In this review article, the authors explore a broad spectrum of subjects associated to marine snails of the genus Phorcus Risso, 1826, namely, distribution, habitat, behaviour and life history traits, and the consequences of anthropological impacts, such as fisheries, pollution, and climate changes, on these species. This work focuses on discussing the ecological importance of these sentinel species and their interactions in the rocky shores as well as the anthropogenic impacts to which they are subjected. One of the main anthropogenic stresses that affect Phorcus species is fisheries. Topshell harvesting is recognized as occurring since prehistoric times and has evolved through time from a subsistence to commercial exploitation level. However, there is a gap of information concerning these species that hinders stock assessment and management required for sustainable exploitation. Additionally, these keystone species are useful tools in assessing coastal habitat quality, due to their eco-biological features. Contamination of these species with heavy metals carries serious risk for animal and human health due to their potential of biomagnification in the food chain. Thus, the use of these species as bioindicators is warranted to the establishment of conservation measures targeting marine coastal environments. Climate change increases the level of environmental stress to which intertidal organisms are subjected to, affecting the functioning of biological systems at different levels of organization. Phorcus species have been widely used as indicators of the effect of climate change on local disturbances of intertidal ecosystems and geographic distribution shifts of these organisms. Further studies concerning biological parameters of Phorcus species and how they react to exploitation, pollution, and climate change will consolidate these species as indicators of large-scale ecological impacts of anthropogenic activities.
- life history traits
- climate change
Topshells are marine gastropods that inhabit the rocky shores. These marine snails together with limpets and winkles are the most successful algal grazers present in the intertidal of the Northeastern Atlantic and Mediterranean Sea . Topshells occupy the rocky sea shores from the supratidal to the subtidal, one of the most extreme, heterogeneous, and dynamic environments in nature that expose these organisms to different levels of thermal and hydric stresses [2, 3]. These unpredictable environmental conditions are therefore responsible for many of their peculiar morphological and biological characteristics that can be perceived as adaptations to the intertidal environment . The marine snails of the genus
The diversity and ecological importance of the genus
Intertidal invertebrates’ life history traits vary inter- and intraspecifically because of genetic differences and environmental effects. Growth, reproductive strategy, and mortality depend on a complex combination of selective forces and are fundamental to understand the distribution and abundance of these species along the intertidal [6, 7]. As such, knowledge of life history traits of
One of the main causes of disturbance in the intertidal ecosystem is the harvest of gastropods in the rocky shores, which has occurred since prehistorical times, resulting in shifts in abundance and/or size structure of these species. Another cause of disturbance is the contamination of coastal waters, by the presence of unnatural chemicals, as a result of industrial spillage and sewage discharges among others. Gastropod molluscs are frequently used as bioindicators to assess the health status of the coast and determine the effect of marine pollution . Walsh et al.  recorded that these sentinel species have the potential to act as a useful biomonitoring system of pollutants in the marine environment. As such, they act as pollution indicators by tracing metals, providing information required for the establishment of protective measures of the ecosystem.
Global climate change also causes disturbance in the intertidal ecosystem that results in changes in the geographical distribution of marine gastropods. Intertidal invertebrates are known to respond to climate change through alterations in biogeographic distributions following a latitudinal gradient, from warmer towards cooler regions.
The aim of this work is to compile and review a wide array of subjects related to
2. Biology and ecology of topshells
Gastropods are comprised essentially of two main parts: the shell and the body. These asymmetrical molluscs have a twisted, spirally coiled shell around its body, which protects them from biotic and abiotic factors present in their environment, and a corneous or calcareous operculum, a flat plate that rests on the upper dorsal side of the foot that acts as a supporting pad for the shell. When the snail actively moves or blocks the aperture, the body withdraws, protecting the animal from predators and preventing water leakage in exposed rocky shores [12, 13].
