Open access peer-reviewed chapter

Patellid Limpets: An Overview of the Biology and Conservation of Keystone Species of the Rocky Shores

Written By

Paulo Henriques, João Delgado and Ricardo Sousa

Submitted: 03 November 2016 Reviewed: 14 February 2017 Published: 16 August 2017

DOI: 10.5772/67862

From the Edited Volume

Organismal and Molecular Malacology

Edited by Sajal Ray

Chapter metrics overview

2,281 Chapter Downloads

View Full Metrics

Abstract

This work reviews a broad spectrum of subjects associated to Patellid limpets’ biology such as growth, reproduction, and recruitment, also the consequences of commercial exploitation on the stocks and the effects of marine protected areas (MPAs) in the biology and populational dynamics of these intertidal grazers. Knowledge of limpets’ biological traits plays an important role in providing proper background for their effective management. This chapter focuses on determining the effect of biotic and abiotic factors that influence these biological characteristics and associated geographical patterns. Human exploitation of limpets is one of the main causes of disturbance in the intertidal ecosystem and has occurred since prehistorical times resulting in direct and indirect alterations in the abundance and size structure of the target populations. The implementation of MPAs has been shown to result in greater biomass, abundance, and size of limpets and to counter other negative anthropogenic effects. However, inefficient planning and lack of surveillance hinder the accomplishment of the conservation purpose of MPAs. Inclusive conservation approaches involving all the stakeholders could guarantee future success of conservation strategies and sustainable exploitation. This review also aims to establish how beneficial MPAs are in enhancing recruitment and yield of adjacent exploited populations.

Keywords

  • Patellidae
  • limpets
  • fisheries
  • MPAs
  • conservation

1. Introduction

The Patellidae are one of the most successful families of gastropods that inhabit the rocky shores from the supratidal to the subtidal, a marine habitat subject to some of the most variable and unpredictable environmental conditions. Therefore, many of their peculiar morphological and biological characteristics can be understood as adaptations to this environment. The biological traits of limpets vary inter- and intraspecifically as a result of genetic differences and environmental influences [1]. Parameters such as growth, reproduction, and mortality are dependent on a complex array of selective forces and are important in understanding the distribution and abundance of a species [2, 3]. Differences in limpet populations from distinct geographic areas are most probably explained by specific environmental and anthropogenic conditions, essentially oligotrophy, sea water temperature, and fishing pressure. Thus, for some of the biological traits, it is expected to find patterns, like temperature which changes somewhat consistently with latitude and has a profound effect on the growth of limpet species, with species inhabiting higher latitudes growing more slowly and achieving larger maximum sizes, therefore having a longer lifespan than limpets from lower latitudes.

Patellid limpets are also subjected to anthropogenic impacts on the coastal ecosystems such as, pollution, habitat removal, and harvest which in some cases has led to the reduction of abundance or even the disappearance of limpets from large areas. The decline of these species, which may have been further accelerated by the progressive deterioration of the coastline, continues at an alarming rate and many of their stocks are on the verge of disappearance. To avert this situation, regulators have established several measures including the implementation of closed seasons and areas where limpet harvest is interdicted, minimum size of capture, and catch limits. Limpet populations seem to respond, in general, in a positive way to these measures; however, the response is closely linked to the ability of the regulators to enforce said measures.

Another popular strategy adopted in the protection of the rocky shores and limpets is the implementation of marine protected areas (MPAs). The effectiveness of MPAs in protectingexploited populations of limpets and underlying their overall success in increasing density and abundance as well as promoting healthy size composition with impact on the reproductive output of these species is well known. Nonetheless, several limitations are recognized that can negatively affect the protective role of MPAs such as, naturally occurring variations of the species biology and ecology as well as limitations regarding the management of MPAs, for instance, the lack of surveillance and enforcement of protection regulations.

The aim of this work is to review a broad spectrum of subjects associated to Patellid limpets’ biology such as growth and reproduction, also the consequences of commercial exploitation on the stocks of these species and the effects of marine protected areas in the biology and populational dynamics of these intertidal grazers. The focus is on determining the effect of identified biotic and abiotic factors that influence these biological characteristics and geographical patterns recognized to be closely connected to growth and reproduction, such as latitude. Regarding conservation of Patellidae, the authors aim to elucidate how beneficial MPAs are in their role of protection of exploited populations and in enhancing recruitment and yield of adjacent exploited populations.

Advertisement

2. Biology and ecology of Patellid limpets

2.1. Taxonomy and distribution

Patellid limpets are marine gastropod grazers belonging to the family Patellidae Rafinesque, 1815 that comprises the genera Patella Linnaeus, 1758, Cymbula, H. Adams & A. Adams, 1854, Helcion Montfort, 1810, and Scutellastra H. Adams & A. Adams, 1854. The worldwide distribution of Patellidae species is anti-tropical with half of the known species restricted to southern Africa and the North-Eastern Atlantic where a high diversity of species is found, while relatively few species are present in the Indian and Pacific Oceans [4, 5]. The Patellidae family is currently represented by, at least, 49 recognized species [6]. The genus Patella is comprised of 14 recognized species with a geographical distribution restricted to the North-Eastern Atlantic and the Mediterranean Sea; the genus Cymbula includes 10 species found in Southern Africa, South-Eastern Atlantic, and Mediterranean; the genus Helcion is represented by four species restricted to Southern Africa, while Scutellastra encompasses 21 species with a wide distribution ranging from Southern Africa to the Indo-West and Eastern Pacific [4, 710]. Limpets are subject to an array of environmental stresses as a result of their extended vertical distribution, which ranges from the upper to the lower shore levels. Thus, limpets 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 [1114]. This impressive phenotypic plasticity allied to the relatively simple shell geometry, convergent shell shape, and sculpturing results in an unclear Patellid limpet’s taxonomy, in such a way that the initial generic names, with broad geographical range, had to be re-evaluated based on superficial similarities [15].

