marine Science Series), CRC Press, Boca Raton, 1-16. https://doi.org/10.1201/EBK1420088304 ). Coastal lagoons are shallow water bodies exposed to conspicuous significant environmental fluctuations and are in most cases very productive systems, where wind and bottom topography have an important effect on water mixing (Kjerfve 1994Kjerfve B. 1994. Coastal Lagoons, In: Kjerfve B. (ed) Coastal Lagoon Processes. Elsevier Oceanography Series 60: 1-8. https://doi.org/10.1016/S0422-9894(08)70006-0 , Kennish and Paerl 2010Kennish M.J., Paerl H.W. 2010. Coastal Lagoons: Critical Habitats of Environmental Change. In: Kennish M.J., Paerl H.W. (eds), Coastal Lagoons: Critical Habitats of Environmental Change (Marine Science Series), CRC Press, Boca Raton, 1-16. https://doi.org/10.1201/EBK1420088304 , Pérez-Ruzafa et al. 2011Pérez-Ruzafa A., Marcos C., Pérez-Ruzafa I.M. 2011. Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Phys Chem Earth 36: 160-166. https://doi.org/10.1016/j.pce.2010.04.013 ). These systems are usually separated from the sea, and the connection is made by one or more restricted inlets (Kjerfve 1994Kjerfve B. 1994. Coastal Lagoons, In: Kjerfve B. (ed) Coastal Lagoon Processes. Elsevier Oceanography Series 60: 1-8. https://doi.org/10.1016/S0422-9894(08)70006-0 ). However, coastal lagoons that remain isolated from the sea for long periods are quite rare (Cancela da Fonseca et al. 1989Cancela da Fonseca L., Costa A.M., Bernardo J.M. 1989. Seasonal variation of benthic and fish communities in a shallow land-locked coastal lagoon (St. André, SW Portugal). Sci. Mar. 53: 663-669.) and become more vulnerable to eutrophication processes (Kjerfve 1994Kjerfve B. 1994. Coastal Lagoons, In: Kjerfve B. (ed) Coastal Lagoon Processes. Elsevier Oceanography Series 60: 1-8. https://doi.org/10.1016/S0422-9894(08)70006-0 ). Despite their fragile environmental balance, coastal lagoons are of great ecological importance, which, combined with their calm and easily predictable conditions, makes them important in regional socio-economic activities related to professional and recreational fisheries (Pérez-Ruzafa et al. 2011Pérez-Ruzafa A., Marcos C., Pérez-Ruzafa I.M. 2011. Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Phys Chem Earth 36: 160-166. https://doi.org/10.1016/j.pce.2010.04.013 ). In Santo André Coastal Lagoon, fisheries are socially and economically important and mostly directed towards the European eel, Anguilla anguilla (Correia et al. 2019Correia M.J., Domingos I., Santos J., et al. 2019. Challenges to reconcile conservation and exploitation of the threatened Anguilla anguilla (Linnaeus, 1758) in Santo André lagoon (Portugal). Ocean Coast. Manag. 181: 104892. https://doi.org/10.1016/j.ocecoaman.2019.104892 ). In some cases, the great abundance of green crab can lead to economic losses for fishermen, mainly due to the damage they cause to fyke nets, and to the fish caught. To overcome this problem, in 2019, the fisheries management authority included the green crab in the local fisheries regulation, but this should be supported in sound knowledge about the population dynamics.
To promote future sustainability of the fishery and improve gains for the fishermen’s community, it is urgent to collect population parameters for a baseline assessment of green crab in the lagoon. This information is fundamental for establishing suitable management practices that ensure the correct management of the resource and avoid its waste. Hence, this study aims to characterize the green crab population in the Santo André Lagoon by analysing population attributes such as abundance, spatial-temporal variability, size structure, sex ratio and reproductive potential, and to estimate the annual catch of green crab in the lagoon.
MATERIALS AND METHODS
⌅Study area
⌅Santo André Lagoon is a coastal lagoon in the northeastern Atlantic located in the southwest of mainland Portugal (38°05’47.57’’N; 8°47’23.69’’W, see Fig. 1). This lagoon is part of the Natural Reserve of Lagoa de Santo André and Sancha and it is under the protection of the Ramsar Convention on Wetlands and Natura 2000 (Birds Directive - Special Protection Area and Habitats Directive - Site of Community Importance). The lagoon has an area of 150 ha (Cancela da Fonseca et al. 2001Cancela da Fonseca L., Bernardo J.M., Costa A.M., et al. 2001. Seasonal chemical changes and eutrophication of a land-locked coastal lagoon (St. André, SW Portugal). Bol. Mus. Mun. Funchal 6: 167-183, ISSN 0870-3876), with an average annual depth of 1.8 m (Cancela da Fonseca et al. 1989Cancela da Fonseca L., Costa A.M., Bernardo J.M. 1989. Seasonal variation of benthic and fish communities in a shallow land-locked coastal lagoon (St. André, SW Portugal). Sci. Mar. 53: 663-669.). The high nutrient levels and shallow depth of this coastal lagoon provide ideal conditions for high rates of primary production (Duarte et al. 2002Duarte P., Bernardo J.M., Costa A.M., et al. 2002. Analysis of coastal lagoon metabolism as a basis for management. Aquat. Ecol. 36: 3-19. https://doi.org/10.1023/A:1013394521627 ).