In topshells, the shell is complete and usually pyramidal, moderately large, conical to globose in shape, with rounded to angular body whorls and often with a flattened base and an interior consisting of mother-of-pearl. This structure is formed in the embryonic stage, with the secretion of protein fibres from the outer skin of the visceral mass and from the mantle, while they are free-swimming larvae and they are followed by the secretion of calcium carbonate from the same cells. Posterior to the embryonic phase, the shell continues to grow through the addition of a protein mesh and calcium carbonate mostly on its margins but also on its interior. Shell growth is not continuous and it frequently leaves different growth lines since maturity and adverse environmental conditions may cease growth. The shell offers refuge both from predators and from desiccation being impervious to gasses and liquids and resistant to crushing [12, 13, 14]. Colour patterns of the shell are usually highly variable in topshells and are mostly related to diet rather than to genetic control (Figure 1) .
The soft body consists of two compartments connected by a waist and present a dark ash colour with a greenish tint . The lower compartment encompasses the muscular foot and the head. The foot is used for locomotion over the substrate, swimming, jumping, and returning the animal to an upright position when overturned. Also, it helps to detect food. The upper compartment is used for respiration, digestion, excretion, gamete production, and shell secretion. The body of these organisms comprises a head with a short snout, a pair of conical and papillate tentacles, cup-shaped open eyes on distinct stalks, a foot, a muscular ventral organ with a flattened base used for locomotion, and a visceral mass, which fills dorsally the spire of the shell and contains most organ systems and the mantle, a collar-like tegument, which lines and secretes the shell, and forms a mantle cavity normally provided with respiratory gills for breathing in water and a well-vascularised mantle cavity, which allows the animals to breathe in air [13, 14].
2.2. Taxonomy and geographic distribution
This genus of gastropod grazers is currently represented by nine recognized living species [5, 6] and is comprised of
There is a clear separation between the species of
In the North Atlantic Ocean,
Concerning the geographic distribution of the genus
Topshells as limpets are subject to an array of environmental stresses due to their extended vertical distribution, which ranges from the upper to the lower shore levels. Thus, these organisms can exhibit varying degrees of structural adaptations since their position relative to the shore influences their exposure to desiccation, hydrodynamic action of the waves, temperature variation, and tidal width [20, 21, 22, 23], resulting in a wide array of intraspecific phenotypic variability.
2.3. Respiratory system
Marine snails of the genus
The marine snails’ blood, the haemolymph, contains haemocyanin, a copper-containing protein that can fix and transport two to three times more oxygen, from the gills to the heart, than organisms without this protein. The heart pulsations push the oxygen-rich blood over a closed system of arteries that lead the blood to a system of open arteries, without epithelial walls, that surround the viscera and the muscles covering all organs with oxygen-rich blood. The body organs receive the oxygen from the haemolymph and release carbon dioxide into it, which then returns to the gills, via a system of veins, where it releases the carbon dioxide and again receives oxygen .
2.4. Feeding habits, behaviour, and ecological importance
Molluscan grazers are known to have an important influence on the overall structure of benthic marine communities, because of the influence and control they exert on algae [24, 25]. Removal of grazers often leads to an imbalance on the population dynamics of the species involved on the rocky shores ecosystem, due to a dramatic development of seaweed beds .
Topshells, winkles, and limpets form a guild of microphagous herbivores that feed on microbial biofilms, by grazing the rocky substrate with the radula, a specialized rasping organ unique to molluscs, on which successive rows upon rows of backwards-pointing teeth are placed. The teeth crack, break, and wear away during use, by the food or the hard substrate from which the sea snail scrapes . Marine snails can all be found together, grazing on the open shore, and it is probable that these various snail species do not feed in exactly the same place, at the same time, in the same manner, or on exactly the same food  in order to avoid interspecific competition. The feeding adaptations between these species can be behavioural through spatial differentiation or anatomical through adaptations in the radula. Among these species, radulae show different hardness and patterns, being multi–fine-toothed rhipidoglossan in topshells, less complex taenioglossan in winkles, and simple docoglossan in pattelid limpets; therefore, it is easy to conclude they feed in different ways .
