Reproductive dynamics of the sympatric topshells Phorcus lineatus and Phorcus sauciatus (Gastropoda: Trochidae) on a rocky intertidal coast in southern Portugal

Introduction

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 1990Hickman C.S., McLean J.H. 1990. Systematic revision and suprageneric classification of trochacean gastropods. Science Series of Natural History Museum of Los Angeles County, Los Angeles, 35: 1-169.
, Herbert 1992Herbert D.G. 1992. Revision of the Umboniinae (Mollusca: Prosobranchia: Trochidae) in southern Africa and Mozambique. Ann. Natal Mus. 33: 379-459.
, Sousa et al. 2018Sousa R., Delgado J., González J.A., et al. 2018. Marine snails of the genus Phorcus: Biology and ecology of sentinel species for human impacts on the rocky shores. In: Ray, S. (ed), Biological resources of water. IntechOpen, Rijeka. pp. 141-167. https://doi.org/10.5772/intechopen.71614
), controlling algal growth, shaping intertidal communities and recycling nutrients (Knox 2000Knox G.A. 2000. The ecology of seashores. CRC Press, Boca Raton, Florida, 576 pp. https://doi.org/10.1201/9781420042634
, Crothers 2001Crothers J.H. 2001. Common topshells: an introduction to the biology of Osilinus lineatus with notes on other species in the genus. Field Stud. 10: 115-160.
).

The species P. lineatus occurs in the upper half of the intertidal zone (Desai 1966Desai B.N. 1966. The biology of Monodonta lineata (Da Costa). Proc. Malacol. Soc. Lond. 37: 1-17.
), reaching its northern distribution limits in Wales and Ireland (Kendall 1987Kendall, M.A. 1987. The age and size structure of some northern populations of the trochid gastropod Monodonta lineata. J. Mollus. Stud. 53: 213-222. https://doi.org/10.1093/mollus/53.2.213
, Donald et al. 2012Donald K.M., Preston J., Williams S.T., et al. 2012. Phylogenetic relationships elucidate colonization patterns in the intertidal grazers Osilinus Philippi, 1847 and Phorcus Risso, 1826 (Gastropoda: Trochidae) in the northeastern Atlantic Ocean and Mediterranean Sea. Mol. Phylogenet. Evol. 62(1): 35-45. https://doi.org/10.1016/j.ympev.2011.09.002
). 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 2005Mieszkowska N. 2005. Changes in the biogeographic distribution of the trochidae gastropods Osilinus lineatus (da Costa) and Gibbula umbilicalis (da Costa) in response to global climate change: range dynamics and physiological mechanisms. PhD thesis, Univ. Plymouth, 188 pp. https://pearl.plymouth.ac.uk/bms-theses/124/
). However, even within these areas its distribution is patchy and erratic (Fretter and Graham 1977Fretter V., Graham A. 1977. The Prosobranch Molluscs of Britain and Ireland Part 2 - Trochacea. J. Mollus. Stud. 3: 1-64.
). 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. 2014Rubal M., Veiga P., Moreira J., et al. 2014. The gastropod Phorcus sauciatus (Koch, 1845) along the north-west Iberian Peninsula: filling historical gaps. Helgol. Mar. Res. 68: 169-177. https://doi.org/10.1007/s10152-014-0379-2
, Costa 2015Costa M.A. 2015. Distribution and shape analysis of Phorcus lineatus and Phorcus sauciatus along the Portuguese coast. MSc thesis, Univ. Lisboa, 68 pp.
, Baptista et al. 2021Baptista L., Santos A.M., Melo C.S., et al. 2021. Untangling the origin of the newcomer Phorcus sauciatus (Mollusca: Gastropoda) in a remote Atlantic archipelago. Mar. Biol. 168: 9. https://doi.org/10.1007/s00227-020-03808-5
).

These topshell species are commonly found on intertidal rocky shores along the coast of mainland Portugal (Macedo et al. 1999Macedo M.C.C., Macedo M.I.C., Borges J.P. 1999. Conchas marinhas de Portugal. Editorial Verbo, Lisboa, 516 pp.
, Donald et al. 2012Donald K.M., Preston J., Williams S.T., et al. 2012. Phylogenetic relationships elucidate colonization patterns in the intertidal grazers Osilinus Philippi, 1847 and Phorcus Risso, 1826 (Gastropoda: Trochidae) in the northeastern Atlantic Ocean and Mediterranean Sea. Mol. Phylogenet. Evol. 62(1): 35-45. https://doi.org/10.1016/j.ympev.2011.09.002
, Cabral 2020Cabral J.P.S. 2020. Morphological variability of Phorcus lineatus (da Costa, 1778) shells along the coast of Portugal and the significance of the environment on shell morphology. Thalassas Int. J. Mar. Sci. 36: 9-22. https://doi.org/10.1007/s41208-019-00187-7
). Both species inhabit an extreme and dynamic coastal environment, which exposes them to thermal and hydric stresses (Raffaelli and Hawkins 1999Raffaelli D., Hawkins S.J. 1999. Intertidal ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, 356 pp.
, Ramírez et al. 2005Ramírez R., Tuya F., Sánchez-Jerez P., et al. 2005. Population structure and spatial distribution of the gastropod molluscs Osilinus atrata and Osilinus sauciatus in the rocky intertidal zone of the Canary Islands (Central East Atlantic). Cienc. Mar. 31(4): 697-706. https://doi.org/10.7773/cm.v31i4.35
).