2.2. Feeding habits and ecological importance

Limpets are grazing herbivores that feed, by scraping the rocky substrate with the radula, on microbial biofilms which are primarily composed of cyanobacteria and microalgae, including diatoms, spores, and other propagules of macroalgae and invertebrates [16, 17]. Limpets’ feeding habits are essential in structuring intertidal communities [1619] since limpet grazing is a key process in rocky shores involved in determining macroalgal abundance and in modifying ecosystem stability, indirectly enhancing or inhibiting the establishment of other organisms [17]. The decline of population density of limpets might result in an abnormal development of algae diversity as reported by Boaventura et al. [20] or in the occupation of their ecological niche by competing organisms such as barnacles or sea urchins [2123]. However, the effect of these grazers is not limited to the removal of algae, and very often they can affect other animal species through competitive interactions [24] and by providing secondary habitats for other invertebrates that settle either on top of, or beneath, their shells [19, 25, 26]. Grazers may also affect the rate of succession [27] or cause different assemblages to develop [28]. Thus, limpets are rightfully considered to be keystone species in intertidal communities [29].

2.3. Movement and homing

Patellid limpets are considered to some extent semi-sessile organisms; nonetheless, they perform small movements in the area surrounding their usual fixation site. This behavior is designated as homing and can often be observed through the scar that remains in the rocky substrate where the limpet settles. Limpet movement patterns and homing behavior have been extensively studied for Patella vulgata Linnaeus, 1758 [30], Patella depressa Pennant, 1777 [31], Patella rustica Linnaeus, 1758 [32], Patella ferruginea Gmelin, 1791 [33], Scutellastra flexuosa (Quoy & Gaimard, 1834), and Scutellastra argenvillei (Krauss, 1848) [34]. This homing behavior has different functions in different species such as avoiding desiccation [35, 36], reducing predation and intraspecific competition [3740], responding to wave action [41, 42] and defending territory or asserting dominance [43, 44]. The mechanism that is most widely accepted as being responsible for the homing behavior reports limpets following chemical trails, laid down on the outward trip, on their way back to the fixation site [31, 45, 46].

2.4. Growth

Biological parameters such as growth rate, asymptotic length, and age structure reflect the overall state of health of a population and are commonly used as stock assessment tools of exploited marine organisms. Growth, reproductive strategy, and mortality are dependent on a complex array of selective forces [2] and are important in understanding the distribution and abundance of a species [3]. To determine these parameters, most studies usually resort to the capture-recapture method [22, 4750] or length-frequency distribution analysis [5153]. Over the past decades, intensive research has focused on the biology of limpets, due to their diversity and ecological significance; however, there remain gaps in the knowledge concerning these species’ age structure and growth patterns.

Patellid limpets, like many marine gastropods, exhibit both intra- and interspecific seasonal variation in growth rates [54]. Although some intraspecific variation may be genetically controlled [55], external factors such as changes in food availability [56, 57], wave action [5860], and vertical distribution on the shore [61] are thought to influence growth rates. Other factors such as population density, available grazing area, predation, and competition are indicated as influencing growth rates of mollusks supporting the idea that the strategy of diverting energy to reproduction and vice versa, according to the organisms’ needs, influences growth rates [24, 49, 62, 63]. It has been suggested that limpets with greater growth rates have smaller lifespan while limpets with slow growth are generally long-lived [46]. As such, rapidly growing limpets are usually associated with early maturation, high mortality, and a short lifespan [46, 64].

Clarke et al. [49] observed a latitudinal cline in annual shell growth of the polar limpet Nacella concinna (Strebel, 1908). This latitudinal pattern could nevertheless be masked by inter-annual variability. The authors suggest that the observed variation could be the result of a simultaneous change in both growth rate and the duration of the growth period. This change would result from the shorter duration of the seasonal blooming of epiphytic microalgal and microbial biomass at higher latitudes. Another factor influencing growth rates in N. concinna is seawater temperature, with warmer temperatures that last longer producing higher growth rates.

Scutellastra and Cymbula species that occur at similar latitudes present variations in terms of growth, namely in maximum size and growth rates. When compared to tropical limpets belonging to the genus Cellana H. Adams, 1869, limpets from temperate regions are generally larger, with wider lifespan and slower growth rates. Additionally, limpets inhabiting the artic regions such as N. conccina achieve larger sizes, even wider lifespans, and slower growth rates. This latitudinal pattern has been usually associated with the latitudinal variation of temperature, photoperiod, and insolation [49]. Even though it is consensual that species from lower latitudes grow more rapidly than species from higher latitudes [49, 52], it is not yet clarified whether physiological constraints, a reduced or prolonged growing season, or combination of both might be the cause of dissimilar growth rates at differing latitudes [49].

Nevertheless, due to Patellids’ anti-tropical distribution, growth patterns are difficult to observe, particularly when considering latitude. Within this family, variations in growth are mostly derived from prevalent local environmental factors. Nonetheless, when comparing to other Patellogastropoda, a latitudinal pattern becomes apparent, in which at lower latitudes limpets grow at faster rates and achieve smaller sizes, while at higher latitudes, they grow at slower rates and achieve larger sizes. For instance, for the polar limpet N. concinna reported growth rates range between 0.059 and 0.323 year−1, while the highest growth rate is exceptionally high for a limpet inhabiting the polar regions, probably due to specific characteristics of the habitat in Signy Island [49]. The overall growth rates are inferior to those reported for limpets of the genus Cellana that inhabit lower latitudes in temperate and tropical regions with growth rates ranging from 0.400 to 1.661 year−1. Patellid limpets exhibit intermediate growth rates ranging from 0.117 year−1 in Scutellastra choclear (Born, 1778) and 1.020 year−1 in Cymbula oculus (Born, 1778) reflecting their anti-tropical distribution.

However, the nonlinearity of growth of marine organisms renders the direct comparison of growth parameters impossible [65]. As such, determination and comparison of the overall growth performance of different marine species is achieved using the growth performance index (GPI) of Pauly and Munro [66], which relates the asymptotic length and growth rate [66]. Nonetheless, the growth performance index in Patellogastropod limpets exhibits the same pattern as growth rates with decreasing GPI as latitude increases and ranging from 1.942 in N. concinna to 3.653 in Cymbula granatina (Linnaeus, 1758), suggesting that growth performance of limpets varies with latitude. Within the Patellidae family the variation of GPI is reduced with values ranging from 2.42 for S. cochlear to 3.65 for C. granatina from South Africa [62], which is in agreement with Sparre et al. [67] who claim that the growth performance index remains relatively constant at similar rates between related taxa. The variability results therefore due to abiotic and biotic factors that different species are subject to, such as greater or lesser extent of hydrodynamics, desiccation, predation, competition, and temperature.

