Introduction
Sea cucumbers (holothurians) are pivotal species in marine ecosystems. In particular, deposit feeders have a critical ecological role in habitat structuring through bioturbation by recycling and redistributing nutrients (e.g., MacTavish et al., Reference MacTavish, Stenton-Dozey, Vopel and Savage2012; Floren et al., Reference Floren, Hayashizaki, Putchakarn, Tuntiprapas and Prathep2021). Holothurians worldwide are also subject to intense fishing and increasing demand, particularly for exportation to Asian countries (Purcell et al., Reference Purcell, Mercier, Conand, Hamel, Toral-Granda, Lovatelli and Uthicke2013; Azevedo e Silva et al., Reference Azevedo e Silva, Brito, Simões, Pombo, Marques, Rocha, Sousa, Venâncio and Félix2021; Dereli̇ and Aydın, Reference Dereli̇ and Aydın2021) and intensive harvest represents a severe ecological problem: the removal of key ecological functions from the ecosystems.
The holothurian Parastichopus regalis is a species with increasing commercial interest (Rámon et al., Reference Ramón, Lleonart and Massutí2010; Maggi and González-Wangüemert, Reference Maggi and González-Wangüemert2015). It belongs to the Stichopodidae family and has a distribution that covers the NE-Atlantic and Mediterranean regions (e.g., Wirtz, Reference Wirtz2009; Ramon et al., Reference Ramón, Lleonart and Massutí2010). Unlike other commercial species from the Atlantic coast (Azevedo e Silva et al., Reference Azevedo e Silva, Brito, Simões, Pombo, Marques, Rocha, Sousa, Venâncio and Félix2021; Félix et al., Reference Félix, Pombo, Azevedo e Silva, Simões, Marques, Melo, Rocha, Sousa, Venâncio, Costa and Brito2021), P. regalis is a deep-water sea cucumber with a bathymetric distribution that is more common in the range between 50 and 300 m depth (Rámon et al., Reference Ramón, Lleonart and Massutí2010). The Natural Park of Ria Formosa (NPRF), a shallow mesotidal lagoon on the southern Portuguese coast, is not part of the P. regalis distribution or habitat. The commercial species in this coastal system are Holothuria arguinensis and H. mammata (Marquet et al., Reference Marquet, Conand, Power, Canário and González-Wangüemert2017). In some parts of the Mediterranean, P. regalis is a target species with recognised economic value (Maggi and González-Wangüemert, Reference Maggi and González-Wangüemert2015) and is part of the trade market (Ramón et al., Reference Ramón, Amor and Galimany2022). However, otherwise, it is primarily discarded as by-catch by trawlers. This species has no commercial interest in Portugal and is commonly discarded, many of which are at, or near, the landing sites (Pedro M. Félix, personal observation). Furthermore, since 2021, all sea cucumber fisheries have been prohibited (National Decree number 38/2021). These discards have mainly been observed at the Sado estuary (Portugal). Despite this, no sea cucumbers occur in that transitional water body due to the unfit estuarine conditions for P. regalis or any coastal species (Félix et al., Reference Félix, Pombo, Azevedo e Silva, Simões, Marques, Melo, Rocha, Sousa, Venâncio, Costa and Brito2021). The NPRF, on the other hand, has suitable environmental settings for the occurrence of detritivore sea cucumbers (Siegenthaler et al., Reference Siegenthaler, Canovas and Wanguemert2017) and could enable, at the very least, the survival of some non-autochthonous species.
Observation
In November 2023, while conducting an underwater visual census (UVC) survey in NPRF involving a triple 30 m × 2 m random transects in four seagrass meadows' sites (Figure 1), a single individual of P. regalis was detected and photographed (Figure 2) at a depth of 3 m with a water temperature of 19°C. The species was around 17 cm in size and without external physical lesions or apparent reduced physiological condition, presenting ambulacral activity and muscle contraction as a stimulus to manipulation (i.e., good fitness). This type of sampling has been conducted since 2022 on four occasions, with 16 UVC dives performed without any record of the species.
Figure 1. Location of studied sites (1–4) inside Ria Formosa Lagoon. The red circle (Site 2) is the location of the record of Parastichopus regalis detected in the present study. Also indicated is the route of the fishing vessels (dashed line) towards the landing site – Olhão fishing harbour (red square). The map was created in R (R Core Team, 2021) using the ‘leaflet’ package and the provider ‘CartoDB positron’.
Figure 2. Photographs of Parastichopus regalis detected during the underwater visual census conducted in Ria Formosa Lagoon at 3 meters. Photographs taken by Nuno Castro.