Classical descriptions of the reproductive biology of diverse trochid species distributed elsewhere were reported by Williams (1965)Williams E.E. 1965. The growth and distribution of Monodonta lineata (da Costa) on a rocky shore in Wales. Field Stud. 2: 189-198.
, Duch (1969) Duch T.M. 1969. Spawning and development in the trochid gastropod Euchelus gemmatus (Gould, 1841) in the Hawaiian Islands. Veliger 11: 415-417.
, Underwood (1972Underwood A.J. 1972. Observations on the reproductive cycles of Monodonta lineata, Gibbula umbilicalis and Gibbula cineraria. Mar. Biol. 17: 333-340. https://doi.org/10.1007/BF00366744
, 1974a)Underwood A.J. 1974a. On models for reproductive strategies in marine benthic invertebrates. Am. Nat. 108(964): 874-878. https://doi.org/10.1086/282962
and Grange (1976)Grange K.R. 1976. Rough water as a spawning stimulus in some trochid and turbinid gastropods. N.Z.J. Mar. Freshw. Res. 10: 203-216. https://doi.org/10.1080/00288330.1976.9515607
. 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)Costa M.A. 2015. Distribution and shape analysis of Phorcus lineatus and Phorcus sauciatus along the Portuguese coast. MSc thesis, Univ. Lisboa, 68 pp.
and Vasconcelos et al. (2022)Vasconcelos P., Santos A.C.N., Pereira F., et al. 2022. Shell morphology, morphometric relationships and relative growth of three topshell species (Gastropoda: Trochidae) from the Algarve coast (southern Portugal). Thalassas 38, 665-674. https://doi.org/10.1007/s41208-021-00351-y
. The zonation of P. sauciatus in Tenerife, Canary Islands, was studied by Alfonso et al. (2015)Alfonso B., Sarabia A., Sancibrián I., et al. 2015. Efecto de la actividad humana sobre la distribución y estructura poblacional del burgado Phorcus sauciatus (Koch, 1845). Rev. Acad. Canar. Cienc. 27: 333-343.
, and its biological invasion in the Azores archipelago was reported by Ávila et al. (2015)Ávila S.P., Madeira P., Rebelo A.C., et al. 2015. Phorcus sauciatus (Koch, 1845) (Gastropoda: Trochidae) in Santa Maria, Azores archipelago: The onset of a biological invasion. J. Mollus. Stud. 81: 516-521. https://doi.org/10.1093/mollus/eyv012
and Baptista et al. (2021)Baptista L., Santos A.M., Melo C.S., et al. 2021. Untangling the origin of the newcomer Phorcus sauciatus (Mollusca: Gastropoda) in a remote Atlantic archipelago. Mar. Biol. 168: 9. https://doi.org/10.1007/s00227-020-03808-5
. Finally, the reproductive dynamics of P. lineatus in Asturias, Spain, was described by Bode et al. (1986)Bode A., Lombas I., Anadon N. 1986. Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiologia 142: 31-39. https://doi.org/10.1007/BF00026745
.

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. 2020Sousa R., Vasconcelos J., Riera R. 2020. Unravelling the effects of exploitation on the size-structure of the intertidal topshell Phorcus sauciatus in harvested and non-harvested Atlantic regions. Reg. Stud. Mar. Sci. 30: 104273. https://doi.org/10.1016/j.rsma.2020.101387
), Azores (Ávila et al. 2015Ávila S.P., Madeira P., Rebelo A.C., et al. 2015. Phorcus sauciatus (Koch, 1845) (Gastropoda: Trochidae) in Santa Maria, Azores archipelago: The onset of a biological invasion. J. Mollus. Stud. 81: 516-521. https://doi.org/10.1093/mollus/eyv012
, Sousa et al. 2020Sousa R., Vasconcelos J., Riera R. 2020. Unravelling the effects of exploitation on the size-structure of the intertidal topshell Phorcus sauciatus in harvested and non-harvested Atlantic regions. Reg. Stud. Mar. Sci. 30: 104273. https://doi.org/10.1016/j.rsma.2020.101387
) and Canary archipelagos (Ramírez et al. 2005Ramírez R., Tuya F., Sánchez-Jerez P., et al. 2005. Population structure and spatial distribution of the gastropod molluscs Osilinus atrata and Osilinus sauciatus in the rocky intertidal zone of the Canary Islands (Central East Atlantic). Cienc. Mar. 31(4): 697-706. https://doi.org/10.7773/cm.v31i4.35
, Tuya et al. 2006Tuya F., García-Diez C., Espino F., et al. 2006. Assessment of the effectiveness of two marine reserves in the Canary Islands (eastern Atlantic). Cienc. Mar. 32(3): 505-522. https://doi.org/10.7773/cm.v32i3.1133
, Alfonso et al. 2015Alfonso B., Sarabia A., Sancibrián I., et al. 2015. Efecto de la actividad humana sobre la distribución y estructura poblacional del burgado Phorcus sauciatus (Koch, 1845). Rev. Acad. Canar. Cienc. 27: 333-343.
), whereas in mainland Portugal topshells are mainly collected recreationally and consumed locally and sporadically (Vasconcelos et al. 2022Vasconcelos P., Santos A.C.N., Pereira F., et al. 2022. Shell morphology, morphometric relationships and relative growth of three topshell species (Gastropoda: Trochidae) from the Algarve coast (southern Portugal). Thalassas 38, 665-674. https://doi.org/10.1007/s41208-021-00351-y
). 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. 2011D.R. 2011. Portaria Nº 82/2011 de 22 de fevereiro que estabelece tamanhos mínimos para algumas espécies de invertebrados marinhos, aplicáveis em águas sob soberania e jurisdição nacional. Diário da República 1ª Série Nº 37: 886-887.
) for both commercial and recreational catches (D.R. 2014D.R. 2014. Portaria Nº 14/2014 de 23 de janeiro que define as artes permitidas, condicionamentos, termos do licenciamento e taxas aplicáveis ao exercício da pesca lúdica em águas oceânicas, em águas interiores marítimas ou em águas interiores não marítimas sob jurisdição da autoridade marítima. Diário da República 1ª Série Nº 16: 474-479.
) 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 1979Underwood A.J. 1979. The ecology of intertidal gastropods. Adv. Mar. Biol. 16: 111-210. https://doi.org/10.1016/S0065-2881(08)60293-X
, Perry et al. 1999Perry R.I., Walters C.J., Boutillier J.A. 1999. A framework for providing scientific advice for the management of new and developing invertebrate fisheries. Rev. Fish. Biol. Fisher. 9: 125-150. https://doi.org/10.1023/A:1008946522213
, Boman et al. 2018Boman E.M., de Graaf M., Nagelkerke L.A.J., et al. 2018. Variability in size at maturity and reproductive season of queen conch Lobatus gigas (Gastropoda: Strombidae) in the Wider Caribbean Region. Fish. Res. 201: 18-25. https://doi.org/10.1016/j.fishres.2017.12.016
).