In several species of sea snails, the digestive fluids contain the cellulase enzyme that breaks down cellulose. This is one of the very few cases throughout the animal kingdom of an animal producing an enzyme capable of breaking down cellulose . Feeding behaviour in topshells is assumed to occur at night or during high tide as stated by Crothers  for
Common topshells and edible winkles swing their head from side to side while crawling and may leave grazing tracks on the rock surface and visible slime trails. Usually, the more active species secrete a thicker layer on which to crawl and this may show up as a pale band over the rock surface. Trail-following, namely the crawling over existing mucus trails, will reduce the expense of producing a mucus trail. These trails might also be used to locomote back home, to find mates, and to assist in feeding, by trapping food particles from the water column . Marine snails crawl by squeezing the front end of the foot against the substrate and by means of a ripple of muscle contraction, pass that point of contact forcing the mass of the snail forwards. In topshells, the two halves of the foot work independently of each other, out of phase, producing a characteristic slime trail .
Contrary to limpets, topshells are active at low tide and respond very rapidly to changes in weather conditions, moving out into the open when the sun shines and hiding from rain or cold winds in crevices or under boulders . These species are limited in their vertical zonation by their tolerance to temperature variation; as such, they undertake vertical migrations up and down the shore over the seasons .
Wave action also acts as a limiting factor on suspension feeders and on semisessile and sessile organisms that are favoured on exposed conditions, since the water movement allows the flow of food, propagules, nutrients, and preys to these organisms. However, in these habitats, the increase of exposure to wave action involves an increase on the risk of dislodgement and physical damage, limiting the range of susceptible and physically fragile species . In order to overcome the adverse conditions of the exposed areas, intertidal gastropods inhabiting these areas have a thin and smooth shell with large aperture due to the large foot required to cope with the higher risk of wave displacement and to be able to maintain a firm hold on rocky surfaces [28, 29]. In dangerous circumstances, a snail withdraws into its shell and adheres firmly to the substrate, so as to not be detached by waves or predators . In the Northeastern Atlantic,
Growth is a key variable in determining the survivability of any given animal, and it is important to understand the factors that drive it . Biological parameters such as growth rate, asymptotic length, longevity, and age structure reflect the overall state of health of a population and are commonly used as stock assessment tools of exploited marine organisms . In gastropods, growth rates have been determined through several features such as growth lines and rings in shells [32, 33], opercula , and statoliths . Size and age of topshells are positively related, thus allowing to investigate population structure .
Size and growth rates in the species of the genus
Topshells’ reproductive system is usually strikingly simple, with a genital duct opening into the mantle cavity through the right kidney. Sea snails commonly have separate sexes but these species are not externally sexually dimorphic and sex determination is only possible through macroscopic observation of the gonads. Internally, the most reliable character for sorting them is the appearance of the urogenital aperture. In males, the lips of this organ are unpigmented and smaller, while in females, the lips are yellow and swollen. Nevertheless, in the ripe state, males have cream testis and females greyish-green ovary covering the digestive gland and viscera [43, 44], being therefore easily differentiated in the breeding state. The lobes of the gonad, whether ovary or testis, lie near the apex of the visceral hump, among the lobes of the digestive tube, and they drain into the pericardium .
Prior to the breeding season, adults migrate up shore to the high eulittoral zone. It seems that this migration brings the animals into a region of higher temperature required for spawning. An increase in temperature may stimulate spawning as suggested by Desai  who observed that adults that have migrated furthest up shore were the first to spawn.