A sand bar separates the water body from the ocean during most of the year. The connection to the sea is artificially established, usually in March, through a man-made channel that typically remains open for a few weeks to a month (Cancela da Fonseca et al. 1989Cancela da Fonseca L., Costa A.M., Bernardo J.M. 1989. Seasonal variation of benthic and fish communities in a shallow land-locked coastal lagoon (St. André, SW Portugal). Sci. Mar. 53: 663-669.). Outside this period, the lagoon may sporadically be in contact with the sea, especially when waves surpass the dunes, usually in autumn and winter (Félix et al. 2015Félix P.M., Correia M.J., Chainho P., et al. 2015. Impact of freshwater inputs on the spatial structure of benthic macroinvertebrate communities in two landlocked coastal lagoons. Hydrobiologia 758: 197-209. https://doi.org/10.1007/s10750-015-2290-5 ). Water renewal occurs when the communication between the lagoon and the sea is re-established, which is essential to maintain the functioning and productivity of the system. In addition to preventing eutrophication processes, this connection also allows the recruitment to the lagoon of several marine animals and their larval stages, as well as plant species (Costa et al. 1985Costa A.M., Bernardo J.M., Cancela da Fonseca L. 1985. Breve caracterização da evolução recente da lagoa de Santo André (1978 - 1985). 2º Congresso sobre O Alentejo. Beja, Portugal, pp. 623-627, Bernardo et al. 1988Bernardo J.M., Costa A.M., Cancela da Fonseca L. 1988. Nutrient dynamics and dystrophy in a brackish coastal lagoon (St. André, SW Portugal). Rapp. Comm. Int. Mer Médit. 31(2): 6 pp., Félix et al. 2015Félix P.M., Correia M.J., Chainho P., et al. 2015. Impact of freshwater inputs on the spatial structure of benthic macroinvertebrate communities in two landlocked coastal lagoons. Hydrobiologia 758: 197-209. https://doi.org/10.1007/s10750-015-2290-5 ). The lagoon can be colonized by both marine and freshwater species, but in most cases the species survive only for short periods due to the lagoon’s highly fluctuating environment (Cancela da Fonseca et al. 1989Cancela da Fonseca L., Costa A.M., Bernardo J.M. 1989. Seasonal variation of benthic and fish communities in a shallow land-locked coastal lagoon (St. André, SW Portugal). Sci. Mar. 53: 663-669., Garside et al. 2014Garside C.J., Glasby T.M., Coleman M.A., et al. 2014. The frequency of connection of coastal water bodies to the ocean predicts Carcinus maenas invasion. Limnol. Oceanogr. 59: 1288-1296. https://doi.org/10.4319/lo.2014.59.4.1288 ).
The lagoon fauna is dominated by macroinvertebrates, fish species and aquatic birds (Cancela da Fonseca et al. 2001Cancela da Fonseca L., Bernardo J.M., Costa A.M., et al. 2001. Seasonal chemical changes and eutrophication of a land-locked coastal lagoon (St. André, SW Portugal). Bol. Mus. Mun. Funchal 6: 167-183, ISSN 0870-3876), some of which are exploited by the fishing community and have high economic value. The European eel supports the most important fishery in the lagoon, with an estimated 4 to 8 t of this species being harvested annually (Correia et al. 2019Correia M.J., Domingos I., Santos J., et al. 2019. Challenges to reconcile conservation and exploitation of the threatened Anguilla anguilla (Linnaeus, 1758) in Santo André lagoon (Portugal). Ocean Coast. Manag. 181: 104892. https://doi.org/10.1016/j.ocecoaman.2019.104892 ).