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.

Materials and methods

Study area and field sampling

 ⌅

Topshells of both P. lineatus and P. sauciatus were caught manually during low tide in Praia da Luz (37°05.1’N, 08°43.8’W), a rocky shore in the municipality of Lagos (Algarve coast, southern Portugal) (Fig. 1). Approximately 20 specimens of each species were collected monthly during two consecutive years (January 2017–December 2018). In the laboratory, specimens were separated by species, counted, measured for shell height (SH) using a digital calliper (precision=0.01 mm) and weighed for total weight on a top-loading digital balance (precision=0.01 g).

Fig. 1.  Map showing the location of the collecting site (black box) for the topshells Phorcus lineatus and Phorcus sauciatus on intertidal rocky shores at Praia da Luz in Lagos (Algarve coast, southern Portugal).

In order to analyse their possible influence on the species reproductive dynamics, data on surface seawater temperature (SST) and significant wave height (WH) recorded during the study period at the Faro oceanographic buoy (closest buoy to the collecting site: 36°54.3'N, 07°53.9'W) of the Portuguese Hydrographic Institute (I.H. 2020I.H. 2020. Dados de temperatura da água e altura da onda registados na boia oceanográfica costeira de Faro (2016-2018). Lisboa: Instituto Hidrográfico (IH).
) was collected. In addition, data on air temperature (AT), daylight duration (DD) and wind speed (WS) recorded in the same period at the Faro airport station (37°01.2'N, 07°58.2'W) were acquired from Weather Underground (2024)Weather Underground 2024. “Weather History for Faro Airport Station, Faro, Portugal: Daily observations between January 2017 and December 2018.” Last modified April 15, 2024. https://www.wunderground.com/history/monthly/pt/montenegro/LPFR/date/2017-1 .
.

Results

Gonad histology and reproductive cycle

 ⌅

Photomicrographs of histological sections of P. lineatus and P. sauciatus, showing the various gonad maturity stages and the most relevant features of gametogenesis, are illustrated in Figures 2 and 3, respectively. Both topshell species are dioecious (i.e. have separate sexes) and their reproductive cycles exhibited similar patterns, with general synchronization between sexes (Figs. 4 and 5). For both species, the Spearman (ρ) correlations established between the monthly frequency of males and females at each gonad maturity stage during the two-year study period confirmed the synchronism in the reproductive cycle between sexes (Table 1). The monthly frequencies of P. lineatus and P. sauciatus at each stage of gonad maturity are presented in Figures 6 and 7, respectively. Both species displayed residual occurrence of inactive gonads (stage I – resting) and extended periods with prevailing mature (stage IV – ripe) and spawning individuals (stage V – partially spent).

Fig. 2.  Histological sections displaying the gonad maturity stages in males (left) and females (right) of Phorcus lineatus from the Algarve coast (southern Portugal): A, pre-active; B, active; C, ripe; D, partially spent; E, spent. Abbreviations: MO, mature oocytes; MS, mature spermatozoa; OA, oocyte atresia; PO, previtellogenic oocytes; SI, spermatids; SO, spawned oocyte; ST, spermatozoa tails. Scale bars: 200 µm.

Fig. 3.  Histological sections displaying the gonad maturity stages in males (left) and females (right) of Phorcus sauciatus from the Algarve coast (southern Portugal): A, pre-active; B, active; C, ripe; D, partially spent; E, spent. Abbreviations: MO, mature oocytes; MS, mature spermatozoa; OA, oocyte atresia; PO, previtellogenic oocytes; SI, spermatids; SO, spawned oocyte; ST, spermatozoa tails. Scale bars: 200 µm.

Fig. 4.  Monthly frequency of Phorcus lineatus males and females at each gonad maturity stage during the two-year study period on the Algarve coast, southern Portugal.

Fig. 5.  Monthly frequency of Phorcus sauciatus males and females at each gonad maturity stage during the 2-year study period on the Algarve coast, southern Portugal.

Table 1.  Spearman (ρ) correlations established between the monthly frequency (%) of Phorcus lineatus and P. sauciatus males and females at each gonad maturity stage during the two-year study period on the Algarve coast, southern Portugal. (M, males; F, females; gonad maturity stages I, II, III, IV, V and IV).

		Stage I	Stage II	Stage III	Stage IV	Stage V	Stage VI
Phorcus lineatus	(M×F)	ρ=0.988 P<0.001	ρ=0.603 P=0.002	ρ=0.766 P<0.001	ρ=0.754 P<0.001	ρ=0.696 P<0.001	ρ=0.674 P<0.001
Phorcus sauciatus	(M×F)	ρ=0.960 P<0.001	ρ=0.662 P<0.001	ρ=0.876 P<0.001	ρ=0.551 P=0.005	ρ=0.790 P<0.001	ρ=0.413 P=0.045

In general, P. lineatus displayed a very short resting period in 2017, which was virtually absent in 2018 (as evidenced by the scarcity of inactive and less developed gonads). Specimens at earlier developmental stages (II and III) were found between January and April 2017, and those stages were much rarer in 2018, with only a few ripe individuals (III) occurring mostly between March and June. Except in early 2017, P. lineatus showed ripe and spawning gonads (IV and V) almost throughout the entire study period (Fig. 6).

Fig. 6.  Monthly frequency of gonad maturity stages in Phorcus lineatus during the two-year study period on the Algarve coast, southern Portugal.

Similarly, inactive gonads of P. sauciatus were quite scarce and only observed in a few months spread through 2017. Pre-active and active individuals (stages II and III) were mostly recorded from January to April 2017 and between February and May 2018. The topshell P. sauciatus also exhibited a continuous presence of spawning gonads during long periods, nearly all individuals being assigned to stages IV (ripe) and V (partially spent) between May 2017 and January 2018 and from June to December 2018 (Fig. 7).