In fact, spawning in intertidal organisms seems to be promoted by environmental triggers such as temperature, high wind speed, and wave action. Biological factors as an increase in phytoplankton concentration may also stimulate spawning as occurs in limpets [38, 45]. As such, breeding stages of a given species may differ according to their geographical position. In fact, in the northernmost range limit, breeding seasons are shorter with a single spawning period, while in southern regions, the breeding season is longer with multiple spawning events [46, 47]. For instance, in
Fertilisation is external, with both sexes releasing their gametes into the sea and the whole process occurs directly in the water. During the reproductive season, males and females approach each other and then females send out chemical signals, leading to sperm being discharged in the water by males, which in turn stimulates females to release the oocytes . According to Desai , males discharge clouds of spermatozoa that become very active 2 or 3 minutes after being released, and females liberate oocytes separately, a few at each spasm. This process of external fertilisation, regarded as a primitive trait in snails, becomes a high-risk strategy and improbable to succeed unless the species is locally common . The fertilised egg develops within approximately a day and becomes trochophore larvae, which are capable of independent locomotion. The veliger larvae enclosed in a tiny shell develop in one or two days. At metamorphosis, the veliger turns upside down with the foot becoming ventral and the shell dorsal. Posterior to the snail’s development, the back dorsal rotates in 180° anticlockwise in relation to the head and foot. Veliger larvae remain in the water column for at most 6–7 days [5, 14, 16], and at settlement, the shell measures a little over 1 mm across . According to Heller , the trochophores of the genus
The gap in size at settlement and size at first capture reported for topshells may be understood as a potential argument for the existence of nursery areas, underneath boulders or fissures, in which small juveniles are much commoner, but there appears to be no uniform pattern . For instance, in Madeira archipelago, the juveniles of
3. Anthropogenic impacts on the genus
Intertidal and shallow-water grazers are extremely vulnerable organisms because of their limited habitat and their accessibility to human activity . Hunter-gatherers have exploited intertidal grazers, since prehistoric times, and there are evidences that the densities and the maximum sizes of several species were reduced by the exploitation [51, 52]. Studies performed in Northern Spain showed that topshells and limpets were collected, at subsistence exploitation levels, from intertidal areas of exposed shores, leading to the formation of huge shell middens . In fact, intertidal resources have always been collected by humans as food supplement or used as a bargaining chip with other products worldwide [54, 55].
Several studies were carried out aiming to investigate the temporal patterns of worldwide topshell exploitation. A proven approach to study these temporal patterns of prehistoric shellfish exploitation is the analysis of the oxygen isotopic ratio (d18O) of the latest growth increment of mollusc shells [56, 57]. Variations in oxygen isotope ratios from shell carbonates are mostly dependent on sea surface temperature (SST), which enables the estimation of temperatures during periods of shell growth and helps to determine the season of the year when the mollusc died . Colonese et al.  applied this approach to the topshell
The same approach has been followed by Gutiérrez-Zugasti et al.  that confirmed the potential of oxygen isotope analysis on
Continued exploitation of these species is likely to incur in shifts on size and shape over time. Colonese et al.  observed a significant change in shell shape of
In recent times, however, the pattern of exploitation has changed both quantitatively and qualitatively, due to the expansion of human population, to the commercial value of several species and to the industrial development that facilitated shipping and flying products around the world . Limpets, abalones, chitons, winkles, and topshells are common gastropods of intertidal rocky shores; however, some species are in serious decline mainly as a consequence of overexploitation . The exploitation of these resources has plentiful direct and indirect effects on the trophic chains of marine ecosystems, with potential complex cascading effects .
The direct effects of exploitation are the decline of the exploited species´ abundance and a shift in size composition of their populations that results from the size-selective nature of harvest. Ramírez et al.  assessed the effects of human impacts over the abundance and size patterns of topshells (
Also, differences on spatial distribution of the abundance and biomass of
Even though species of the genus
Overexploitation of marine organisms prompts the implementation of management policies in order to protect the exploited populations and mitigate human impacts. Currently, protection of
3.3.1. Harvest of
Phorcus sauciatusin the Madeira archipelago: an historical perspective
Given the current scenario, it has become vital to know the biological and ecological traits of
3.2. Pollution: topshells as bioindicators of habitat health
The ecological effects of increasing levels of heavy metal concentrations in the environment are of great concern due to their high bioaccumulative nature, persistent behaviour, and high toxicity .