Field sampling and laboratory work
⌅Sampling (experimental fishing) was conducted monthly at five locations from January to December 2019. To cover the habitat diversity, the five sampling sites were selected on the basis of the distance between them and the substrate type. Sediments were then grouped as Mud <63 µm; 0.063 mm ≤Muddy sand/Sandy mud <0.2 mm; 0.2 mm ≤Sand <2 mm; 2 mm ≤Gravel, following the classification system adopted in the sediment charts of the Portuguese Navy Hydrographic Institute (Moita 1985Moita I. 1985. Carta dos sedimentos superficiais da Plataforma Continental: Cabo S. Vicente ao Rio Guadiana (SED 7 e 8), 1st ed. Instituto Hidrográfico, Lisbon.). Site A is the closest to the sea and has a sandy bottom; site B is located in the middle of the lagoon, with mud and sand; site C is the upstream area, with a muddy and sandy bottom; site D in the southern area has a sandy bottom and is an even more closed water body inside the lagoon; and site E, in the northern area, has a muddy bottom and is an important fishery area (Fig. 1).
At each location, four unbaited winged fyke nets with the same dimensions as those used by fishermen (2 m bag length, 5 m wing length, 1.5 m wing height and 18 mm mesh size in cod-end) were set during the afternoon and removed the next morning. On each sampling occasion, four environmental variables (Table 1) were measured using a multiparametric probe (YSI II Water Quality Sonde).
| Variable | Units | Range [minimum - maximum] | Mean | ||||
|---|---|---|---|---|---|---|---|
| Site A | Site B | Site C | Site D | Site E | |||
| Water temperature | °C | [9.57 - 25.08] | [9.57 - 25.86] | [10.35 - 26.24] | [10.51 - 25.82] | [9.58 - 25.81] | 18.92 |
| Depth | m | [1.17 - 3.06] | [0.88 - 1.84] | [0.77 - 1.76] | [0.52 - 1.45] | [0.93 - 1.98] | 1.49 |
| Total dissolved solids | g/L | [17.10 - 24.85] | [17.05 - 24.66] | [16.42 - 23.82] | [16.88 - 24.62] | [17.09 - 24.66] | 20.39 |
| Salinity | [16.10 - 24.31] | [16.09 - 24.10] | [15.44 - 23.25] | [15.87 - 24.08] | [16.09 - 24.11] | 19.57 | |
For each fyke net, the total number of crabs caught were counted and weighed. A random subsample of 20 individuals per fyke net was retained and transported to the laboratory and frozen until processing, to collect individual data: carapace width, measured between the tips of their fifth anterior lateral spines (±1 mm accuracy); weight (precision±0.01 g); sex, determined by analysis of the abdomen (V-shaped abdomen in males and wider and U-shaped abdomen in females); and ovigerous females, depending on whether visible eggs were present.
Data on crab catches from the artisanal fishery were obtained from three volunteer fishermen (≈8% of the total number of fishermen with a fishing licence) during the 2019 fishing season, which was divided into two fishing periods. The first fishing period ran from 1 January to 17 March and the second from 16 July to 30 September. Logbooks were distributed to fishermen who volunteered to record the number and/or total weight of crabs caught per day, as well as the number of fyke nets used daily.
Statistical analysis
⌅Spatial-temporal variability of green crab abundance was assessed using a permutational analysis of variance (PERMANOVA) (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E: Plymouth, UK), in which a two-way fixed-effect crossed design was performed (factors: sampling month and sampling site). A square root transformation was applied to the variables, and the Bray-Curtis similarity coefficient was used as a resemblance measure. A posteriori pairwise tests were conducted when significant interactions between factors were identified. These procedures were performed using PRIMER® v6 (Clarke and Gorley 2006Clarke K.R., Gorley R.N. 2006. PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E, Plymouth.).
The influence of environmental factors on the abundance of green crab (response variable) was assessed with a generalized linear model (GLM, McCullagh and Nelder 1989McCullagh P., Nelder J.A. 1989. Generalized Linear Models. London: Chapman and Hall. https://doi.org/10.1201/9780203753736 ) performed in R environment (R Core Team 2021) using the “MASS” software package (Venables and Ripley 2002Venables W.N., Ripley B.D. 2002. Modern applied statistics with S, 4th Edition. Springer-Verlag, New York. https://doi.org/10.1007/978-0-387-21706-2 ). In addition to the environmental variables measured on each sampling occasion (Table 1), the remaining explanatory variables included in the analysis were sampling month (January-December), sediment type and total organic matter content (%) (unpublished data). Before modelling, a Spearman correlation test was performed between the predictors, and a high correlation coefficient (ρ>0.7, Dormann et al. 2013Dormann C.F., Elith J., Bacher S., et al. 2013. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1): 027-046. https://doi.org/10.1111/j.1600-0587.2012.07348.x ) was identified between total dissolved solids and salinity. Thus, to avoid redundancy, total dissolved solids was removed from subsequent analysis. The Akaike information criterion (Sakamoto et al. 1986Sakamoto Y., Ishiguro M., Kitagawa G. 1986. Akaike Information Criterion Statistics. D. Reidel Publishing Company.) was chosen for the selection of the best model. Subsequently, an ANOVA was performed with the chi-squared (χ2) test to verify the significance of the variables in the model.