Fig. 7.  Monthly frequency of gonad maturity stages in Phorcus sauciatus during the two-year study period on the Algarve coast, southern Portugal.

Atmospheric and oceanographic parameters vs mean gonadal index

 ⌅

The months with lowest and highest mean values of atmospheric and oceanographic parameters recorded in 2017 and 2018 are summarized in Table 2. The mean GI of both topshell species displayed positive correlations with air and seawater temperatures, namely P. lineatus (AT, ρ=0.638, P<0.01; SST, ρ=0.597, P<0.01) and P. sauciatus (AT, ρ=0.483, P<0.05; SST, ρ=0.680, P<0.01). The mean GI of P. lineatus showed a positive correlation with daylight duration (DD, ρ=0.421, P<0.05). By contrast, the topshells’ mean GIs appeared to be negatively influenced by other atmospheric and oceanographic parameters, namely WS and WH. Indeed, negative correlations were obtained between P. lineatus GI and WH (ρ=−0.584, P<0.01) and between P. sauciatus GI and WS (ρ=−0.523, P<0.01) (Table 3).

Table 2.  Lowest and highest monthly mean values of atmospheric and oceanographic parameters recorded during the two-year study period on the Algarve coast, southern Portugal. (AT, air temperature; SST, surface seawater temperature; DD, daylight duration; WS, wind speed; WH, wave significant height).

	2017		2018
	Minimum	Maximum	Minimum	Maximum
AT (ºC)	Feb 13.2±1.8	Sep 24.7±1.4	Feb 11.8±1.8	Aug 25.7±2.5
SST (ºC)	Feb 15.4±0.4	Sep 22.0±1.9	Mar 14.7±0.4	Oct 23.6±0.8
DD (h)	Jan 9.7	Jul 14.7	Jan 9.8±0.1	Jul 14.7±0.1
WS (km/h)	Oct 12.4±3.8	Feb 17.4±8.0	Sep/Dec 12.4±2.6; 12.4±5.0	Apr 19.8 ±6.5
WH (m)	Aug – Oct 0.7±0.2	Feb 1.4±0.6	Jul/Sep 0.6±0.2	Apr/Dec 1.2±0.4; 1.2±0.5

Table 3.  Spearman (ρ) correlations established between the mean gonadal index (GI) of Phorcus lineatus and P. sauciatus and diverse atmospheric/oceanographic parameters (AT, air temperature; SST, surface seawater temperature; DD, daylight duration; WS, wind speed; WH, wave significant height) recorded during the two-year study period on the Algarve coast, southern Portugal. Statistically significant correlations (P<0.05) are highlighted in bold.

	AT	SST	DD	WS	WH
Phorcus lineatus GI	ρ=0.638 P=0.001	ρ=0.597 P=0.002	ρ=0.421 P=0.041	ρ=−0.283 P=0.180	ρ=−0.584 P=0.003
Phorcus sauciatus GI	ρ=0.483 P=0.017	ρ=0.680 P=0.000	ρ=0.097 P=0.653	ρ=−0.523 P=0.009	ρ=−0.353 P=0.091

The temporal variation in the mean GI of both topshells species and the respective relationships with relevant atmospheric and oceanographic parameters are illustrated in Figure 8. The GI displayed monthly oscillations throughout the study period, closely reflecting the reproductive cycle of both species. In practice, increasing trends in mean GI reflect gradual gonadal maturation and subsequent spawning events. Higher GIs in both species, corresponding to gonadal ripening and spawning, were spread several times over the two-year study period. In 2017, P. lineatus showed higher GI in July (4.88), P. sauciatus in June (4.85) and both species in September (4.94 and 4.71, respectively), the warmest month in both air (AT=24.7±1.4°C) and seawater temperatures (SST=22.0±1.9°C). In 2018, warmer AT and SST were recorded between August and October, being reflected in relatively high GIs (range: 4.35–5.00) from July to October in P. lineatus and from June to December in P. sauciatus (Fig. 8).

Fig. 8.  – Monthly variation in the mean gonadal index (GI) of Phorcus lineatus and P. sauciatus and its relationship with diverse atmospheric and oceanographic parameters, namely air temperature (AT), surface seawater temperature (SST), daylight duration (DD), wind speed (WS) and significant wave height (WH): A, P. lineatus GI vs AT; B, P. sauciatus GI vs AT; C, P. lineatus GI vs SST; D, P. sauciatus GI vs SST; E, P. lineatus GI vs DD; F, P. sauciatus GI vs WS; G, P. lineatus GI vs WH.

Discussion

Like other topshell species, P. lineatus and P. sauciatus do not exhibit external sexual dimorphism (Desai 1966Desai B.N. 1966. The biology of Monodonta lineata (Da Costa). Proc. Malacol. Soc. Lond. 37: 1-17.
, Fretter and Graham 1977Fretter V., Graham A. 1977. The Prosobranch Molluscs of Britain and Ireland Part 2 - Trochacea. J. Mollus. Stud. 3: 1-64.
, Crothers 2001Crothers J.H. 2001. Common topshells: an introduction to the biology of Osilinus lineatus with notes on other species in the genus. Field Stud. 10: 115-160.
), so their sex is only distinguishable through gonadal examination (Sousa et al. 2018Sousa R., Delgado J., González J.A., et al. 2018. Marine snails of the genus Phorcus: Biology and ecology of sentinel species for human impacts on the rocky shores. In: Ray, S. (ed), Biological resources of water. IntechOpen, Rijeka. pp. 141-167. https://doi.org/10.5772/intechopen.71614
, 2020Sousa R., Vasconcelos J., Riera R. 2020. Unravelling the effects of exploitation on the size-structure of the intertidal topshell Phorcus sauciatus in harvested and non-harvested Atlantic regions. Reg. Stud. Mar. Sci. 30: 104273. https://doi.org/10.1016/j.rsma.2020.101387
). 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)Bode A., Lombas I., Anadon N. 1986. Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiologia 142: 31-39. https://doi.org/10.1007/BF00026745
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)Lasiak T. 1987. The reproductive cycles of three trochid gastropods from the Transkei coast, southern Africa. J. Moll. Stud. 53: 24-32. https://doi.org/10.1093/mollus/53.1.24
in three other trochid species (Monodonta australis, Oxystele tabularis and O. antoni) in the Transkei coast (South Africa). Mora et al. (2017)Mora J.P.R., Mancera-Pineda J.E., Vargas L.A.G. 2017. Population ecology of Cittarium pica (Gastropoda: Trochidae) of San Andrés Island, International Biosphere Reserve, Seaflower. Rev. Biol. Trop. 65(4): 1496-1506. https://doi.org/10.15517/rbt.v65i4.26208
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 (Sousa2019Sousa R. 2019. Key exploited species as surrogates for coastal conservation in an oceanic archipelago: Insights from topshells and limpets from Madeira (NE Atlantic Ocean). Ph.D. thesis, Univ. Madeira, 279 pp.
).

