The topshells Phorcus lineatus (da Costa, 1778) and Phorcus sauciatus (F.C.L. Koch, 1845) are herbivorous marine snails (Gastropoda: Vetigastropoda) belonging to the family Trochidae. These species are commonly found in shallow and sheltered shores and play important roles in intertidal food webs (Hickman and McLean 1990, Herbert 1992, Sousa et al. 2018), controlling algal growth, shaping intertidal communities and recycling nutrients (Knox 2000, Crothers 2001).

The species P. lineatus occurs in the upper half of the intertidal zone (Desai 1966), reaching its northern distribution limits in Wales and Ireland (Kendall 1987, Donald et al. 2012). Its distribution is continuous along the Portuguese, Spanish and French Atlantic coasts, and its southern limit is reached on the Atlantic coast of Morocco (Mieszkowska 2005). However, even within these areas its distribution is patchy and erratic (Fretter and Graham 1977). The species P. sauciatus is a common subtropical topshell with a northern limit in the Iberian Peninsula (Galicia) and the same southern limit as P. lineatus, and also occurs in the archipelagos of Madeira, Canary and more recently also in the Azores (Rubal et al. 2014, Costa 2015, Baptista et al. 2021).

These topshell species are commonly found on intertidal rocky shores along the coast of mainland Portugal (Macedo et al. 1999, Donald et al. 2012, Cabral 2020). Both species inhabit an extreme and dynamic coastal environment, which exposes them to thermal and hydric stresses (Raffaelli and Hawkins 1999, Ramírez et al. 2005).

Classical descriptions of the reproductive biology of diverse trochid species distributed elsewhere were reported by Williams (1965), Duch (1969), Underwood (1972, 1974a) and Grange (1976). However, the general knowledge on the biology and ecology of P. lineatus and P. sauciatus, especially on their reproductive cycle, is extremely scarce. The distribution and shell morphometrics of both species were analysed along the Portuguese coast by Costa (2015) and Vasconcelos et al. (2022). The zonation of P. sauciatus in Tenerife, Canary Islands, was studied by Alfonso et al. (2015), and its biological invasion in the Azores archipelago was reported by Ávila et al. (2015) and Baptista et al. (2021). Finally, the reproductive dynamics of P. lineatus in Asturias, Spain, was described by Bode et al. (1986).

Topshells are harvested for human consumption in some coastal communities. For instance, commercial and recreational harvesting of P. sauciatus are ancestral and traditional activities in the Madeira (Sousa et al. 2020), Azores (Ávila et al. 2015, Sousa et al. 2020) and Canary archipelagos (Ramírez et al. 2005, Tuya et al. 2006, Alfonso et al. 2015), whereas in mainland Portugal topshells are mainly collected recreationally and consumed locally and sporadically (Vasconcelos et al. 2022). In Portugal, the regulations currently in force for harvesting topshells (sensu lato) stipulate a minimum conservation reference size (MCRS=12 mm in shell height, D.R. 2011) for both commercial and recreational catches (D.R. 2014) of P. lineatus and P. sauciatus, in order to ensure the collection of mostly adult and mature individuals from exploited populations. In addition, information on the species’ reproductive cycle is also crucial to promote the sustainable management of commercially and recreationally exploited topshell populations (Underwood 1979, Perry et al. 1999, Boman et al. 2018).

The present study aimed to describe the gametogenic cycle of P. lineatus and P. sauciatus from southern Portugal, as well as to evaluate the influence of biologically/ecologically relevant atmospheric and oceanographic parameters on the reproductive dynamics of these sympatric intertidal species. Overall, this study delivers valuable baseline information for the proposal of management measures (namely seasonal closures for both professional and recreational harvesting activities), which might contribute to promote the long-term sustainable exploitation of these topshell species.