Laboratory data were used for the biological characterization of the green crab population. Regarding carapace width, after verifying the normality and homoscedasticity of the dataset, a two-way ANOVA was conducted to examine the effect of sampling month and sampling site on carapace width. A Tukey HSD post hoc test was performed for multiple comparisons between effects. The statistical tests were conducted in IBM® SPSS® Statistics 26 (IBM Corp. Released 2019IBM Corp. Released. 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp).
The gender data of the individuals were analysed by sampling month and by sampling site using a χ2 test. Data on ovigerous and non-ovigerous females were also analysed by sampling month and by sampling site using a χ2 test. These statistical tests were conducted using IBM® SPSS® Statistics 26 (IBM Corp. Released 2019IBM Corp. Released. 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp). To estimate the size at which 50% of the green crab females were sexually mature in the lagoon, a logistic regression model was used, and the maturity ogive was calculated using the “sizeMat” software package (Torrejon-Magallanes 2020Torrejon-Magallanes J. 2020. SizeMat Package: Estimate Size at Sexual Maturity. Version 1.1.2. Repository CRAN. Date/Publication 2020-06-03 22:00:02 UTC) in R environment (R Core Team 2021R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing Version 4.1.2. Vienna, Austria.).
Data from fishing logbooks and experimental fishing were used to estimate the total weight of green crabs harvested annually (kg/ha/year). The catch per unit effort (CPUE), was determined as the average ± standard deviation of the estimated CPUE for each fisherman and the average obtained from the experimental fishery, expressed as kg of green crabs per fyke net per fishing day. The total annual green crab catch in the Santo André Lagoon was estimated by multiplying the average CPUE obtained by the total number of fishing days, by the total number of fishermen with a fishing licence, and by the number of fyke nets they used in each fishing period.
RESULTS
⌅Abundance and distribution
⌅A total of 15063 green crabs were collected over the study period: 6740 at site A, 1995 at site B, 904 at site C, 3123 at site D and 2301 at site E (Fig. 2). The highest number (1944 crabs) were collected at site A in January and the lowest number (14 crabs) at site C in February. January and December were the months with the highest catches (2819 and 2116, respectively) and October was the month with the lowest (326 crabs) (Fig. 2). The highest catches were at site A from January to May plus December and at site D from July to September.
Regarding the spatial-temporal variability, PERMANOVA tests showed that the abundance of green crab was significantly different for both factors, sampling month (F=6.0738, df=11, ρ<0.05) and sampling site (F=15.4270, df=4, ρ<0.05), and for the interaction between factors (F=2.3634, df=44, ρ<0.05). Pairwise tests revealed significant differences between October and all months, except for February and March (Supplementary material Table S1). Pairwise tests for each pair of sampling sites revealed significant differences between all sampling sites, except for site E, which did not differ from sites B and D (Supplementary material Table S2).
The GLM developed to understand the relationship between abundance and environmental factors showed a predictive performance of 37.18%. The variables that best explained the species abundance inside the lagoon were sediment type (27.26%), temperature (6.15%), salinity (3.06%) and depth (0.71%). The abundance increased in deeper sandy areas and decreased in the remaining sediment types and with higher water temperature and salinity. The summary of the model coefficients is presented in Table 2.
| Variable | Estimate | Std. error | z value | Pr (>|z|) |
|---|---|---|---|---|
| (Intercept) | 7.04 | 0.08 | 85.25 | < 0.05 |
| Sediment type (muddy) | - 0.92 | 0.04 | - 23.24 | < 0.05 |
| Sediment type (muddy sand) | - 0.14 | 0.03 | - 4.42 | < 0.05 |
| Sediment type (sand) | 0.71 | 0.02 | 29.90 | < 0.05 |
| Temperature | - 0.05 | 0.00 | - 31.29 | < 0.05 |
| Salinity | - 0.05 | 0.00 | - 16.47 | < 0.05 |
| Depth | 0.14 | 0.01 | 11.05 | < 0.05 |
Size and sex structure
⌅Of the 3898 specimens analysed in the laboratory over the study period, 2288 (58.70%) were males and 1610 (41.30%) were females. The carapace width of the largest green crab measured was 73.60 mm and that of the smallest 21.24 mm. The carapace width of males ranged from 21.24 to 71.46 mm and that of females from 26.68 to 73.60 mm. The average carapace width of the whole green crab population was 45.50 mm (Figs 3 and 4), with 40.79 mm for females and 48.81 mm for males (Fig. 5). The largest green crabs were predominant in the summer months (Fig. 3). The results of the ANOVA showed that there were statistically significant differences in carapace width between sampling months (F=90.07, df=11, ρ<0.05) and between sampling sites (F=18.00, df=4, ρ<0.05) and a statistically significant interaction between the effects of both factors (F=4.66, df=44, ρ<0.05). The Tukey HSD post hoc test revealed that the smaller carapace width of green crabs caught in January was significantly different (ρ<0.05) when compared with the measures obtained for the remaining months (Fig. 3). Regarding sampling sites, the Tukey HSD test showed that the carapace width was significantly different between site C and the other sampling sites (ρ<0.05) and between site D and the other sampling sites (ρ<0.05). There was no statistically significant difference in carapace width between sites A and B (ρ=0.10), A and E (ρ=0.54) or B and E (ρ=0.87).