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. 2001Counihan R.T., McNamara D.C., Souter D.C., et al. 2001. Pattern, synchrony and predictability of spawning of the tropical abalone Haliotis asinina from Heron Reef, Australia. Mar. Ecol. Prog. Ser. 213: 193-202. https://doi.org/10.3354/meps213193
), H. trunculus from Bizerte lagoon in northern Tunisia (Gharsallah et al. 2010Gharsallah I.H., Vasconcelos P., Zamouri-Langar N., et al. 2010. Reproductive cycle and biochemical composition of Hexaplex trunculus (Gastropoda: Muricidae) from Bizerte lagoon, northern Tunisia. Aquat. Biol. 10: 155-166. https://doi.org/10.3354/ab00275
) and Tegula eiseni (currently accepted as Agathistoma eiseni) from Bahía Asunción in Mexico (Vélez-Arellano et al. 2009Vélez-Arellano N., Del Próo S.G., Ordoñez E.O. 2009. Gonadal cycle of Tegula eiseni (Jordan 1936) (Mollusca: Gastropoda) in Bahia Asunción, Baja California Sur, Mexico. J. Shellfish Res. 28(3): 577-580. https://doi.org/10.2983/035.028.0321
) 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 2014Romero Bastías M.S. 2014. Spawning and larval development of Tegula euryomphala (Jones, 1844) (Trochoidea: Tegulidae) from La Herradura Bay, Chile. Invertebr. Reprod. Dev. 58(4): 278-283. https://doi.org/10.1080/07924259.2014.920423
).

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 1985Garwood P.R., Kendall M.A. 1985. The reproductive cycles of Monodonta lineata and Gibbula umbilicalis on the coast of Mid-Wales. J. Mar. Biol. Assoc. U.K. 65: 933-1008. https://doi.org/10.1017/S0025315400019470
). Moreover, in P. lineatus from Asturias, both sexes also behaved similarly during the study period (Bode et al. 1986Bode A., Lombas I., Anadon N. 1986. Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiologia 142: 31-39. https://doi.org/10.1007/BF00026745
). 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 2019Sousa R., Vasconcelos J., Delgado J., et al. 2019. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U. K. 99: 841-849. https://doi.org/10.1017/S0025315418001054
, Sousa et al. 2019Sousa R., Vasconcelos J., Delgado J., et al. 2019. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U. K. 99: 841-849. https://doi.org/10.1017/S0025315418001054
).