Like other topshell species, P. lineatus and P. sauciatus do not exhibit external sexual dimorphism (Desai 1966, Fretter and Graham 1977, Crothers 2001), so their sex is only distinguishable through gonadal examination (Sousa et al. 2018, 2020). These trochid gastropods showed a balanced sexual proportion during almost the entire two-year study period, except in a few months when significantly unbalanced and male-biased sex-ratios were recorded (one month for P. lineatus and three months for P. sauciatus). Bode et al. (1986) studied the P. lineatus population from northern Spain and also recorded a balanced sex ratio (1:1) in the overall sampled individuals. Similarly, no significant deviations from the expected parity sex ratio (1:1) were detected by Lasiak (1987) in three other trochid species (Monodonta australis, Oxystele tabularis and O. antoni) in the Transkei coast (South Africa). Mora et al. (2017) studied the trochid Cittarium pica in San Andrés Isla (Gran Caribe) and observed balanced sex-ratios (1:1), except in November when males prevailed over females. In contrast, the overall sex ratio of P. sauciatus in Madeira archipelago was female-biased (1:1.3), with females predominating almost year-round, except in February when males were more abundant (Sousa2019).

In the present study, both topshell species from the Algarve coast displayed synchronous gonadal development between sexes. Several studies have reported synchronized spawning between males and females in marine gastropods worldwide. For instance, Haliotis asinina from Heron Reef in Australia (Counihan et al. 2001), H. trunculus from Bizerte lagoon in northern Tunisia (Gharsallah et al. 2010) and Tegula eiseni (currently accepted as Agathistoma eiseni) from Bahía Asunción in Mexico (Vélez-Arellano et al. 2009) exhibited synchronized gametogenic development between sexes. Conversely, in the case of Tegula euryomphala collected in La Herradura Bay in Chile and studied under laboratory conditions, males spawned consistently before females (Romero Bastías 2014).

The same trend was also observed in topshell species belonging to the genus Phorcus. For instance, P. lineatus collected from Aberaeron, mid-Wales, showed a similar pattern of gonadal development between males and females throughout the year (Garwood and Kendall 1985). Moreover, in P. lineatus from Asturias, both sexes also behaved similarly during the study period (Bode et al. 1986). Likewise, P. sauciatus from Madeira archipelago showed a synchronous gametogenetic cycle between sexes, females and males exhibiting a similar gonadal pattern all year round with only minor dissimilarities in the proportion of mature individuals (Sousa 2019, Sousa et al. 2019).

Both P. lineatus and P. sauciatus from the Algarve coast showed a clear predominance of mature and spawning gonads throughout the reproductive cycle, which is probably related to successive processes of gonadal re-ripening and partial gametic emissions. This process was more evident in P. lineatus, whose individuals exhibited a continuous shift between mature and spawning gonads. Accordingly, both topshells exhibited an extensive spawning season, whereas resting or inactive gonads were only recorded during a short period or were completely absent. In northern Spain, P. lineatus also displayed an extensive spawning season (May–November) without a resting period in the reproductive cycle (Bode et al. 1986). Daguzan (1991) analysed P. lineatus from the Morbihan coast (France) and observed two reproductive periods per year, one in spring (April–June) and one in autumn (September–October).

By contrast, P. lineatus from Plymouth in England (Underwood 1972) and Craig-yr-Wylfa in North Wales (Williams 1965) displayed shorter spawning periods, between June and September and between August and October, respectively, followed by brief resting phases (Fretter and Graham 1977). Indeed, P. lineatus populations nearer to northern range limits (North Wales and North Ireland) appear to have a single spawning period, whereas those closer to the centre of the species distributional range have a longer spawning season comprising multiple spawning events (Garwood and Kendall 1985, Bode et al. 1986, Mieszkowska 2005). However, the literature on the reproductive cycle of P. sauciatus is extremely scarce, with only one study performed in the Madeira archipelago by Sousa (2019). According to this author, the continuous presence of mature and partially spawned individuals indicates that P. sauciatus is reproductively active all year round, with a main spawning season between March and August.