2.5. Reproduction

Patellid limpets have a simple reproductive system, consisting of a simple gonad inserted in the visceral mass and a reduced gonoduct leading to the right nephridium [68, 69]. These species are not externally sexually dimorphic, and sex determination is only possible through macroscopic observation of the gonads. Spawning results in the release of oocytes and sperm directly in the ocean where fecundation occurs. According to Orton et al. [68], spawning is stimulated by environmental triggers, such as high wind speed and wave action. An increase in phytoplankton concentration may also stimulate spawning as suggested by Underwood [24] who observed that gastropod species with planktotrophic larvae spawn when phytoplankton concentration is high.

Most limpet species have a reproductive cycle with a gonadal development stage culminating in a spawning period followed by a resting phase. The spawning period varies inter- and intraspecifically; it may also vary from year to year and is supposed to be triggered by temperature variations, increased wave action, and onshore winds [70]. In regions with higher temperatures, spawning occurs in a short period contrary to what happens in regions with colder waters, where the development of the gonads requires a longer time period [71]. P. vulgata is believed to be a winter breeder, with spawning occurring from October to March; however, in colder localities, sexual maturation occurs earlier [68]. On the other hand, in south-west England, P. depressa is considered a summer breeder [72] with spawning occurring between late July and early September and without a resting phase unlike P. vulgata. The same authors suggested that an increase in temperature associated with wave action stimulates spawning in this species. Patella ulyssiponensis Gmelin, 1791 has a spawning period that lasts from October to December, being also considered a winter breeder in south-west England [59, 68, 73]. Orton et al. [68] and Orton and Southward [72] suggested that although the development of the gonad in P. vulgata and P. depressa, respectively, is well related with temperature, the act of spawning is triggered by violent onshore storms. Thompson [59] also found P. ulyssiponensis spawning during the autumn storms. Hence, it seems likely that spawning cannot take place until a population is sufficiently mature, but after that stage is reached, the first strong windstorm will trigger spawning [59]. Another factor that potentially affects the timing of spawning in limpets is food availability; Underwood [24] reported that species with planktotrophic larval stage time spawning with periods when phytoplankton concentrations are high. One such case is that of the closely related species of P. ulyssiponensis from the Portuguese mainland and Patella aspera Röding, 1798 from Madeira Island. P. ulyssiponensis is reported to be a summer breeder while P. aspera was reported to be a winter breeder with spawning occurring when the phytoplankton concentration is higher (P. Henriques, pers. comm.). Similarly, it has been reported that in limpets with restricted geographic distribution, the reproductive cycle is influenced by geographic locality, namely in the timing of gametogenesis and spawning [6274]. For limpets with broader geographic distribution, it is possible that the reproductive cycle is adjusted to regional environmental conditions [74].

Limpets, like many sessile or sedentary marine invertebrates, have life cycles that include a prolonged pelagic larval phase that can last up to 2 weeks as reported by Hawkins et al. [75] for Patella species. Veliger larvae remain in the water column as plankton until eventually fixating in the rocky substrate on the inferior level of the coast. As the juveniles grow, they begin a slow vertical migration, colonizing different levels of the rocky shores [76], leading to variability in patterns of recruitment [77]. Moreover, larvae in the water column are subject to processes of physical transport that can disperse them from the site of reproduction [78]. Thus, the number of recruits on a specific location may be independent of the local larvae production [16, 79] and influenced by current regimes. Nonetheless, limpet populations cannot be considered fully open or fully closed, since some local larval retention is likely to occur despite larval dispersal [80, 81].

Orton [82] suggested the existence of the phenomenon of protandrous hermaphroditism in limpets of the genus Patella based on sexual dimorphism in size-frequency of P. vulgata; subsequently Thompson [59], Branch [46], and Le Quesne [83] observed that some individuals reach maturity as males and become females in the more advanced stages of their life cycle. This phenomenon of sequential hermaphroditism is also suggested to occur in species of the genera Cymbula [46], Helcion [74], and Scutellastra [62, 84, 85]. Not all male limpets change sex, since a considerable proportion of males can be found in the larger size-groups, these individuals might eventually change sex or remain as males if the signals that lead to sex change are not present [86]. Also, some limpet species are sequential hermaphrodites in which the sex change can be reverted as reported for P. ferruginea by Guallart et al. [87].

Sex change in limpet species is thought to be genetically controlled. However, high variability in the timing or on the limpet size at which the change occurs suggests that environmental factors may influence the process. Species such as C. oculus have a relatively fixed timing of sex change [88], while in other species, the sex change occurs at sizes that are highly variable. These differences in size and age at which the sex change occurs are often mediated by environmental factors [46, 8992]. For instance, sex change in mollusks can be delayed in populations where large females are present [89, 90]. Additionally, in populations subjected to higher mortality rates or slower growth rates, sex change seems to occur earlier [93]. Also, it has been reported that social control of sex change occurs in Patellogastropod limpets [91, 92]. In this case, several possible cues for sex change have been suggested such as, contact frequency between individuals, available movement area, food availability, growth rate, pheromonal information, and communication by mucus traces left by individuals during foraging excursions [91].

Hermaphroditism is an evolutionarily advantageous strategy for species with low population densities or low motility such as limpets, since under such conditions, hermaphroditism is supposed to increase the likelihood of successful fertilization [87]. Reproductive success in broadcast spawners, such as limpets, is correlated to the quantity of gametes released into the water column. It is believed that larger limpets produce more gametes than smaller individuals. Additionally, sex change in protandrous hermaphrodite species results in an increase of female individuals in the larger size classes. Thus, the sex distribution through sizes in protandrous hermaphrodite limpets makes these species extremely vulnerable to harvest [33], since the depletion of larger and more fecund individuals and females in a higher percentage may potentially alter the sex ratio and reduce the reproductive output of populations [86].

