Larvae and juveniles – age-group 0
Sea surface temperature (SST) is considered one of the main environmental factors driven biological and ecological changes in the marine environment (Teixeira and Cabral, 2009; Baptista et al., 2018). Larval development in fish species is highly affected by the increase of temperature, accelerating planktonic larval duration and consequently survivorship (Pauly and Pullin, 1988; Pepin, 1991). In the case of flatfish species, SST has been reported to affect growth, maturity, spawning, and development of eggs, larvae, and juveniles (Rijnsdorp and Vingerhoed, 1994; Henderson and Seaby, 2005; Petitgas et al., 2012; Vinagre et al., 2013). In the present study, negative relationships between SST and LPUE of P. platessa were found in the Southwestern region during spring, corresponding to the end of the spawning season and development of early phases (eggs and larvae). These results are in accordance with previous findings reporting negative relationships between P. platessa year-class strength and water temperature in North Atlantic during spawning (van der Veer et al., 2000) and early life periods (van der Veer and Witte, 1999). Teal et al. (2008) also suggested that growth of age-group 0 P. platessa is determined by temperature. LPUE of Solea solea had also a negative relation with SST in Southwestern (spring and summer) and Southern coasts (spring and autumn). Although several studies found positive correlations between SST and Solea spp. in Portuguese estuaries (e.g., Vinagre et al., 2008; Ramos et al., 2009; Gamito et al., 2015), Rijnsdorp et al. (1992) reported that lower SST at the spawning season might enhance the reproductive success of S. solea. Cozzi and Giani (2011) also registered low recruitment rates in years with warm temperatures in Adriatic Sea. Solea solea is a temperate species with a metabolic optimum temperature estimated of 18.8°C (Lefrançois and Claireaux, 2003), possibly suffering thermal stress in Southwestern and Southern regions of Portuguese coast, with temperatures varying between 18.4 and 22.5°C during spring, summer, and autumn (
Table 2
). During these conditions, the ingestion rates decrease (Yamashita et al., 2001) as well as the growth rates, since the energy is spent to face unfavourable conditions, as previously described in Tagus Estuary (Southwestern coast- IXaCS) (Vinagre and Cabral, 2008; Vinagre et al., 2008). Still, egg mortality in P. platessa and S. solea has also been associated with the increase of pathogens activity caused by warm temperatures (Fonds, 1995; Henderson, 1998).
In addition, time-series analysis also revealed positive relationships between LPUE and SST for D. cuneata and Microchirus spp., beneficiating from winter (IXaS) and spring SST (IXaCS and IXaS), and matching with spawning and larval periods (Andrade, 1990; Santos and Lino, 2010;
Table 1
). As reported by Lange and Greve (1997), temperature influences the rate of gonadal maturation and spawning time, and consequently recruitment of flatfish species. Désaunay et al. (2006) also reported that winter warming can be favourable for growth and survival of D. cuneata early phases in the Bay of Biscay. Increases in SST may also influence other marine trophic levels such as phytoplankton and zooplankton communities (Colebrook, 1982; Tunberg and Nelson, 1998), important food resources for flatfish larvae. Furthermore, D. cuneata had a subtropical range distribution (Froese and Pauly, 2016) tolerating warmer temperatures than other flatfish species occurring in these waters. In fact, Teixeira et al. (2014) reported the increase of D. cuneata landings in warm years in Portuguese coast. Microchirus spp. LPUE was also positively related with both winter and spring SST, corresponding to their spawning period (February to June; Andrade, 1990;
Table 1
). Therefore, favourable SST conditions might determine an early spawning and decrease pelagic larval duration (O’Connor et al., 2007) increasing the settlement success through larval retention (Lacroix et al., 2018). Microchirus spp. are a temperate species with a remarkably southern distribution (Quéro et al., 1986) taking advantage of warmer SST conditions. Teixeira and Cabral (2009) reported that temperature was the most important predictor explaining Microchirus azevia landings, by its effects on food resources. Also, Teixeira et al. (2014) and Gamito et al. (2015) demonstrated that Microchirus spp. landings were higher in warm years and lower during cold periods.
Although the same North Atlantic Oscillation (NAO) Index was used for all the regions, LPUE of different flatfish species were associated to it in different regions of the Portuguese coast. The NAO Index was positively related to LPUE of P. platessa (IXaCN and IXaS), Microchirus spp. and S. lascaris (IXaCS) during winter, coinciding with their spawning season and the beginning of the larval period (Andrade, 1990; Félix et al., 2011;
Table 1
). Thus, high biomass was observed during positive NAO periods, characterized, in the Southern Europe, by a predominance of relatively lower SST (Henriques et al., 2007) and Northern wind conditions favouring upwelling and productivity (Huthnance et al., 2002; Borges et al., 2003; Santos et al., 2004). The correlation between NAO and recruitment of Microchirus spp. and S. solea was previously observed in the Portuguese coast (Gamito et al., 2015). It was related with S. solea growth, due to the possible relation with productivity and food availability (phytoplankton and zooplankton) (Henderson and Seaby, 2005). Also, cold winters could favour the spawning processes of some flatfish species, as previously reported for P. platessa and S. solea (e.g., Rijnsdorp et al., 1992; van der Veer and Witte, 1999), and may also reduce eggs and larval mortality due to lower predator activity or to the match between larval production and their food (Cushing, 1972; Leggett and Deblois, 1994).