The increase of human population and anthropogenic activities, such as the development of industry on the coastline, are the major responsible factors for pollution hot spots that occur predominantly close to major ports, industrial areas, and cities . Maritime traffic also acts as a source of pollution due to the antifouling paints of boats . Marine and especially coastal ecosystems are increasingly endangered by the large amounts of metal pollutants, arriving to this environment mainly by superficial runoff of rain, by direct atmospheric deposition, and by discharges from sewage effluents, spillage, and industrial establishments [70, 71]. Biological and physiological alterations in benthic communities may occur due to the toxic effects of metals and due to the sedentary lifestyle of these species . Aquatic organisms can accumulate petrogenic and anthropogenic compounds such as n-alkanes, polycyclic aromatic hydrocarbons (PAHs), and polychlorinated biphenyls (PCBs) from the environment into their lipid tissues, some of which can be carcinogenic and/or highly toxic for living organisms . Most of the comparative studies between taxonomic groups indicate that bioaccumulation of pollutants in molluscs is, in general, much superior than in fish . Mollusc shell and tissues reflect the higher degree of environmental pollution by heavy metals and are the most useful bioindicator tools. The metal body burden in molluscs may reflect the concentrations and availability of heavy metals in the surrounding water and sediment and may thus be an indication of the quality of the surrounding environment . These organisms accumulate comparatively higher concentrations of metals, both from water and sediment, because of their sedentary nature .
The worldwide increase of pollution levels on coastal zones has led to the awareness of the need to perform ecotoxicological research and to define sensitive bioindicators that allow the evaluation of contamination degrees, aiming to recommend the appropriate measures to conserve the ecology of the coastal areas. The species of the genus
In fact, several environmental factors such as water current, water flow, renewal of water, pH, and salinity affect the distribution of heavy metals in molluscs as reported by Grupta and Singh . Survival is significantly affected by salt concentration and by temperature, as well as by the interaction between them, so that the toxicities of salts are generally enhanced at higher temperatures.
Other studies support the efficacy of topshells as bioindicators, such as Bordbar et al.  who investigated the impact of a ferronickel smelting plant on the coastal zone of Northern Greece through the study of metal bioconcentration in
Bioaccumulation of pollutants in molluscs is, in general, much superior than in fish due to their sedentary nature. Thus, their shell and tissues reflect the levels of environmental pollution and are the most useful bioindicators regarding the quality of the surrounding environment. As such, there is a growing interest in the use of these marine gastropods as bioindicators, due to their ecobiological features, both in a scientific and ecosystem management perspective. This approach will contribute to the establishment of conservation measures targeting marine coastal environments. Also, all species of the genus
3.3. Climate change effects on intertidal communities: impacts on topshells of the genus
The history of earth is riddled with events that have shaped different ages, each with specific conditions that characterized them. One of these characteristics is global temperature that has oscillated numerous times over the course of earths’ long history and thus shaped biodiversity throughout the ages. For instance, the change in mean temperature between the late Pleistocene (colder conditions) and the early Holocene (warmer conditions) lead to a taxa alteration between these two periods. The more abundant species adapted to cold water, such as the periwinkle
Nowadays, however, global climate change is recognized as a reality, driven mostly as a direct consequence of human activity [83, 84], namely, through the cumulative postindustrial carbon emissions to the Earth’s atmosphere . Known consequences of climatic change in the marine environment are the increasing global temperature, perturbed regional weather patterns with increasing wind velocity and storm frequency, rising sea levels, ocean acidification, changed nutrient loads, and altered ocean circulation . These and other physical consequences are affecting marine biological processes from genes to ecosystems, over scales from rock pools to ocean basins, impacting ecosystem services and threatening human food security . The rates of physical change are unprecedented in some cases and biological changes are also likely to occur at a quick rate, although the resilience of organisms and ecosystems is highly variable. Biological changes founded in physiological response manifest as species range changes, invasions and extinctions, and ecosystem regime shifts .