Discussion
The NPRF is a shallow mesotidal lagoon located on the south coast of Portugal. This valuable transition water body of regional, national, and international ecological importance is a site of Natura 2000 network (PTZPE0017), EU Birds Directive Special Protection Area and has been part RAMSAR wetland convention since 1980. This coastal lagoon is an important ecosystem with high biodiversity and serves as a nursery area for several species, including several commercial species (Erzini et al., Reference Erzini, Parreira, Sadat, Castro, Bentes, Coelho, Gonçalves, Lino, Martinez-Crego, Monteiro, Oliveira, Ribeiro, de los Santos and Santos2022). The lagoon has several seagrass meadows with associated species, including several endangered species, such as Hippocampus guttulatus and H. hippocampus (Caldwell and Vincent, Reference Caldwell and Vincent2012). It also has several associated leisure and economic activities, such as aquaculture, fishing, shellfish and polychaete harvesting (Oliveira et al., Reference Oliveira, Castilho, Cunha and Pereira2013; Newton et al., Reference Newton, Brito, Icely, Derolez, Clara, Angus, Scherneski, Inácio, Lillebo, Sousa, Béjaoui, Solidoro, Tosic, Cañedo-Arguelles, Yamamuro, Reizopoulou, Tseng, Canu, Roselli, Maanan, Cristina, Ruiz-Fernández, de Lima, Kjerfve, Rubio-Cisneros, Pérez-Ruzafa, Marcos, Pastres, Pranovi, Snoussi, Turpie, Tuchkovenko, Dyack, Brookes, Povilanskas and Khokhlov2018; Cabral et al., Reference Cabral, Alves, Castro, Chainho, Sá, da Fonseca, Fidalgo e Costa, Castro, Canning-Clode, Pombo and Costa2019).
Regarding fisheries, trawling, mainly targeting crustaceans, is heavily intensive in the south of Portugal due to the quantity and value of landings (Borges et al., Reference Borges, Erzini, Bentes, Costa, Gonçalves, Lino, Pais and Ribeiro2001; Monteiro et al., Reference Monteiro, Araújo, Erzini and Castro2001). Considering the distribution of trawling efforts in all regions of Portugal (Northwest, Midwest, Southwest, and South), the landing ports in the south are the most critical recipients, accounting for an average of 64.8% nationwide. According to a three-year survey carried out by Bueno-Pardo et al. (Reference Bueno-Pardo, Ramalho, García-Alegre, Morgado, Vieira, Cunha and Queiroga2017), the port of Olhão was the second most important in terms of landing, corresponding to a trawling effort of 13,212 h, on average per year, which corresponds to 23% on a national level. Regarding discards, trawl fisheries in this region are responsible for an overwhelming 70% of the total discarded catch (Monteiro et al., Reference Monteiro, Araújo, Erzini and Castro2001; Erzini et al., Reference Erzini, Costa, Bentes and Borges2002).
Globalisation has led to a significant increase in biological invasions, with an ever-growing number of species being introduced into regions that are far from their native range. Although most of these introductions have negligible impacts, some result in competition with local species, the growth of invasive populations, and a general decrease in native biodiversity (e.g., Brooks et al., Reference Brooks, Mittermeier, Mittermeier, Da Fonseca, Rylands, Konstant, Flick, Pilgrim, Oldfield, Magin and Hilton-Taylor2002; Clavero and García-Berthou, Reference Clavero and García-Berthou2005; Burgess et al., Reference Burgess, Polasky and Tilman2013; Cahill et al., Reference Cahill, Aiello-Lammens, Fisher-Reid, Hua, Karanewsky, Yeong Ryu, Sbeglia, Spagnolo, Waldron, Warsi and Wiens2013). Consequently, it can incur significant economic costs through direct and indirect adverse impacts on ecosystem function and services (Diagne et al., Reference Diagne, Leroy, Vaissière, Gozlan, Roiz, Jarić, Salles, Bradshaw and Courchamp2021). Many aquatic ecosystems have been seriously affected by non-indigenous species (NIS), which can displace native organisms (i.e., predation and competition), modify the genetic characteristics of the populations through hybridisation, and introduce exotic diseases (Bax et al., Reference Bax, Williamson, Aguero, Gonzalez and Geeves2003). The impacts caused by NIS may be irreversible, particularly in the marine environment, where NIS that becomes invasive can be very difficult to eradicate once they have established self-sustaining populations (e.g., Green et al., Reference Green, Akins, Maljković and Côté2012; Sempere-Valverde et al., Reference Sempere-Valverde, Ostalé-Valriberas, Maestre, Aranda, Bazairi and Espinosa2021).