Upwelling (UPW) events usually occur along the Portuguese coast during spring and summer (Leitão et al., 2019;
Table 2
) when equatorward winds occur for consecutive days (Relvas et al., 2007; Vinagre et al., 2007). During upwelling events, the surface water is pushed offshore being replaced by deep, cool, and nutrient enriched waters favouring biological production. Generally, drifting larvae is hampered by these oceanographic events, threatening the chance of flatfish early stages to reach the nursery grounds close to the coast (Vinagre et al., 2008; Vinagre et al., 2007). Thus, upwelling events can have opposite effects on fish larvae and juveniles. Pleuronectes platessa and D. cuneata were negatively correlated with upwelling in summer (Southwest) and spring (South), respectively. These seasons corresponded to the higher upwelling index registered in each region (
Table 2
), increasing the offshore advection of larvae (Guisande et al., 2001; Landaeta and Castro, 2002) and affecting the recruitment success. Contrarily, Microchirus spp. LPUE was found to be positively related with summer (IXaCN) and autumn (IXaS) upwelling, as well as S. solea with spring and summer upwelling (IXaCS). Although upwelling provokes the offshore advection of the surface water layer, several mechanisms can retain larvae in the nursery grounds near the coast (Gibson, 1994; Moita et al., 2003; Vinagre et al., 2007). It is the case of upwelling shadow zones that may play an important role in the retention of flatfish early stages preventing their offshore advection (Moita et al., 2003; Mason et al., 2005).
Coastal drift currents are affected by wind strength and direction (Moita, 1986; Melo, 1989; Vila-Concejo et al., 2003) influencing the transport and/or the retention of eggs and larvae along the coastline through changes in hydrodynamics (Jager, 2001; Borges et al., 2007; Vinagre et al., 2009; Lacroix et al., 2018), and food supply (Fernández et al., 1993; Santos et al., 2012). Wind magnitude also influences the dispersal of the river plumes into the sea, helping larvae to successfully reach estuarine nursey areas (Tanaka, 1985; Vinagre et al., 2007) by using the chemical cues released by the river discharge and spread by the force of the wind (e.g., Gibson, 1997; Arvelund and Takemura, 2006). Thus, as reported by several authors, the recruitment of flatfish species is related to prevailing wind conditions (e.g., Werner et al., 1997; Nielsen et al., 1998; van der Veer et al., 2000). In the present study, the increase of wind strength negatively affected the LPUE of P. platessa and S. solea during summer (IXaS) and autumn (IXaCN) probably by promoting the larval dispersion from the nursery areas in a way that larval mortality was also enhanced (Vinagre et al., 2009; Lacroix et al., 2018) and by increasing turbidity in shallow waters (Gibson, 1994; Laffargue et al., 2007). On the other hand, S. lascaris larvae have been also found to benefit from the increase of river plumes (Vinagre et al., 2007) and retention in coastal areas (Vinagre et al., 2009) caused by the increase of summer wind magnitude (Southwest). The LPUE of Microchirus spp. was negatively related to wind magnitude during winter (IXaCS) and spring (IXaCN), and positively during summer (IXaS), revealing the importance of regionality and seasonality for recruitment.
Together with wind magnitude, the variability of the wind direction also played an important role on larval transport (Lacroix et al., 2018). In fact, in our study, D. cuneata and Microchirus spp. LPUE were positively related with Westerly winds (UWIND) in Southern coast (IXaS) during spring and autumn, respectively, meaning that recruitment was higher when the wind blew from the west. These winds are responsible for upwelling conditions in the Southern coast of Portugal (Fiúza, 1983; Baptista et al., 2016), but with less intensity than on the Western coast (IXaCN and IXaCS) due to the oceanographic characteristics. Therefore, it is more likely that these winds might influence the surface coastal drift current retaining eggs and larvae in the coastal areas and preventing them to run away to the open sea. On the contrary, negative relationships were found in P. platessa (IXaCS and IXaS), S. lascaris (IXaS), D. cuneata and S. solea (IXaCS). In these cases, recruitment enhanced when the winds bellow from the East, corresponding to downwelling conditions in Southern coast of Portugal (Fiúza, 1983; Baptista et al., 2016). Therefore, winds blowing from the east may enhance the retention of flatfish eggs and larvae in coastal areas (Moita, 1986; Vinagre et al., 2009; Baptista et al., 2016). Furthermore, specific characteristics, such as temperature, salinity, and nutrients of the water transported by the Easterly winds (e.g., from the Mediterranean Sea in Southern regions) might have a positive effect on the survivorship of flatfish larvae, improving the recruitment success and consequently, the landings on the following years. In relation to the Northerly wind component (VWIND), winds from South increased the recruitment of Microchirus spp. during winter in Southern region. These winds seem to transport and retain larvae in coastal nursery areas (Vinagre et al., 2009). Contrarily, in Western coast, winds from North (negative values) improved the recruitment of D. cuneata during spring (IXaCN and IXaCS), and S. lascaris and S. solae during summer (IXaCS). In Western coast of Portugal, these winds are responsible for upwelling events (Relvas et al., 2007), increasing biological production (Vinagre et al., 2007) and recruitment of flatfish species.