The population sex ratio varied significantly, in relation to both the sampling month (χ2=752.06, df=11, ρ<0.05), and the sampling sites (χ2=37.36, df=4, ρ<0.05). The highest female-biased sex ratios occurred in January and December, with respectively 79.13% and 80.05%, followed by February, with 63.16%. From March to November, catches were dominated by males, with August standing out with the highest proportion of males (92.79%), while March was the month closest to a balanced distribution between sexes, with 45.51% females and 54.48% males (Fig. 6). Overall, the sex ratio was biased towards males at all sampling sites except site A, where the sex ratio was closer to a 1:1 balance (48.75% females; 51.25% males) (Fig. 6).
The ratio between ovigerous and non-ovigerous females varied significantly with the sampling month (χ2=143.13, df=11, ρ<0.05) but not with the sampling site (χ2=7.19, df=4, ρ=0.13). Non-ovigerous females (n=1430; 88.82%) predominated over ovigerous females (n=180; 11.18%) in all months and sites sampled. The highest catches of ovigerous females occurred in January and December (23.29% and 22.74%, respectively), whereas in June, August and September no ovigerous females were caught. All sampling sites followed the same pattern, with an average of 11.59% ovigerous females per site.
Over the study period, the size of ovigerous females varied between 26.68 and 56.22 mm (mean, 41.07 mm) and that of non-ovigerous females between 27.05 and 73.60 mm (mean, 40.75 mm). In Santo André Lagoon, 50% of females attained sexual maturity when they reached an average carapace width of 45.11 mm (Fig. 7).
Estimation of annual catches
⌅In 2019, for the first fishing period, each fisherman caught on average 2.92±3.23 kg/fyke net/fishing day, ranging from 0.14 kg/fyke net/fishing day in February to 12.86 kg/fyke net/fishing day in January. In the second fishing period, each fisherman caught on average 1.60±0.39 kg/fyke net/fishing day, ranging from 0.16 kg/fyke net/fishing day in September to 2.75 kg/fyke net/fishing day in August (Fig. 8).
The average obtained with experimental fishing throughout the entire year, using the same gear as the fishermen, was 1.24±1.44 kg/fyke net/fishing day, ranging from 0.04 kg/fyke net/fishing day in February to 6.97 kg/fyke net/fishing day in December (Fig. 8).
The average daily catch from the two commercial fishing periods and the average daily catch from the experimental fishing were used to estimate the total amount of green crab harvested in the lagoon in 2019. Considering the whole fishing period allowed (155 days), the entire fishing community (39 licensed fishermen) and the area of the lagoon (150 ha), the total green crab catches in 2019 was estimated to range between 281 and 503 t. As there is no catch limit imposed by the legislation, these values suggest that fishermen can harvest 1.87 to 3.35 t/ha (1873 to 3354 kg/ha) of green crab annually.