Such differences in topshell reproductive cycles are probably correlated with different environmental parameters. Several authors (e.g. Shanks et al. 2020, Shin et al. 2020, Sukhan et al. 2021) have stated that temperature influences gonad maturation and reproduction in marine gastropods. In general, populations in colder habitats display shorter development phases and more pronounced spawning periods than populations under warmer conditions (Crothers 2001). Furthermore, several studies on the reproductive cycle of Patagonian marine gastropods, namely Buccinanops cochlidium (Averbuj et al. 2010), Odontocymbiola magellanica (Bigatti et al. 2008), Tegula patagonica (currently accepted as Agathistoma patagonicum) (Nieto-Vilela et al. 2021) and Trophon geversianus (Cumplido et al. 2010), reported that increasing temperature seemed to induce spawning.

Indeed, in the present study the fluctuation of SST revealed inter-annual differences with an atypical pattern recorded in 2017. In fact, during 2017 the SST displayed slight oscillations, exhibiting sequential small increases and decreases between June and November, without reaching very high values (maximum of 22°C in September). In 2018, SST fluctuation showed a distinct pattern, with a gradual increase from March to October (maximum of 23.6°C in October), followed by a pronounced decrease. These dissimilarities in SST between years were reflected in the gametogenic cycles of both species. Individuals in maturity stages I (resting) and II (pre-active) were observed almost only in 2017, and were reflected in some declines in GI during the spring and summer of this year.

Molluscs can be characterized as bradytictic or tachytictic, depending on whether spawning occurs during short or extended periods, with spawning duration being often correlated to latitude, temperature and food availability (Boman et al. 2018, Melchior et al. 2023, Seinor et al. 2023). In addition, species with an extensive geographical distribution might display variable reproductive strategies in both time and intensity of spawning, which have also been related to latitude and its influence on temperature and food availability (Ward and Davis 2002, Freije and Al-Sayed 2009, Ramesh et al. 2010). Therefore, species’ reproductive dynamics and duration of spawning are characteristics of each population, linked to biological features and environmental conditions.

Some diversity has been observed in the reproductive cycles and spawning periods of gastropod species. Collin et al. (2017) studied six intertidal gastropod species in the Bay of Panama (Cerithideopsis californica, Crepidula cf. marginalis, Littoraria variegata, Nerita scabricosta, Notocochlis chemnitzii and Siphonaria maura) and reported strong differences in the intensity of reproduction and spawning peaks. Some marine gastropods seem to breed continuously throughout the year, while others have well-defined reproductive patterns, with distinct periods of gonad inactivity, gametogenesis and spawning. Indeed, some species release ripe gametes continuously throughout the year (e.g. Aranda et al. 2003, Di Stefano and Giménez 2022), while others display spawning peaks (e.g. Joll 1980, Joska and Branch 1993). Even species inhabiting the same location might exhibit dissimilar reproductive strategies and gametogenic cycles as a specific response to the local environment (Aranda et al. 2003, Collinet al. 2017). Lasiak (1987) reported lacking phylogenetic or geographic relationships in the pattern and timing of reproductive cycles of trochid topshells. Regarding trochoid species, diverse studies reported that Austrocochlea constricta (Underwood 1974b), Cantharidus capillaceus (Simpson 1977), Oxystele antoni and O. tabularis (Lasiak 1987) and Steromphala cineraria (Underwood 1972) appear to spawn several times throughout the year. Other trochoid species, such as P. lineatus and S. umbilicalis, have well-defined reproductive cycles with distinct periods of inactivity and spawning (Garwood and Kendall 1985). Moreover, since these topshell species are exposed to severe and instable environmental conditions (Raffaelli and Hawkins 1999, Ramírez et al. 2005), their reproductive cycles are expected to display some spatial and temporal fluctuations (Aranda et al. 2003).