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. 1986Bode A., Lombas I., Anadon N. 1986. Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiologia 142: 31-39. https://doi.org/10.1007/BF00026745
). Daguzan (1991)Daguzan J. 1991. Recherches sur la croissance et l'écologie de Monodonta lineata (da Costa) Gastropoda, Prosobranchia, Trochidae) vivant sur littoral atlantique armoricain. Cah. Biol. Mar. 32: 3-22.
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 1972Underwood A.J. 1972. Observations on the reproductive cycles of Monodonta lineata, Gibbula umbilicalis and Gibbula cineraria. Mar. Biol. 17: 333-340. https://doi.org/10.1007/BF00366744
) and Craig-yr-Wylfa in North Wales (Williams 1965Williams E.E. 1965. The growth and distribution of Monodonta lineata (da Costa) on a rocky shore in Wales. Field Stud. 2: 189-198.
) displayed shorter spawning periods, between June and September and between August and October, respectively, followed by brief resting phases (Fretter and Graham 1977Fretter V., Graham A. 1977. The Prosobranch Molluscs of Britain and Ireland Part 2 - Trochacea. J. Mollus. Stud. 3: 1-64.
). 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 1985Garwood P.R., Kendall M.A. 1985. The reproductive cycles of Monodonta lineata and Gibbula umbilicalis on the coast of Mid-Wales. J. Mar. Biol. Assoc. U.K. 65: 933-1008. https://doi.org/10.1017/S0025315400019470
, Bode et al. 1986Bode A., Lombas I., Anadon N. 1986. Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiologia 142: 31-39. https://doi.org/10.1007/BF00026745
, Mieszkowska 2005Mieszkowska N. 2005. Changes in the biogeographic distribution of the trochidae gastropods Osilinus lineatus (da Costa) and Gibbula umbilicalis (da Costa) in response to global climate change: range dynamics and physiological mechanisms. PhD thesis, Univ. Plymouth, 188 pp. https://pearl.plymouth.ac.uk/bms-theses/124/
). 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)Sousa R., Vasconcelos J., Delgado J., et al. 2019. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U. K. 99: 841-849. https://doi.org/10.1017/S0025315418001054
. 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. 2020Shanks A.L., Rasmuson L.K., Valley J.R., et al. 2020. Marine heat waves, climate change, and failed spawning by coastal invertebrates. Limnol. Oceanogr. 65: 627-36. https://doi.org/10.1002/lno.11331
, Shin et al. 2020Shin S.R., Kim H.J., Lee D.H., et al. 2020. Gonadal maturation and main spawning period of Haliotis gigantea (Gastropoda: Haliotidae). Dev. Reprod. 24: 79-88. https://doi.org/10.12717/DR.2020.24.2.79
, Sukhan et al. 2021Sukhan Z.P., Cho Y., Sharker M.R., et al. 2021. Effective accumulative temperature affects gonadal maturation by controlling expression of GnRH, GnRH receptor, serotonin receptor and APGWamide gene in Pacific abalone, Haliotis discus hannai during broodstock conditioning in hatcheries. J. Therm. Biol. 100: 103037. https://doi.org/10.1016/j.jtherbio.2021.103037.
) 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 2001Crothers J.H. 2001. Common topshells: an introduction to the biology of Osilinus lineatus with notes on other species in the genus. Field Stud. 10: 115-160.
). Furthermore, several studies on the reproductive cycle of Patagonian marine gastropods, namely Buccinanops cochlidium (Averbuj et al. 2010Averbuj A., Bigatti G., Penchaszadeh P.E. 2010. Gametogenic cycle and size at first maturity of the Patagonic edible snail Buccinanops cochlidium from Argentina. Mar. Biol. 157: 2229-2240. https://doi.org/10.1007/s00227-010-1488-3
), Odontocymbiola magellanica (Bigatti et al. 2008Bigatti G., Marzinelli E.M., Penchaszadeh P.E. 2008. Seasonal reproduction and sexual maturity of Odontocymbiola magellanica (Neogastropoda: Volutidae). Invertebr. Biol. 127(3): 314-326. https://doi.org/10.1111/j.1744-7410.2008.00139.x
), Tegula patagonica (currently accepted as Agathistoma patagonicum) (Nieto-Vilela et al. 2021Nieto-Vilela R.A., Cumplido M., Zabala S., et al. 2021. Biochemical composition during the reproductive cycle of a novel gastropod resource from Atlantic Patagonia. Mar. Freshw. Res. 73(3): 388-397. https://doi.org/10.1071/MF21208
) and Trophon geversianus (Cumplido et al. 2010Cumplido M., Averbuj A., Bigatti G. 2010. Reproductive seasonality and oviposition induction in Trophon geversianus (Gastropoda: Muricidae) from Golfo Nuevo, Argentina. J. Shellfish Res. 29(2): 423-428. https://doi.org/10.2983/035.029.0219
), 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. 2018Boman E.M., de Graaf M., Nagelkerke L.A.J., et al. 2018. Variability in size at maturity and reproductive season of queen conch Lobatus gigas (Gastropoda: Strombidae) in the Wider Caribbean Region. Fish. Res. 201: 18-25. https://doi.org/10.1016/j.fishres.2017.12.016
, Melchior et al. 2023Melchior M., Clearwater S.J., Collier K.J. 2023. Reproductive phenology and the influence of temperature in two sympatric New Zealand freshwater mussel species. Mar. Freshw. Res. 74: 1478-1491. https://doi.org/10.1071/MF23072
, Seinor et al. 2023Seinor K., Purcell S.W., Malcom H., et al. 2023. Extended and spatially asynchronous reproductive periodicity in a harvested, warm-temperate rocky-reef gastropod (Turbinidae). Fish. Oceanogr. 33(1):1-12. https://doi.org/10.1111/fog.12653
). 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 2002Ward D.W., Davis A. R. 2002. Reproduction of the turban shell Turbo torquatus Gmelin 1791 (Mollusca: Gastropoda), in New South Wales, Australia. Mar. Freshw. Res. 53: 85-91. https://doi.org/10.1071/MF00066
, Freije and Al-Sayed 2009Freije A., Al-Sayed H. 2009. Lipids and glycogen utilization in the intertidal gastropod mollusc species Turbo coronatus (Gmelin 1791). Arab Gulf J. Sci. Res. 57: 204-215.
, Ramesh et al. 2010Ramesh R., Ravichandran S., Kumaravel K. 2010. Annual cycle of reproduction in Turbo brunneus, from Tuticorin South East Coast of India. World J. Fish Mar. Sci. 2: 14-20.
). 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)Collin R., Kerr K., Contolini G., et al. 2017. Reproductive cycles in tropical intertidal gastropods are timed around tidal amplitude cycles. Ecol. Evol. 7: 5977-5991. https://doi.org/10.1002/ece3.3166
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. 2003Aranda D.A., Cárdenas E.B., Morales I.M., et al. 2003. A review of the reproductive patterns of gastropod mollusks from Mexico. Bull. Mar. Sci. 73(3): 629-641.
, Di Stefano and Giménez 2022Di Stefano V.L., Giménez J. 2022. Gonadal morphology in the marine snail Tegula patagonica (Vetigastropoda: Tegulidae) from the intertidal area, in Patagonia, Argentina. Mar. Biodivers. 52: 6. https://doi.org/10.1007/s12526-021-01248-y
), while others display spawning peaks (e.g. Joll 1980Joll L.M. 1980. Reproductive biology of two species of Turbinidae (Mollusca: Gastropoda). Aust. J. Mar. Freshwater Res. 31: 319-336 https://doi.org/10.1071/MF9800319
, Joska and Branch 1993Joska M.A.P., Branch G.M. 1993. The reproductive cycle of the trochid gastropod Oxystele variegata (Anton, 1839). Veliger 26: 47-51.
). 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. 2003Aranda D.A., Cárdenas E.B., Morales I.M., et al. 2003. A review of the reproductive patterns of gastropod mollusks from Mexico. Bull. Mar. Sci. 73(3): 629-641.
, Collinet al. 2017Collin R., Kerr K., Contolini G., et al. 2017. Reproductive cycles in tropical intertidal gastropods are timed around tidal amplitude cycles. Ecol. Evol. 7: 5977-5991. https://doi.org/10.1002/ece3.3166
). Lasiak (1987)Lasiak T. 1987. The reproductive cycles of three trochid gastropods from the Transkei coast, southern Africa. J. Moll. Stud. 53: 24-32. https://doi.org/10.1093/mollus/53.1.24
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 1974bUnderwood A.J. 1974b. The reproductive cycles and geographical distribution of some common Eastern Australian prosobranchs (Mollusca: Gastropoda). Aust. J. Mar. Freshwater Res. 25: 63-88. https://doi.org/10.1071/MF9740063
), Cantharidus capillaceus (Simpson 1977Simpson R.D. 1977. The reproduction of some littoral molluscs from Macquarie Island (Sub-Antarctic). Mar. Biol. 44: 125-142. https://doi.org/10.1007/BF00386953
), Oxystele antoni and O. tabularis (Lasiak 1987Lasiak T. 1987. The reproductive cycles of three trochid gastropods from the Transkei coast, southern Africa. J. Moll. Stud. 53: 24-32. https://doi.org/10.1093/mollus/53.1.24
) and Steromphala cineraria (Underwood 1972Underwood A.J. 1972. Observations on the reproductive cycles of Monodonta lineata, Gibbula umbilicalis and Gibbula cineraria. Mar. Biol. 17: 333-340. https://doi.org/10.1007/BF00366744
) 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 1985Garwood P.R., Kendall M.A. 1985. The reproductive cycles of Monodonta lineata and Gibbula umbilicalis on the coast of Mid-Wales. J. Mar. Biol. Assoc. U.K. 65: 933-1008. https://doi.org/10.1017/S0025315400019470
). Moreover, since these topshell species are exposed to severe and instable environmental conditions (Raffaelli and Hawkins 1999Raffaelli D., Hawkins S.J. 1999. Intertidal ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, 356 pp.
, Ramírez et al. 2005Ramírez R., Tuya F., Sánchez-Jerez P., et al. 2005. Population structure and spatial distribution of the gastropod molluscs Osilinus atrata and Osilinus sauciatus in the rocky intertidal zone of the Canary Islands (Central East Atlantic). Cienc. Mar. 31(4): 697-706. https://doi.org/10.7773/cm.v31i4.35
), their reproductive cycles are expected to display some spatial and temporal fluctuations (Aranda et al. 2003Aranda D.A., Cárdenas E.B., Morales I.M., et al. 2003. A review of the reproductive patterns of gastropod mollusks from Mexico. Bull. Mar. Sci. 73(3): 629-641.
).