Variability in river discharges has important consequences for recruitment of fish species, leading to changes in salinity, organic matter input, food abundance and currents (Vinagre et al., 2007). Pleuronectes platessa and Microchirus spp. LPUE were positively related with spring river discharge, and D. cuneata with winter river discharge, that matches with the seasons where these species spawn and larval development occurs (Andrade, 1990; Santos and Lino, 2010; Félix et al., 2011;
Table 1
). Microchirus spp. LPUE also were positively related to river discharges during autumn, corresponding to a post-metamorphosis and juvenile phase. In fact, larvae living on the coast take advantage of the increase of food abundance driven by the inputs of organic matter from the river discharges (Cushing, 1996; Lloret et al., 2001). The positive relationship between river discharge and the landings of marine fish in Portugal has been recently described using multiple DFA models (Bueno-Pardo et al., 2020), resulting to be especially relevant in the South region during winter. Larvae of various organisms can follow cues released by river plumes such as odour, temperature, salinity and turbidity (e.g., Gibson, 1997; Arvelund and Takemura, 2006) which cloud orient them to the coastal nursery areas where food resources and refuge are available (Tanaka, 1985; Tamburri et al., 1996). Thus, high river discharge increases the river plumes to a wider area, increasing the possibility of being detected by flatfish larvae spawned on the coast (Vinagre et al., 2007). On the other hand, river discharges can also have negative impacts on flatfish LPUE, such as S. solae during spring at the Northwestern region. Despite being described that S. solea larvae benefit from the increase of river discharges to ingress into Portuguese estuaries (Martinho et al., 2010; Vinagre et al., 2007; Martinho et al., 2009), Ramos et al. (2009) reported that this species is not able to migrate into Lima estuary (Northwest) due to the increase of river flow enhancing turbidity. Turbidity, an indirect consequence of the river runoff, can affect the passive tidal migration of flatfish larvae (Ramos et al., 2009). Thus, years with high river discharges during spring, when larvae ingress into nursery habitats, could compromise their estuarine migration, and consequently the recruitment of S. solea.
Juveniles to young-adults – age-groups I and II
After spending the first months (at least six months) in coastal nursery grounds to complete their development, many juveniles of flatfish species migrate into deeper coastal waters (Dorel et al., 1991; Gibson, 1997), where they will grow and reach sexual maturity, returning or not to inshore habitats during their life cycle (Gibson, 1997). Thus, as shown by present results, the effects of environmental variability on age-groups I and II of flatfish species seems to be related with growth and maturation. In fact, Fuiman (1997) described the juvenile phase as a period dominated by growth, and the adulthood a period dominated by reproduction. As previously reported, the SST could affect metabolic and physiological rates (Brander et al., 2003) and food availability (Cushing, 1990) which in turn affect growth of flatfish juveniles (Yamashita et al., 2001; Teal et al., 2008), since the energy expended for growth will be diverted to face adverse temperatures (Vinagre et al., 2008). In fact, despite flatfishes are quite sedentary, they can perform small migrations to avoid unfavourable conditions, like temperature (Marchand, 1991). Temperature could also affect the duration of maturation of flatfish species by its influence on gonadal maturation (Lange and Greve, 1997). Beyond the thermal conditions, hydrographic conditions could also have an impact on distribution and abundance of juvenile and young-adult flatfishes (Yeung and Yang, 2017), such as coastal currents affected by wind strength and direction. Yet, juveniles and adults living on the coast could also take advantage of the increase of food abundance driven by the inputs of organic matter from the river discharges (Cushing, 1996; Lloret et al., 2001).
It should be noted that in most cases where the environmental effect was repeated from one year to the next, this effect occurred in the following year, that is, if the effect occurred in the age-group 0, it was repeated in the age-group I and not in the age-group II. In other words, it appears that the effects of environmental variability over the life cycle of flatfish species have a gradual transition over the life cycle phases. Also, although there are some effects of environmental variability during the juvenile-young-adults’ phases (age-groups I and II), these effects are stronger during the larval-juvenile phase (age-group 0), as previously described. For example, it was reported that the year-class abundance is determined by environmental factors experienced early in life in many temperate flatfish species, like plaice (P. platessa) (e.g., van der Veer et al., 1990), sole (S. solea) (Rijnsdorp et al., 1992; Henderson and Seaby, 1994), flounder (Platichthys flesus) (van der Veer et al., 1991; Henderson and Seaby, 1994), and dad (Limanda limanda) (Henderson and Seaby, 1994). Thus, the year-class strength of flatfish species is fixed by the end of the first year (Henderson and Seaby, 1994).