Advertisement

3. Anthropogenic impact on Patellid limpets

Patellid limpets are common gastropods of intertidal rocky shores; however, some species are in serious decline mainly as a consequence of overexploitation [94]. These intertidal and shallow-water grazers are highly vulnerable because of their restricted habitat and its accessibility to human activity [26]. Worldwide, shellfish exploitation has often been shown to lead to decreased biomass and species richness and cause shifts in community composition [9598]. These effects are driven by the increase of human population density along the coast, the replacement of subsistence by commercial exploitation, and technological advances in methods of collection, processing, storage, and transport [99, 100]. As a result, the effects of human exploitation add to those of natural processes that influence population size of exploited limpets and are a concern in conservation biology [101]. Limpets have been exploited by human populations since the Palaeolithic period [102] at a subsistence level and used as food and bait in several parts of the world, including Mexico, the United States of America [101], Hawaii [103], Australia [104], South Africa [105], Chile [106], and Macaronesia [53, 107, 108]. More recently, this subsistence activity has been replaced, in many parts of the world, by heavy and highly profitable commercial exploitation, increasing the pressure on these species’ stocks. Limpet harvest results in reductions in density and shifts toward smaller individuals and can decrease reproductive output since individual fecundity is greater in larger individuals [44, 109, 110]. Thus, harvesting has both direct and indirect effects on these species. There are also effects on the overall community composition as removal of grazing limpets facilitates the growth of algae [20, 111, 112], leading to further changes within the rocky shore communities [16, 17].

The direct effects of limpet 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 limpet harvest [100]. This is a result of larger individuals being more visible, thus more prone to be caught, and due to their greater commercial value [22, 113, 114]. The loss of older and larger individuals results in cascading effects on the biology of these species and the affected populations, including changes in life-history parameters, demographics, reproductive success, and ecological interactions [98].

For instance, the decline of larger individuals in an exploited population of limpets might lead to the complete disappearance of the population’s viable size as a consequence of a seriously diminished reproductive success, affecting different species in a differentiated manner, as observed by Martins et al. [115] in the Azores. Protandrous hermaphrodite species are particularly susceptible to changes in their population size composition that promote a decline of frequency of larger individuals, since it directly affects the sex ratio of the population resulting in a decrease in female specimens that in natural conditions occur with higher frequency in the larger size classes. Also, larger individuals represent a greater contribution to the reproductive effort in limpets [104], thus the harvest of larger individuals contributes to a decrease in the reproductive success of marine invertebrates such as reported for P. ferruginea [33] and may eventually result in the collapse of exploited populations [86, 116, 117].

Reduction of sizes and abundance of larger individuals in exploited populations of limpets have been reported for Patella candei d'Orbigny, 1840 [116] and Patella candei crenata [114] in the Canaries, P. candei e P. aspera in the Azores [115], Helcion concolor (Krauss, 1848) [44], and P. ferruginea in Algeria [118] and Spain [86], as well as for the species C. oculus in Southern Africa [88]. The overexploitation of limpets has prompted the implementation of management strategies in order to protect the exploited populations and mitigate human impacts in several parts of the world [26, 53]. The establishment of species-specific total allowable catch, minimum size of capture, closed seasons, and closed areas has been the most common measures ensued with this objective. These strategies are thought to maintain sex ratios, preserve age structure, prevent sperm limitation, enhance yield, and restrict evolutionary changes in response to fishing, such as shifts to early maturation [119122]. When considering limpets, due to the phenomenon of protandrous hermaphroditism, in addition to minimum size limits used to prevent recruitment overfishing, management policies should also consider minimum and maximum size limits [122].

For instance, in Madeira archipelago the harvest of Patella candei sensu lato and P. aspera is regulated since 2006, enforcing the maximum allowable commercial catch of 15 kg/person/day or 200 kg/boat/day and a minimum capture size of 40 mm. Additionally, the competent authorities became responsible for issuing harvest licenses, limiting the number of active fishermen involved in limpet harvest. A closed season was also implemented between November and February in order to prevent limpet harvest during the reproductive season. More recently, the closed season was modified in order to more effectively provide protection to these heavily exploited species, now lasting from December to March. In the Azores, the overexploitation of limpets resulted in a drastic decline in population density and abundance of limpet populations, and in order to prevent a complete collapse of the stocks, regulation was implemented through the establishment of limpet protected zones that comprise stretches of coast of a few kilometers where the collection of limpets is strictly prohibited throughout the year, seasonal fishing closures, and minimum legal catch sizes [123].

Martins et al. [123] studied the effect of regulation on the recovery of the exploited populations of limpets in the Azores and concluded that the legislation and current levels of enforcement were insufficient to protect the exploited populations and greater levels of enforcement, such as the establishment of physical barriers and other protective strategies should be considered to protect limpet populations. The authors further elaborate that in the absence of adequate enforcement, a complementary approach that has had positive results is co-management [124], due to increasing awareness of the need to increase ownership of conservation areas and to involve all interested parties in the development of management schemes [125, 126].

Advertisement

4. Marine protected areas and their protective role in exploited limpet populations

Marine protected areas are frequently considered as a key tool in the conservation of marine biodiversity in coastal regions [127, 128] due to its ecosystem-level approach for exploited species. Reserves are supposed to restore and protect exploited marine organisms within their boundaries and have been shown to harbor denser populations, larger individuals, and higher biomass of exploited species [129].

MPAs potentially offer a way to conserve marine biodiversity by prohibiting harvest and at the same time sustaining fisheries by re-establishing natural conditions for reproduction [129131]. Thus, protected populations would have higher densities and larger individuals leading to greater production of larvae that would eventually settle outside of the protected area [88, 132134]. However, increase in recruitment outside reserves can be difficult to verify in the field [135, 136], and there is debate about whether marine reserves can benefit fisheries, as well as act as a conservation tool [137139].