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. 2014Aranda D.A., Oxenford H.A., Bissada C., et al. 2014. Reproductive patterns of queen conch, Strombus gigas (Mollusca, Gastropoda), across the Wider Caribbean Region. Bull. Mar. Sci. 90: 813-831. https://doi.org/10.5343/bms.2013.1072
, Di Stefano and Giménez 2022Di Stefano V.L., Giménez J. 2022. Gonadal morphology in the marine snail Tegula patagonica (Vetigastropoda: Tegulidae) from the intertidal area, in Patagonia, Argentina. Mar. Biodivers. 52: 6. https://doi.org/10.1007/s12526-021-01248-y
). In addition, lowest winter temperatures can affect the survival of larvae and juveniles, subsequently impacting recruitment (Kendall et al. 1987Kendall M.A., Williamson P., Garwood P.R. 1987. Annual variation in recruitment and population structure of Monodonta lineata and Gibbula umbilicalis populations at Aberaeron. Mid-Wales Estuar. Coast. Shelf. Sci. 24(4): 499-511. https://doi.org/10.1016/0272-7714(87)90130-2
). In addition to temperature, the photoperiod also seems to influence gamete release and reproductive activity in marine gastropod species (Himmelman 1999Himmelman J. H. 1999. Spawning, marine invertebrates. In: Knobil E., Neill J.D. (eds), Encyclopedia of reproduction, vol. 4. New York, Academic Press, pp. 524-533.
). For instance, the reproductive cycles of various Patagonian gastropods, such as Adelomelon ancilla (Penchaszadeh et al. 2009Penchaszadeh P.E., Antelo C.S., Zabala S., et al. 2009 Reproduction and imposex in the edible snail Adelomelon ancilla from northern Patagonia, Argentina. Mar. Biol. 156: 1929-1939 https://doi.org/10.1007/s00227-009-1225-y
), B. cochlidium (Averbujet al. 2010Averbuj A., Bigatti G., Penchaszadeh P.E. 2010. Gametogenic cycle and size at first maturity of the Patagonic edible snail Buccinanops cochlidium from Argentina. Mar. Biol. 157: 2229-2240. https://doi.org/10.1007/s00227-010-1488-3
), O. magellanica (Bigatti et al. 2008Bigatti G., Marzinelli E.M., Penchaszadeh P.E. 2008. Seasonal reproduction and sexual maturity of Odontocymbiola magellanica (Neogastropoda: Volutidae). Invertebr. Biol. 127(3): 314-326. https://doi.org/10.1111/j.1744-7410.2008.00139.x
), and T. geversianus (Cumplido et al. 2010Cumplido M., Averbuj A., Bigatti G. 2010. Reproductive seasonality and oviposition induction in Trophon geversianus (Gastropoda: Muricidae) from Golfo Nuevo, Argentina. J. Shellfish Res. 29(2): 423-428. https://doi.org/10.2983/035.029.0219
), 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 1979Underwood A.J. 1979. The ecology of intertidal gastropods. Adv. Mar. Biol. 16: 111-210. https://doi.org/10.1016/S0065-2881(08)60293-X
, Freije and Al-Sayed 2009Freije A., Al-Sayed H. 2009. Lipids and glycogen utilization in the intertidal gastropod mollusc species Turbo coronatus (Gmelin 1791). Arab Gulf J. Sci. Res. 57: 204-215.
, Seinor et al. 2023Seinor K., Purcell S.W., Malcom H., et al. 2023. Extended and spatially asynchronous reproductive periodicity in a harvested, warm-temperate rocky-reef gastropod (Turbinidae). Fish. Oceanogr. 33(1):1-12. https://doi.org/10.1111/fog.12653
). In particular, trochacean gastropod spawning seems to be also stimulated by intense water movement (Grange 1976Grange K.R. 1976. Rough water as a spawning stimulus in some trochid and turbinid gastropods. N.Z.J. Mar. Freshw. Res. 10: 203-216. https://doi.org/10.1080/00288330.1976.9515607
). 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 2015Costa M.A. 2015. Distribution and shape analysis of Phorcus lineatus and Phorcus sauciatus along the Portuguese coast. MSc thesis, Univ. Lisboa, 68 pp.
). However, while calmer sea conditions might be advantageous to avoid larval dispersal after fertilization (Seinor et al. 2023Seinor K., Purcell S.W., Malcom H., et al. 2023. Extended and spatially asynchronous reproductive periodicity in a harvested, warm-temperate rocky-reef gastropod (Turbinidae). Fish. Oceanogr. 33(1):1-12. https://doi.org/10.1111/fog.12653
), rough sea conditions might improve population connectivity (Grange 1976Grange K.R. 1976. Rough water as a spawning stimulus in some trochid and turbinid gastropods. N.Z.J. Mar. Freshw. Res. 10: 203-216. https://doi.org/10.1080/00288330.1976.9515607
) and promote a quick transfer of larvae out of the surf zone, thus avoiding benthic predators (Shanks 1997Shanks A.L. 1997. Apparent oceanographic triggers to the spawning of the limpet Lottia digitalis. J. Exp. Mar. Biol. Ecol. 222: 31-42.
, Gyory and Pineda 2011Gyory J., Pineda J. 2011. High-frequency observations of early-stage larval abundance: Do storms trigger synchronous larval release in Semibalanus balanoides? Mar. Biol. 158: 1581-1589. https://doi.org/10.1007/s00227-011-1671-1
).