DISCUSSION
⌅This study analysed the population dynamics of green crab and explored its potential importance as a fishery resource in Portugal. The distribution and abundance of green crab in the Santo André Lagoon are highly variable in time and space (Fig. 2), displaying active habitat selection during the life cycle, similar to the results of other authors elsewhere (Baeta et al. 2005Baeta A., Cabral H.N., Neto J.M., et al. 2005. Biology, population dynamics and secondary production of the green crab Carcinus maenas (L.) in a temperate estuary. Estuar. Coast. Shelf Sci. 65: 43-52. https://doi.org/10.1016/j.ecss.2005.05.004 , Almeida et al. 2008Almeida C., Coelho R., Silva M., et al. 2008. Use of different intertidal habitats by faunal communities in a temperate coastal lagoon. Estuar. Coast. Shelf Sci. 80: 357-364. https://doi.org/10.1016/j.ecss.2008.08.017 ). The species is present throughout the lagoon, but the highest catches were obtained at site A (the closest to the sea and with a sandy bottom), mostly in winter and spring and at site D (the second closest to the sea and with a sandy bottom), with particularly high catches in summer. These two sampling sites seem to be the preferential areas for the species in the lagoon, which can be attributed to their greater proximity to the sea or to the type of bottom sediment (sand), as confirmed by the GLM and previously verified by Cancela da Fonseca and Luís (1992)Cancela da Fonseca L., Luís O. 1992. Considerações Sobre a População do Caranguejo-Verde (Carcinus maenas) na Lagoa De Santo André. Colóquio Conservação Dos Recursos Vivos Marinhos. Lisboa, Portugal. Publicações Avulsas do I.N.I.P. 17: 329-347.. Despite the past (Cancela da Fonseca and Luís 1992Cancela da Fonseca L., Luís O. 1992. Considerações Sobre a População do Caranguejo-Verde (Carcinus maenas) na Lagoa De Santo André. Colóquio Conservação Dos Recursos Vivos Marinhos. Lisboa, Portugal. Publicações Avulsas do I.N.I.P. 17: 329-347.) and current habitat preference observed in this lagoon, the species seems to benefit from other habitats like shellfish beds or vegetation areas (Almeida et al. 2008Almeida C., Coelho R., Silva M., et al. 2008. Use of different intertidal habitats by faunal communities in a temperate coastal lagoon. Estuar. Coast. Shelf Sci. 80: 357-364. https://doi.org/10.1016/j.ecss.2008.08.017 , Amaral et al. 2009Amaral V., Cabral H.N., Jenkins S., et al. 2009. Comparing quality of estuarine and nearshore intertidal habitats for Carcinus maenas. Estuar. Coast. Shelf Sci. 83: 219-226. https://doi.org/10.1016/j.ecss.2009.03.029 , Almeida et al. 2011Almeida M.J., González-Gordillo J.I., Flores A.A.V, Queiroga H. 2011. Cannibalism, post-settlement growth rate and size refuge in a recruitment-limited population of the shore crab Carcinus maenas. J. Exp. Mar. Biol. Ecol. 410: 72-79. https://doi.org/10.1016/j.jembe.2011.10.011 ). The assessment of habitat quality and species preferences is very important as it allows the implementation of more accurate policies, management or conservation measures or strategies (Amaral et al. 2009Amaral V., Cabral H.N., Jenkins S., et al. 2009. Comparing quality of estuarine and nearshore intertidal habitats for Carcinus maenas. Estuar. Coast. Shelf Sci. 83: 219-226. https://doi.org/10.1016/j.ecss.2009.03.029 ).
The green crab carapace width is within the size range reported for the species (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434., Baeta et al. 2005Baeta A., Cabral H.N., Neto J.M., et al. 2005. Biology, population dynamics and secondary production of the green crab Carcinus maenas (L.) in a temperate estuary. Estuar. Coast. Shelf Sci. 65: 43-52. https://doi.org/10.1016/j.ecss.2005.05.004 ). The male-biased sex ratio was observed for almost the whole year, in line with that of other green crab populations on the Atlantic coast (Lyons et al. 2012Lyons L.J., O’Riordan R.M., Cross T.F., Culloty S C, 2012. Reproductive biology of the shore crab Carcinus maenas (Decapoda, Portunidae): a macroscopic and histological view. Invertebr. Reprod. Dev. 56: 144-156. https://doi.org/10.1080/07924259.2011.582693 , Ladeira 2016Ladeira C.N. 2016. Ecology, Distribution, Habitat segregation and tidal migration of green crab Carcinus maenas in Ria de Aveiro, Portugal. Master Thesis in Marine Biology, University of Aveiro, Portugal. In press. 52pp). Lyons et al. (2012)Lyons L.J., O’Riordan R.M., Cross T.F., Culloty S C, 2012. Reproductive biology of the shore crab Carcinus maenas (Decapoda, Portunidae): a macroscopic and histological view. Invertebr. Reprod. Dev. 56: 144-156. https://doi.org/10.1080/07924259.2011.582693 reported larger specimens in spring/summer in southwest Ireland which were also mature adults of the population. Thus, the relative size of individuals from both sexes might be related to the breeding season, as males must be larger than females (Reid et al. 1997Reid D.G., Abello P., Kaiser M.J., Warman C.G. 1997. Carapace colour, inter-moult duration and physiological ecology of the shore crab Carcinus maenas. Estuar. Coast. Shelf Sci. 44: 203 - 211. https://doi.org/10.1006/ecss.1996.0212 ) and the mating process is estimated to occur in late summer (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434.).