Human harvesting of limpets is usually size-selective with a strong preference for larger individuals [98] that may potentially alter the sex ratio and reduce the reproductive output of populations in successive hermaphrodite species [75, 140]. A reduction in the abundance of large limpet species, induced by high harvesting pressure, has been observed worldwide with several documented cases of drastic declines such as in the case of the endemic limpet P. candei in the Macaronesian Archipelagos [115, 141, 142], P. ferruginea considered one of the most endangered marine invertebrates on western Mediterranean rocky shores [118, 143] and C. oculus in South Africa [88]. In a more extreme case, the overexploitation as a food source and adornments [144], since pre-Columbian times [145] of Scutellastra mexicana (Broderip & G. B. Sowerby I, 1829), resulted in this species being thought extinct [146]. However, some populations of this species were reported to have survived and now the species is considered endangered [147, 148].

MPAs are zones where the harvest of marine organisms is interdicted and are considered a popular alternative to traditional marine resource management measures [149]. Exploited marine organisms in general achieve higher abundance, biomass, and size in MPAs [104, 150]. Halpern [129] reported that abundance and species diversity of marine invertebrates were significantly higher in MPAs regardless of their size.

Halpern and Warner [149] reported that establishing MPAs results in significant increases in the average level of density and biomass in a period of 3 years and that these values are persistent over time. Even though it is considerably difficult to predict the amount of time needed for a community to respond to MPA protection, evidence collected by some authors suggests that the response occurs within 2 years [151, 152]. The speed of response to MPA protection depends on the degree of exploitation to which the species is subjected. If exploitation levels are high, the species are more probable to respond rapidly to the MPA protection, when recruitment occurs at the required levels, as a consequence of the removal of the fishing activity that limits population size, demographics of the species [153155], and the trophic level occupied by the species, since recruitment is associated to the species’ life-history parameters.

In general, for marine invertebrates with a long lifespan and slow growth, it is assumed that the response to protection from MPAs occurs at a slower rate [149]. Some limpet species such as P. candei sensu lato and P. aspera are considered to have slow growth and relatively long lifespan, thus they are extremely vulnerable to size-selective harvest and would have a slower response to MPA protection [53] (P. Henriques, pers. comm.).

Another possible effect of MPAs is the enhancement of recruitment on adjacent exploited populations, since the higher densities and larger individuals in reserves are expected to lead to greater production of larvae than in nearby exploited areas [88]. Therefore, MPAs are expected to enhance adjacent fisheries through the export of larvae [132, 133]. However, it is still unclear how and to what extent reserves influence exploited populations regarding the renewal of recruitment on these populations, due to the export of larvae originated in MPAs [137, 138, 156]. For instance, Hockey and Branch [157] found that limpet populations closer to protected areas benefit from an increase in juvenile individuals, suggesting a spillover of recruitment from MPAs. Nevertheless, the correlation between larvae production in MPAs and recruitment on exploited populations is difficult to predict, due to the difficulties in determining patterns of physical transport, especially at small scales [78, 79, 158].

According to Halpern [129], the average values of several biological variables are 20 to 30% higher in populations of MPAs when compared to exploited populations, independent of MPA size, indicating that small MPAs can also produce high values. Several studies have reported a pattern of better preserved populations of limpets in MPAs regarding abundance and biometric structure, for example P. candei in Fuerteventura [116], P. candei crenata, P. aspera and P. rustica in the Canaries archipelago [114], P. ferruginea in the Mediterranean [159], C. oculus in South Africa [88] as well as H. concolor, Scutellastra longicosta (Lamarck, 1819) and Scutellastra granularis (Linnaeus, 1758) in South Africa [26].

Núñez et al. [116] studied the abundance and size composition of eight populations of the heavily exploited P. candei in the island of Fuerteventura, two of which were included in two protected areas, and reported that these two populations were the best preserved in terms of abundance and size composition, while the areas closer to human settlement, thus more accessible, exhibited less abundance and smaller size individuals. Another study in the Canaries archipelago by Ramírez et al. [114] showed that the populations of limpets exposed to anthropogenic effects return lower levels of abundance and smaller size composition compared to more isolated populations; even when the populations are encompassed in an MPA, the non-enforcement of the imposed regulations and lack of surveillance may compromise their effectiveness. Coppa et al. [159] also reported that the impact of MPAs in the protection of the endangered limpet P. ferruginea in terms of population density, spatial distribution, and morphometric characteristics is inversely correlated to accessibility.

The effect of MPAs in population density, size structure, and biomass of the exploited limpet C. oculus in South Africa was assessed by Branch and Odendaal [88], resulting in important increases of the studied parameters in MPAs when compared to exploited populations. Also, survivability, sex ratio, and reproductive output were significantly higher in MPAs. Other examined parameters such as growth rate and age at maturity were apparently unaffected by the protection of MPAs. Conversely, recruitment was higher in exploited populations than in protected areas. These results clearly show the necessity for MPAs among the tools used for coastal management.

Nakin and McQuaid [26] reported the effect of MPAs in the populations of heavily exploited limpets S. longicosta and H. concolor and the less exploited S. granularis. The authors evidenced a subtle enhancement of population density and size structure, more evident in heavily exploited species. However, the effects of spatial and temporal variation allied to the existence of poaching activities appear to dilute the effect of marine reserves.

Even though these studies put in evidence the overall benefits of establishing MPAs in protecting the intertidal habitat and the species that inhabit it, they also raise important questions regarding their effectiveness. If on one side, MPAs allow exploited limpet populations to recover in regard to certain biological parameters, on the other hand their effectiveness is in some cases hindered by the lack of surveillance and poor enforcement of protection regulations. In fact, these two factors seem the most important in determining the effectiveness of MPAs. Nonetheless, the implementation of MPAs even when unable to fully stop illegal harvest of limpet species, results in direct improvements for the protected populations in terms of abundance, size structure, and population density and indirect effects regarding reproductive output of these broadcast spawners. For this reason, the implementation of MPAs has become one of the most widely advocated tools for the management and conservation of coastal marine ecosystems in the recent decades [160, 161].