Coastal ecosystems are among the most vulnerable to climate change, especially the intertidal areas, which have shown faster biogeographic changes [87, 88] than those found in terrestrial environments . Long-term monitoring studies have shown that the distribution limits of the intertidal biota of hard substrates have progressed towards the poles at a rate of over 50 km per decade [88, 90, 91].
Invertebrates and seaweeds, inhabiting the intertidal, may be particularly vulnerable to fluctuating temperatures, since individuals must adapt to the extreme temperatures of both the terrestrial and marine environments . Even in small spatial scales in the intertidal zone, a broad range of thermal conditions is found that may exceed the range of large latitudinal bands. Therefore, intertidal organisms are believed to be at the limit of their physiological tolerance since these organisms are sorted by zonation in which the upper limit of one species is set by physiological stress, and species replace one another moving up the shore [88, 93]. The species most tolerant to heat and desiccation live at the top of these zones . Since these organisms are thought to live at the utmost extremes of their physiological tolerance limits, any changes in abiotic parameters such as temperature and air exposure time could lead to death or local extinction [95, 96].
On the other hand, these changes can also lead to the expansion of the range and distribution area of some species. Thus, intertidal ecosystems are thought to be among the first to show responses to increases in global temperatures [95, 97] and are potential environments to assess the effects of climate change .
Rising temperatures can result in increased thermal stress and desiccation at low tide and in latitudinal changes in species abundance and distribution. However, changes in temperature affect the rocky intertidal; for instance, rising sea levels can result in altered zonation of intertidal biota and compression on vertical engineered defences. Also, increased storm frequency can result effectively in higher levels of wave exposure, resulting in shifts in community structure, due to a replacement of grazers by filter feeders, and shifts in direction of trophic control .
Intertidal organisms are subject to other factors that can lead to significant physiological stress and mortality such as shifts in salinity, increased levels of siltation, and prolonged oxygen or nutrient deprivation [99, 100, 101, 102]. These factors play an important role in reproduction and survival of these organisms and are predicted to change in the coming decades as a result of global climate change. In fact, some of these changes are believed to have already occurred as ecological impacts on coastal ecosystems .
A species geographic limit reflects the interactions of organisms and their environment and is likely one of the first signals of the effect of climate change on the biota of the planet . Geographical range limits impose environmental stresses, such as temperature, to populations that restrict adult survival or juvenile recruitment [88, 93]. This is related to the organisms’ physiological tolerance to temperature. Exceeding these tolerance limits results in the organism’s death and can lead to the local extinction of a population if temperatures are extreme enough . Changing climatic conditions results in shifts of geographical limits in which populations can survive and reproduce thus acting as indicators of the processes of long-term climate change [88, 89, 93].
Species of the genus
The extension of northernmost geographic limits of
Another possible example of geographic range extension due to climate change could be the colonization of Santa Maria Island in the Azores archipelago by
Changes in the abundance and distribution of
These changes in oceanographic conditions could result in shifts in the distribution and abundance of
Climate change increases the level of environmental stress to which intertidal organisms are traditionally subjected to and these may severely affect the functioning of biological systems at different levels of organization. The reviewed works of several authors provide strong evidence of the suitability of
The Service Directorate of Investigation of the Regional Directorate of Fisheries of the Autonomous Region of Madeira (DSI/DRP) and UE FEDER (INTERREG V-A MAC 2014-2020) in the framework of the project MARISCOMAC under contract MAC/2.3d/097, are acknowledged for providing financial support for this work. The first author (RS) was supported by a grant from ARDITI-OOM/2016/010 (M1420-01-0145-FEDER-000001-Observatório Oceânico da Madeira-OOM). The authors are grateful to Inhaki Gaztanhaga, Gonzálo- Lorenzo, and André Pinto for the collection of specimens from Cape Verde, Canaries archipelago, and mainland Portugal. The authors are also thankful to the Instituto das Florestas e Conservação da Natureza (IFCN IP-RAM) for providing specimens from the Natural Reserve of the Selvagens Islands.