In the present study, the mean GI of P. lineatus and P. sauciatus showed positive correlations with both air and seawater temperatures, meaning that increases in these environmental parameters prompted gonadal maturation and spawning. The mean GI of P. lineatus also displayed positive correlation with daylight duration. Several authors stated that fluctuations in seawater temperature appear to affect gamete development and duration of spawning in gastropod species (e.g. Aranda et al. 2014, Di Stefano and Giménez 2022). In addition, lowest winter temperatures can affect the survival of larvae and juveniles, subsequently impacting recruitment (Kendall et al. 1987). In addition to temperature, the photoperiod also seems to influence gamete release and reproductive activity in marine gastropod species (Himmelman 1999). For instance, the reproductive cycles of various Patagonian gastropods, such as Adelomelon ancilla (Penchaszadeh et al. 2009), B. cochlidium (Averbujet al. 2010), O. magellanica (Bigatti et al. 2008), and T. geversianus (Cumplido et al. 2010), appear to be regulated by the quantity of light hours.

Spawning in intertidal organisms appears to be also influenced by other atmospheric and oceanographic conditions, such as, high wind speed, strong wave action and increased phytoplankton (Underwood 1979, Freije and Al-Sayed 2009, Seinor et al. 2023). In particular, trochacean gastropod spawning seems to be also stimulated by intense water movement (Grange 1976). In the present study, a negative correlation was detected between P. lineatus GI and WH, indicating that this topshell species spawned preferentially under low-wave conditions. Such spawning behaviour was already expectable, because this species is an indicator of sheltered areas where organisms are more protected from wave action (Costa 2015). However, while calmer sea conditions might be advantageous to avoid larval dispersal after fertilization (Seinor et al. 2023), rough sea conditions might improve population connectivity (Grange 1976) and promote a quick transfer of larvae out of the surf zone, thus avoiding benthic predators (Shanks 1997, Gyory and Pineda 2011).

In addition, P. sauciatus GI showed a negative correlation with WS, meaning that spawning occurred preferentially under favourably weaker wind conditions. This species is apparently more tolerant to wave action than P. lineatus due to the larger foot and wider shell opening, which are helpful to deal with the risk of displacement by waves (Costa 2015). Furthermore, air temperature fluctuation and desiccation are key stress factors acting on rocky shore organisms (Bertness et al. 2006, Noke 2016). In particular, P. sauciatus is highly vulnerable to desiccation due to its large area of contact with the air (Costa 2015, Sousa 2019), which might supress body humidity under strong wind conditions.

In conclusion, both P. lineatus and P. sauciatus from the Algarve coast exhibited an extensive spawning season, with short resting phase and scarce inactive gonads throughout the year. The reproductive cycle of both species appeared to be influenced by various atmospheric and oceanographic parameters, namely air and seawater temperatures, wind speed and wave height. Overall, the information obtained in this study is relevant for proposing harvesting management measures for the long-term sustainable exploitation of this shellfish resource. Although the commercial harvesting of topshells along the coast of mainland Portugal, including the Algarve coast, can be considered residual (annual reported catches <100 kg in 2008–2014) (DOCAPESCA 2014), both commercial and recreational harvesting activities targeting these species still require suitable tailor-made regulations.

The species P. lineatus and P. sauciatus co-occurring in the rocky intertidal are relatively difficult to distinguish and are therefore harvested and sold altogether. Based on the extensive spawning period exhibited by both species and on the spawning peaks identified in 2017 and 2018, in order to avoid jeopardizing the harvesters profitability, it would be practical and beneficial to implement a two-month closure in the harvesting activity targeting both topshell species in southern Portugal in September and October. Similarly, in the Madeira archipelago, a closed season for P. sauciatus was proposed between February and May (Sousa 2019), whereas in some locations of Galicia (Spain) topshell harvesting can be banned during two consecutive months depending on specific management measures applied in each shellfish area (D.O.G. 2023). Finally, future studies should also estimate the size at first sexual maturity of both P. lineatus and P. sauciatus in the Algarve coast in order to confirm the suitability of the minimum conservation reference size for topshells currently in force in Portugal (MCRS=12mm, D.R. 2011), which is less stringent than in Galicia (Spain) (MCRS=15mm, D.O.G. 2012).