Several factors affect the response of protected populations, thus comparison between different MPAs is somewhat difficult. In fact, the recovery indicators reported for protected populations may be a consequence not only of MPA protection but also of changes in environmental conditions, biological characteristics of the species and, level of exploitation to which they are subjected [162164]. The degree of exposure to wave action, as well as the vertical distribution of the species is thought to play an important role in the recovery of limpet populations; limpets more exposed to wave action as well as species exposed for longer periods to desiccation have a less pronounced response to the protection given by MPAs as shown by Branch and Odendaal [88] for C. oculus in South Africa.

Unsatisfactory results generally occur in those MPAs that are affected by inappropriate planning, ineffective surveillance, poor acceptance by local communities, and the lack of political will to reinforce the importance of environmental protection [140, 165167]. For instance, Coppa et al. [159] concluded that although the designation of MPAs as a tool to preserve the remaining populations of the heavily exploited P. ferruginea is of extreme importance, for these MPAs to fulfil their goal, additional measures must be considered. In 2015, Coppa et al. [163] suggested that without a joint effort toward the protection of intertidal habitats by enforcement bodies, regulators, researchers, and sea users, the MPAs will not be able to achieve their conservation objectives.

The effectiveness of MPAs’ conservation of limpet populations could be enhanced through the implementation of several additional measures that encompass a broader view of these exploited populations and the biological and ecological factors that influence their capacity to recover. For instance, it is necessary to determine which actions are required to ensure the reproductive success of individuals, essential to maintain the genetic biodiversity of overexploited species, particularly in species with absent gene flow between populations, since inbreeding increases the extinction probability of wild populations [168]. Also, the reintroduction or reinforcement of recruitment of depleted populations with allochthonous specimens produced by artificial fertilization procedures could be considered as a strategy to further fulfil the MPAs’ conservation objective [169].

The establishment of MPAs as a conservation tool of marine coastal habitats and species has returned valuable contributions over the years, particularly in terms of density, abundance, and size structure of exploited species. However, to overcome limitations a possible route to improve the success of conservation strategies could be the establishment of networks of MPAs based on solid scientific information that identifies the type of measures that need to be implemented. Planning should consider the number and size of MPAs, which should be large enough to ensure the recovery of protected populations but sufficiently spaced in order to allow the spillover of recruits and adults to the exploited populations. MPA planning should ultimately target the ecosystem and not a specific exploited species, since the success of a reserve depends not only on the recovery of a single species but on the recovery of the ecosystem to which the species belongs. Additionally, due to geographic specificities, the prevalent abiotic factors and how they influence the target ecosystem should be considered when planning MPAs. Also, continuous monitoring of the effects of MPAs on the exploited populations would allow for a more adequate management of MPAs, allowing for the adjustment of the protective measures as needed.

Besides adequate planning of MPAs, new conservation strategies are required to implement measures that raise public awareness and the political will of decision makers that would allow for innovative approaches involving not only decision makers but also the end users of these marine resources in the conservation effort of exploited species, particularly to avoid illegal poaching, which is one if not the greatest factors hindering MPA success.

Advertisement

Acknowledgments

ARDITI (Agência Regional para o Desenvolvimento da Investigação, Tecnologia e Inovação) is acknowledged for providing financial support for this work in the framework of the grant ARDITI-OOM/2016/010 (M1420-01-0145-FEDER-000001-Observatório Oceânico da Madeira-OOM). The third author (RS) was supported by a grant from ARDITI-OOM/2016/010 (M1420-01-0145-FEDER-000001-Observatório Oceânico da Madeira-OOM).