To the best of our knowledge, this is the first record of P. regalis in NPRF, and its presence may have several possible explanations. The most plausible reason for this is the discard by fishers when returning to their home port. However, this is a common Atlantic Sea cucumber, a deep-sea species (50 and 300 m depth) (Rámon et al., Reference Ramón, Lleonart and Massutí2010) and is a common by-catch in trawlers, which are usually discarded during the selection process, not rarely at the landing sites (Borges, Reference Borges2007). According to Tsagarakis et al. (Reference Tsagarakis, Nikolioudakis, Papandroulakis, Vassilopoulou and Machias2018), assessing the survival of discards in trawl fisheries in the Eastern Mediterranean Sea revealed that the survival rate of P. regalis after rejection was noticeably high, reaching almost 90% survival rate. This type of introduction vector is common worldwide and responsible for several species' introductions (Bailey et al., Reference Bailey, Brown, Campbell, Canning-Clode, Carlton, Castro, Chainho, Chan, Creed, Curd, Darling, Fofonoff, Galil, Hewitt, Inglis, Keith, Mandrak, Marchini, McKenzie, Occhipinti-Ambrogi, Ojaveer, Pires-Teixeira, Robinson, Ruiz, Seaward, Schwindt, Son, Therriault and Zhan2020). Given the observations made in other estuaries and the testimonies of local fishers, the discard hypothesis is the most plausible one to explain the occurrence of this specimen of royal sea cucumber. Through human activities, the royal sea cucumber and other species often incoming from distant shores can carry a hidden menace – parasites (e.g., Chalkowski et al., Reference Chalkowski, Lepczyk and Zohdy2018; Whalen et al., Reference Whalen, Millard-Martin, Cox, Lemay and Paulay2020). These hitchhiking parasites find new opportunities for transmission and infection in the novel ecosystems they encounter, whether by the introduction of NIS fish species hosting debilitating pathogens or the colonisation of invasive shellfish transporting microsporidian parasites (Graczyk et al., Reference Graczyk, Conn, Lucy, Minchin, Tamang, Moura and DaSilva2004; White et al., Reference White, Morado and Friedman2014; Moratal et al., Reference Moratal, Magnet, Izquierdo, del Águila, López-Ramon and Dea-Ayuela2023). In this case, P. regalis is known to host the earlfish Carapus acus. The occurrence of this fish depends mainly on host availability and distribution from potential larval areas (González-Wangüemert et al., Reference González-Wangüemert, Maggi, Valente, Martínez-Garrido and Vasco-Rodrigues2014).
The study area has a growing abundance of NIS, particularly Amanthia verticillata, Styela plicata, and the Mediterranean native Caulerpa prolifera (personal observations by the authors during the present UVC). Caulerpa prolifera has been recently and rapidly expanding to gain space in deeper unvegetated soft bottoms and compete with the local seagrasses in the shallower areas (Parreira et al., Reference Parreira, Martínez-Crego, Afonso, Machado, Oliveira, dos Santos Gonçalves and Santos2021). A further example of recently introduced NIS into the NPRF through maritime activities is the Atlantic blue crab (Callinectes sapidus), a Western Atlantic endemic species (Morais et al., Reference Morais, Gaspar, Garel, Baptista, Cruz, Cerveira, Leitão and Teodosio2019). This growing number of NIS and associated species in NPRF requires monitoring since the introduction of NIS is a human-assisted global phenomenon with devastating effects on biodiversity, ecosystem services, and human well-being (Hulme, Reference Hulme2009; Sheets et al., Reference Sheets, Cohen, Ruiz and da Rocha2016; Vilà and Hulme, Reference Vilà, Hulme, Vilà and Hulme2017). In addition, this study also highlights the need to incorporate biosecurity protocols in sensitive habitats. Prevention is the most effective method of avoiding or mitigating the impacts associated with unwanted NIS (e.g., Castro et al., Reference Castro, Ramalhosa, Jiménez, Costa, Gestoso and Canning-Clode2020, Reference Castro, Schäfer, Parretti, Monteiro, Gizzi, Chebaane, Almada, Henriques, Freitas, Vasco-Rodrigues, Silva, Radeta, Freitas and Canning-Clode2021). For example, the Ballast Water Management Convention (BWM Convention) is a biosecurity example adopted by the International Maritime Organization (IMO) to help avoid the spread of potentially harmful aquatic organisms and pathogens in ships' ballast water. Since September 2017, vessels must oversee their ballast water so that aquatic organisms and pathogens are eliminated or rendered harmless before being released into a new environment (IMO, 2020). Finally, implementing the best practice rules for discarding fisheries is a pressing issue for this sensitive region to avoid new introductions that might cause ecological and economic catastrophes.
Author Contributions
NC: conceptualisation, methodology, formal analysis, investigation, writing – original draft, writing – review and editing; FR: methodology, formal analysis, investigation, writing – original draft, writing – review and editing. PF: methodology, formal analysis, investigation, visualisation, writing – original draft, writing – review and editing.
Financial Support
NC is funded by a doctoral grant (https://doi.org/10.54499/SFRH/BD/146881/2019) awarded by Fundação para a Ciência e Tecnologia (FCT). FCT also funds FR (2022.03193.CEECIND). This study had the support of FCT through projects UIDB/04292/2020 (https://doi.org/10.54499/UIDB/04292/2020) and UIDP/04292/2020 (https://doi.org/10.54499/UIDP/04292/2020) awarded to MARE and through project LA/P/0069/2020 (https://doi.org/10.54499/LA/P/0069/2020). Civil Engineering Research and Innovation for Sustainability (CERIS) is also funded by FCT (UIDB/04625/2020).
Competing interest
The authors declare no conflict of interest.
Ethical Standards
None.
Data Availability
No new data were created or analysed during this study. Data sharing is not applicable to this article.