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 2015Costa M.A. 2015. Distribution and shape analysis of Phorcus lineatus and Phorcus sauciatus along the Portuguese coast. MSc thesis, Univ. Lisboa, 68 pp.
). Furthermore, air temperature fluctuation and desiccation are key stress factors acting on rocky shore organisms (Bertness et al. 2006Bertness M.D, Crain C.M, Silliman B.R., et al. 2006. The community structure of western Atlantic Patagonian rocky shores. Ecol. Monogr. 76: 439-60. https://doi.org/10.1890/0012-9615(2006)076[0439:TCSOWA]2.0.CO;2
, Noke 2016Noke R. 2016. What is driving the range extension of Gibbula umbilicalis (Gastropoda, Trochidae) in the eastern English Channel? MSc thesis, Bournemouth Univ., UK, 84 pp.
). In particular, P. sauciatus is highly vulnerable to desiccation due to its large area of contact with the air (Costa 2015Costa M.A. 2015. Distribution and shape analysis of Phorcus lineatus and Phorcus sauciatus along the Portuguese coast. MSc thesis, Univ. Lisboa, 68 pp.
, Sousa 2019Sousa R., Vasconcelos J., Delgado J., et al. 2019. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U. K. 99: 841-849. https://doi.org/10.1017/S0025315418001054
), 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 2014DOCAPESCA 2014. Dados relativos às vendas declaradas de caramujos nep em lota em Portugal, Docapesca, Portos e Lotas, SA, Lisboa.
), 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 2019Sousa R., Vasconcelos J., Delgado J., et al. 2019. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U. K. 99: 841-849. https://doi.org/10.1017/S0025315418001054
), 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. 2023D.O.G. 2023. Orden de 21 de diciembre de 2023. Consellería del Mar aprueba el plan general de explotación marisquera para el trienio 2024-2026. Diario Oficial de Galícia Núm. 246, Viernes, 29 de diciembre de 2023, 71786-71833 pp.
). 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. 2011D.R. 2011. Portaria Nº 82/2011 de 22 de fevereiro que estabelece tamanhos mínimos para algumas espécies de invertebrados marinhos, aplicáveis em águas sob soberania e jurisdição nacional. Diário da República 1ª Série Nº 37: 886-887.
), which is less stringent than in Galicia (Spain) (MCRS=15mm, D.O.G. 2012D.O.G. 2012. Orden de 27 de julio de 2012. Consellería del Medio Rural y del Mar regulan los tamaños mínimos de diversos productos pesqueros en la Comunidad Autónoma de Galícia. Diario Oficial de Galícia Núm. 226, Martes, 27 de noviembre de 2012, 44545-44563 pp.
).

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgements

The authors are grateful to the Portuguese Hydrographic Institute (IH) for kindly providing data on SST and WH, as well as to the website Weather Underground for the freely available data on AT, DD and WS. The authors also acknowledge the useful comments and suggestions provided by the Assistant Editor (Montserrat Ramón Herrero) and two anonymous referees, which helped to improve the overall quality of the manuscript.

Declaration of competing interests

The authors declare no conflict of interests.

Funding sources

The present study was supported by the research project “Contributo para a Gestão Sustentada da Pequena Pesca e da Apanha (PESCAPANHA)” (MAR-01.03.02-FEAMP-0021) (field surveys, biological sampling and laboratory analyses), funded by the Fisheries Operational Programme (MAR 2020) and co-financed by the European Maritime and Fisheries Fund (EMFF 2014-2020), and also by the “Programa de Monitorização da Pequena Pesca e Apanha (MOPPA)” (MAR-014.7.2-FEAMPA-00005) (data treatment, statistical analyses and manuscript writing), funded by the Fisheries Operational Programme (MAR 2030) and co-financed by the European Maritime, Fisheries and Aquaculture Fund (EMFAF 2021-2027).

Authorship contribution statement

Paula Moura: Conceptualization, Formal analysis, Investigation, Methodology, Writing – original draft; Paulo Vasconcelos: Conceptualization, Investigation, Methodology, Project administration, Writing – review & editing; Fábio Pereira: Conceptualization, Formal analysis, Investigation, Methodology, Writing – review & editing; André N. Carvalho: Investigation, Methodology, Writing – review & editing; Miguel B. Gaspar: Funding acquisition, Project administration, Writing – review & editing.

References