References

  1. 1. Bowman RS, Lewis JR. Geographical variation in the breeding cycles and recruitment of Patella spp. Hydrobiologia. 1986;142:41-56. DOI: 10.1007/BF00026746
  2. 2. Stearns SC. The evolution of life histories (1st ed.). Oxford: Oxford University Press; 1992. 249 p
  3. 3. Begon M, Harper JL, Townsend CR. Ecology: individuals, populations and communities (2nd ed.). Oxford: Blackwell Scientific Publications; 1996. 945 p
  4. 4. Ridgway SA, Reid DG, Taylor JD, Branch GM, Hodgson AN. A cladistic phylogeny of the family Patellidae (Mollusca: Gastropoda). Phil Trans R Soc B. 1998;353:1645-1671. DOI: 10.1098/rstb.1998.0316
  5. 5. Koufopanou V, Reid DG, Ridgway SA, Thomas RH. A molecular phylogeny of the Patellid limpets (Gastropoda: Patellidae) and its implications for the origins of their antitropical distribution. Mol Phylogenet Evol. 1999;11(1):138-156. DOI: 10.1006/mpev.1998.0557
  6. 6. WoRMS Editorial Board. World register of marine species [Internet]. 2017. Available from: http://www.marinespecies.org [Accessed: 24-01-2017]
  7. 7. Branch GM. The ecology of Patella Linnaeus from the Cape Peninsula, South Africa. I. Zonation, movements, and feeding. Zool Afr. 1971;6:1-38. DOI: 10.1080/00445096.1971.11447402
  8. 8. Christiaens J. Révision du genre Patella (Mollusca, Gastropoda). B Mus Natl Hist Nat. 1973;182(3):1305-1392
  9. 9. Powell AWR. The patellid limpets of the world (Patellidae) (1st ed.). Delaware: Delaware Museum of Natural History; 1973. 132 p
  10. 10. Espinosa F, Nakano T, Guerra-García JM, García-Gómez JC. Population genetic structure of the endangered limpet Cymbula nigra in a temperate Northern hemisphere region: influence of palaeoclimatic events? Mar Ecol. 2010;32:1-5. DOI: 10.1111/j.1439-0485.2010.00410.x
  11. 11. Moore HB. The relation of shell growth to environment in Patella vulgata. Proc Malacol Soc Lond. 1934;21(3):217-222
  12. 12. Davies PS. Effect of environment on metabolic activity and morphology of Mediterranean and British species of Patella. Pubbl Stn Zool. 1969;37:641-656
  13. 13. Bannister JV. Shell parameters in relation to zonation in Mediterranean limpets. Mar Biol. 1975;31:63-67. DOI: 10.1007/BF00390648
  14. 14. Boukhicha J, Kalthoum O, Hassine B, Tlig-Zouari S. Morphological evidence for adaptive diversification of sympatric Mediterranean Patella limpets. Rapp Comm Int Mer Medit. 2013;40:686
  15. 15. Scuderi D, Eernisse DJ. A new alien limpet for the Mediterranean: Lottia sp. (Patellogastropoda: Lottiidae). Biodivers J. 2016;7(2):287-293
  16. 16. Jenkins SR, Coleman RA, Burrows MT, Hartnoll RG, Hawkins SJ. Regional scale differences in determinism of limpet grazing effects. Mar Ecol Prog Ser. 2005;287:77-86. DOI: 10.3354/meps287077
  17. 17. Coleman RA, Underwood AJ, Benedetti-Cecchi L, Aberg P, Arenas F, Arrontes J, Castro J, Hartnoll RG, Jenkins SR, Paula J, Della Santina P, Hawkins SJ. A continental scale evaluation of the role of limpet grazing on rocky shores. Oecol. 2006;147(3):556-564. DOI: 10.1007/s00442-005-0296-9
  18. 18. Southward AJ. Limpet grazing and the control of vegetation on rocky shores. In: Crisp DJ, editor. Grazing in terrestrial and marine environments (1st ed.). Oxford: Blackwell Publications; 1964. pp. 265-273
  19. 19. Hawkins SJ, Hartnoll RG. Grazing of intertidal algae by marine invertebrates. Oceanogr Mar Biol Annu Rev. 1983;21:195-282
  20. 20. Boaventura D, Alexander M, Della Santina P, Smith ND, Ré P, da Fonseca LC, Hawkins SJ. The effects of grazing on the distribution and composition of low-shore algal communities on the central coast of Portugal and the southern coast of Britain. J Exp Mar Biol Ecol. 2002;267:185-206. DOI: 10.1016/S0022-0981(01)00372-0
  21. 21. Menge B. Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr. 1995;65(1):21-74. DOI: 10.2307/2937158
  22. 22. Kido JS, Murray SN. Variation in owl limpet Lottia gigantea population structures, growth rates and gonadal production on southern California rocky shores. Mar Ecol Prog Ser. 2003;257:111-124. DOI: 10.3354/meps257111
  23. 23. Arrontes J, Arenas F, Fernández C, Rico JM, Oliveros J, Martínez B, Viejo RM, Alvarez D. Effect of grazing by limpets, on mid-shore species assemblages in northern Spain. Mar Ecol Prog Ser. 2004;277:117-133. DOI: 10.3354/meps277117
  24. 24. Underwood AJ. The biology of gastropods. Adv Mar Biol. 1979;16:111-210
  25. 25. Branch GM. Limpets: their role in littoral and sublittoral community dynamics. In: Moore PG, Seed R, editors. The ecology of rocky coasts (1st ed.). London: Hodder & Stoughton; 1985. pp. 97-116
  26. 26. Nakin MDV, McQuaid CD. Marine reserve effects on population density and size structure of commonly and rarely exploited limpets in South Africa. Afr J Mar Sci. 2014;3:1-9. DOI: 10.2989/1814232X.2014.946091
  27. 27. Farrell TM. Models and mechanisms of succession: an example from a rocky intertidal community. Ecol Monogr. 1991;61:95-113. DOI: 10.2307/1943001
  28. 28. Anderson MJ, Underwood AJ. Effects of gastropod grazers on recruitment and succession of an estuarine assemblage: a multivariate and univariate approach. Oecol. 1997;109:442-453. DOI: 10.1007/s004420050104
  29. 29. Menge BA, Freidenburg TL. Keystone species. In: Levin SA, editor. Encyclopedia of biodiversity (Vol. 4). New York: Academic Press; 2001. pp. 613-631
  30. 30. Bree PJH. Homing-gedrag van Patella vulgata L. Verslagen van de gewone vergadering der Afdeeling natuurkunde K. Nederlandse Akademie van wetenschappen. 1959;68:106-108
  31. 31. Cook A, Bamford OS, Freeman JDB, Teidman DJ. A study on the homing habit of the limpet. Anim Behav. 1969;17:330-339. DOI: 10.1016/0003-3472(69)90019-0
  32. 32. Evans MR, Williams GA. Time partitioning of foraging in the limpet Patella vulgata. J Anim Ecol. 1991;60(2):563-575. DOI: 10.2307/5298
  33. 33. Espinosa F, Guerra-García JM, Fa D, García-Gómez JC. Aspects of reproduction and their implications for the conservationof the endangered limpet, Patella ferruginea. Invertebr Reprod Dev. 2006;49:85-92. DOI: 10.1080/07924259.2006.9652197