The reproduction was not inhibited by the salinity of the lagoon, as this species can reproduce at salinities above 10 (Crothers 1967Crothers J.H. 1967. The biology of the shore crab Carcinus maenas (L.). 1. The background - anatomy, growth and life history. Field studies 2: 407 - 434.). Ovigerous females were more abundant in this lagoon in the winter period, which has also been reported for other areas of the Portuguese Atlantic coast (Baeta et al. 2005Baeta A., Cabral H.N., Neto J.M., et al. 2005. Biology, population dynamics and secondary production of the green crab Carcinus maenas (L.) in a temperate estuary. Estuar. Coast. Shelf Sci. 65: 43-52. https://doi.org/10.1016/j.ecss.2005.05.004 , Queiroga et al. 1994Queiroga H., Costlow D., Moreira M.H. 1994. Larval abundance patterns of Carcinus maenas (Decapoda, Brachyura) in Canal de Mira (Ria de Aveiro, Portugal). Mar. Ecol. Prog. Ser. 111: 63-72. https://doi.org/10.3354/meps111063 ). The estimated carapace width of females at maturity was 45.11 mm, which is lower than the sizes reported for North Wales or southwest Ireland (Reid et al. 1997Reid D.G., Abello P., Kaiser M.J., Warman C.G. 1997. Carapace colour, inter-moult duration and physiological ecology of the shore crab Carcinus maenas. Estuar. Coast. Shelf Sci. 44: 203 - 211. https://doi.org/10.1006/ecss.1996.0212 , Lyons et al. 2012Lyons L.J., O’Riordan R.M., Cross T.F., Culloty S C, 2012. Reproductive biology of the shore crab Carcinus maenas (Decapoda, Portunidae): a macroscopic and histological view. Invertebr. Reprod. Dev. 56: 144-156. https://doi.org/10.1080/07924259.2011.582693 ) and lower than the sizes reported for other Portuguese brackish water systems except the Sado estuary (Monteiro et al. 2022Monteiro J.N., Ovelheiro A., Ventaneira A.M., et al. 2022. Variability in Carcinus maenas Fecundity Along Lagoons and Estuaries of the Portuguese Coast. Estuaries Coast. 45: 1716-1727. https://doi.org/10.1007/s12237-021-01035-9 ).
The current estimate of the annual catch of green crab in Santo André Lagoon is higher than that obtained in a previous study conducted in 1985/1986 (1873 to 3354 kg/ha vs 130 kg/ ha, respectively) (Cancela da Fonseca and Luís 1992Cancela da Fonseca L., Luís O. 1992. Considerações Sobre a População do Caranguejo-Verde (Carcinus maenas) na Lagoa De Santo André. Colóquio Conservação Dos Recursos Vivos Marinhos. Lisboa, Portugal. Publicações Avulsas do I.N.I.P. 17: 329-347.). The exploitation of this aquatic resource could increase sustainability of fisheries, as pressure on other vulnerable species (e.g. European eel) would be reduced. Although green crab currently has no commercial value in Portugal, in the second half of the 20th century it had some importance in European landings (Portugal, Spain, France, England, Italy), especially in the Venice lagoon in Italy (Cohen et al. 1995Cohen A.N., Carlton J.T., Fountain M.C. 1995. Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay, California. Mar. Biol. 122: 225-237. https://doi.org/10.1007/BF00348935 , Libralato et al. 2004Libralato S., Pranovi F., Raicevich S et al. 2004. Ecological stages of the Venice Lagoon analysed using landing time series data. J. Mar. Syst. 51: 331-344. https://doi.org/10.1016/j.jmarsys.2004.05.020 ). Future studies should therefore assess the potential of using this resource to develop high-value by-products that can improve benefits and returns to fishermen.
The considerable biomass of green crab available in the Santo André Lagoon could be used to produce crab flour (Fulton and Fairchild 2013Fulton B.A., Fairchild E.A. 2013. Nutritional Analysis of Whole Green Crab, Carcinus maenas, for Application as a Forage Fish Replacement in Agrifeeds. Sustain. Agric. Res. 2: 126-135. https://doi.org/10.5539/sar.v2n3p126 ), fish bait (Morris et al. 2007Morris E.S., Goudge H., Duce C. 2007. An introductory review of the biology and population dynamics of the green shore crab, Carcinus maenas (L.), in the UK, with specific reference to the Menai Strait. CCW Policy Research Report No. 07/18.) and food for shrimp aquaculture (Cancela da Fonseca and Luís 1992Cancela da Fonseca L., Luís O. 1992. Considerações Sobre a População do Caranguejo-Verde (Carcinus maenas) na Lagoa De Santo André. Colóquio Conservação Dos Recursos Vivos Marinhos. Lisboa, Portugal. Publicações Avulsas do I.N.I.P. 17: 329-347.). Beyond these uses, green crab is also appropriate for human consumption (Morris et al. 2007Morris E.S., Goudge H., Duce C. 2007. An introductory review of the biology and population dynamics of the green shore crab, Carcinus maenas (L.), in the UK, with specific reference to the Menai Strait. CCW Policy Research Report No. 07/18.), as it provides a nutritious source of protein (Cancela da Fonseca and Luís 1992Cancela da Fonseca L., Luís O. 1992. Considerações Sobre a População do Caranguejo-Verde (Carcinus maenas) na Lagoa De Santo André. Colóquio Conservação Dos Recursos Vivos Marinhos. Lisboa, Portugal. Publicações Avulsas do I.N.I.P. 17: 329-347., Naczk et al. 2004Naczk M., Williams J., Brennan K., Liyanapathirana C., Shahidi F. 2004. Compositional characteristics of green crab (Carcinus maenas). Food Chem. 88: 429-434. https://doi.org/10.1016/j.foodchem.2004.01.056 ; Fulton and Fairchild 2013Fulton B.A., Fairchild E.A. 2013. Nutritional Analysis of Whole Green Crab, Carcinus maenas, for Application as a Forage Fish Replacement in Agrifeeds. Sustain. Agric. Res. 2: 126-135. https://doi.org/10.5539/sar.v2n3p126 ), with similar nutritional values to and lower cholesterol levels than other harvested crabs (Skonberg and Perkins 2002Skonberg D.I., Perkins B.L. 2002. Nutrient composition of green crab (Carcinus maenas) leg meat and claw meat. Food Chem. 77: 401-404. https://doi.org/10.1016/S0308-8146(01)00364-8 ). By-products of this resource, such as shell powder, could also be transformed into innovative biofertilizers for agriculture (Nekvapil et al. 2021Nekvapil F., Ganea I.V., Ciorîță A., et al. 2021. Wasted Biomaterials from Crustaceans as a Compliant Natural Product Regarding Microbiological, Antibacterial Properties and Heavy Metal Content for Reuse in Blue Bioeconomy: A Preliminary Study. Materials 14: 4558. https://doi.org/10.3390/ma14164558 ), supplements to improve eggshell quality in the poultry industry (Lichovnikova 2007Lichovnikova M. 2007. The effect of dietary calcium source, concentration and particle size on calcium retention, eggshell quality and overall calcium requirement in laying hens. Br. Poult. Sci. 48: 71-75. https://doi.org/10.1080/00071660601148203 ), or fine filler material in concrete for construction purposes (Mo et al. 2018Mo K.H., Alengaram U.J., Jumaat M.Z et al. 2018. Recycling of seashell waste in concrete: A review. Constr Build Mater. 162: 751-764. https://doi.org/10.1016/j.conbuildmat.2017.12.009 ), thus contributing to the circular economy (Nekvapil et al. 2021Nekvapil F., Ganea I.V., Ciorîță A., et al. 2021. Wasted Biomaterials from Crustaceans as a Compliant Natural Product Regarding Microbiological, Antibacterial Properties and Heavy Metal Content for Reuse in Blue Bioeconomy: A Preliminary Study. Materials 14: 4558. https://doi.org/10.3390/ma14164558 ).
In conclusion, despite all the advantages of exploiting this resource, the green crab fishing is intrinsically dependent on eel fishing. The European eel is the most valuable resource in the lagoon (Correia et al. 2019Correia M.J., Domingos I., Santos J., et al. 2019. Challenges to reconcile conservation and exploitation of the threatened Anguilla anguilla (Linnaeus, 1758) in Santo André lagoon (Portugal). Ocean Coast. Manag. 181: 104892. https://doi.org/10.1016/j.ocecoaman.2019.104892 ), while green crab is currently considered a bycatch. Non-targeted crab fishing has been carried out (and the crabs have been discarded) with the same fishing gears and in the same fishing periods, jeopardizing compliance with the minimum allowed green crab size and the possibility of closing the crab fishery in subsequent years. The continued study of population dynamics will also help to identify and measure changes in the ecosystem, which can be used as an alternative approach in the absence of other elements to evaluate the system (Glamuzina et al. 2017Glamuzina L., Conides A., Mancinelli G., et al. 2017. Population Dynamics and Reproduction of Mediterranean Green Crab Carcinus aestuarii in Parila Lagoon (Neretva Estuary, Adriatic Sea, Croatia) as Fishery Management Tools. Mar Coast Fish: Dynamics, Management, and Ecosystem Science 9: 260-270. https://doi.org/10.1080/19425120.2017.1310155 ). The future management of this resource should be included in an integrated science-based strategy in which the lagoon is evaluated as a whole and treated in conformity with its socio-economic importance.