  34. 34. Sebastián CR, Steffani CN, Branch GM. Homing and movement patterns of a South African limpet Scutellastra argenvillei in an area invaded by an alien mussel Mytilus galloprovincialis. Mar Ecol Prog Ser. 2002;243:111-122. DOI: 10.3354/meps243111
  35. 35. Branch GM, Cherry MI. Activity rhythms of the pulmonated limpet Siphonaria capensis Q. and G. as an adaptation to osmotic stress, predation and wave action. J Exp Mar Biol Ecol. 1985;87:153-168
  36. 36. Iwasaki K. Intra- and interspecific variation in activity patterns of intertidal limpets. Venus Jpn J Malacol. 1994;53:85-104
  37. 37. Mackay DA, Underwood AJ. Experimental studies on homing in the intertidal patellid limpet Cellana tramoserica (Sowerby). Oecol. 1977;30:215-237
  38. 38. Branch GM. The response of South African patellid limpets to invertebrate predators. Zool Afr. 1978;13:221-232. DOI: 10.1080/00445096.1978.11447624
  39. 39. Garrity SD, Levings SC. Homing to scars as a defence against predators in the pulmonate limpet Siphonaria gigas (Gastropoda). Mar Biol. 1983;72:319-324. DOI: 10.1007/BF00396838
  40. 40. Iwasaki K. Analyses of limpet defence and predator offense in the field. Mar Biol. 1993;116:277-289. DOI: 10.1007/BF00350018
  41. 41. Branch GM. Activity rhythms in Siphonaria thersites. In: Chelazzi G, Vannini M, editors. Behavioural adaptation to intertidal life NATO ASI Series (Vol. 151. 1st ed.). New York: Plenum Press; 1988. pp. 27-44
  42. 42. Gray DR, Hodgson AN. Foraging and homing behaviour in the high-shore, crevice-dwelling limpet Helcion pectunculus (Prosobranchia: Patellidae). Mar Biol. 1998;132:283-294. DOI: 10.1007/s002270050394
  43. 43. Stimson J. Territorial behaviour of the owl limpet Lottia gigantea. Ecology. 1970;51:113-118. DOI: 10.2307/1933604
  44. 44. Branch GM. Mechanisms reducing intraspecific competition in Patella spp.: migration, differentiation and territorial behaviour. J Anim Ecol. 1975;44:575-600
  45. 45. Funke W. Heimfindevermögen und Ortstreue bei Patella L. (Gastropoda: Prosobranchia). Oecol. 1968;2:19-142. DOI: 10.1007/BF00394506
  46. 46. Branch GM. The biology of limpets: physical factors, energy flow and ecological interactions. Oceanogr Mar Biol Annu Rev. 1981;19:235-380
  47. 47. Kenny R. Growth studies of the tropical intertidal limpet Acmaea antillarum. Mar Biol. 1977;39:161-170. DOI: 10.1007/BF00387001
  48. 48. Gray DR, Hodgson AN. Growth and reproduction in the high-shore South African limpet Helcion pectunculus (Mollusca: Patellogastropoda). Afr Zool. 2003;38(2):371-386
  49. 49. Clarke A, Prothero-Thomas E, Beaumont JC, Chapman AL, Brey T. Growth in the limpet Nacella concinna from contrasting sites in Antarctica. Polar Biol. 2004;28:62-71. DOI: 10.1007/s00300-004-0647-8
  50. 50. Espinosa F, Gonzáles AR, Maestre MJ, Fa D, Guerra-García JM, García‐Gómez JC. Responses of the endangered limpet Patella ferruginea to reintroduction under different environmental conditions: survival, growth rates and life history. Ital J Zool. 2008;75:371-384. DOI: 10.1080/11250000801887740
  51. 51. Brêthes JC, Ferreyra G, de la Vega S. Distribution, growth and reproduction of the limpet Nacella (Patinigera) concinna (Strebel 1908) in relation to potential food availability, in Esperanza Bay (Antarctic Peninsula). Polar Biol. 1994;14:161-170. DOI: 10.1007/BF00240521
  52. 52. Khow AS. Growth determination of tropical limpet Cellana testudinaria (Linnaeus, 1758) living on the rocky shore of Ohoiwait, Southeast Moluccas, Indonesia. J Coastal Dev. 2007;10(2):89-103
  53. 53. Henriques P, Sousa R, Pinto AR, Delgado J, Faria G, Alves A, Khadem M. Life history traits of the exploited limpet Patella candei (Mollusca: Patellogastropoda) of the north-eastern Atlantic. J Mar Biol Assoc UK. 2012;92(1):1-9. DOI: 10.1017/S0025315411001068
  54. 54. Vermeij GJ. Gastropod shell growth rate, allometry & adult size: environmental implications. In: Rhodes DC, Lutz RA, editors. Skeletal growth of aquatic organisms (1st ed.). New York: Plenum Press; 1980. pp. 379-394
  55. 55. Janson K. Genetic and environmental effects on the growth rate of Littorina saxatilus. Mar Biol. 1982;69:73-78. DOI: 10.1007/BF00396963
  56. 56. McQuaid CD. The establishment and maintenance of vertical size gradients in populations of Littorina africana knysnaensis (Philippi) on an exposed rocky shore. J Exp Mar Biol Ecol. 1981;54:77-89. DOI: 10.1016/0022-0981(81)90104-0
  57. 57. Bosman AL, Hockey PAR. Life-history patterns of populations of the limpet Patella granularis: the dominant roles of food supply and mortality rate. Oecol. 1988;75:412-419. DOI: 10.1007/BF00376945
  58. 58. Branch GM, Marsh AC. Tenacity and shell shape of six Patella species: adaptive features. J Exp Mar Biol Ecol. 1978;87:153-168. DOI: 10.1016/0022-0981(78)90035-7
  59. 59. Thompson GB. Distribution and population dynamics of the limpet Patella aspera (Lamarck) in Bantry Bay. J Exp Mar Biol Ecol. 1979;40:115-135. DOI: 10.1016/0022-0981(79)90039-x
  60. 60. Brown KM, Quinn JF. The effect of wave action on growth in three species of intertidal gastropods. Oecol. 1988;75(3):420-425
  61. 61. Lewis JR, Bowman RS. Local habitat-induced variations in the population dynamics of Patella vulgata L. J Exp Mar Biol Ecol. 1975;17:165-203
  62. 62. Branch GM. The ecology of Patella Linnaeus from the Cape peninsula, South Africa. 3. Growth rates. Trans R Soc S Afr. 1974;41:161-193
  63. 63. Black R. Population regulation in the intertidal limpet Patelloida alticostata (Angas, 1865). Oecol. 1977;30:9-22. DOI: 10.1007/BF00344888
  64. 64. Gray DR. Studies of the biology and ecology of the high shore South African limpet, Helcion pectunculus (Mollusca: Patellogastropoda) [thesis]. South Africa: Rhodes University; 1996. 304 p
  65. 65. Etim L, Sankare Y. Growth and mortality, recruitment and yield of the fresh-water shrimp, Macrobrachium vollenhovenii, Herklots, 1851 (Crustacea, Palaemonidae) in the Fahe reservoir, Côte d'Ivoire, West Africa. Fish Res. 1988;38:211-223. DOI: 10.1016/S0165-7836(98)00161-1
  66. 66. Pauly D, Munro JL. Once more on the comparison of growth in fish and invertebrates. ICLARM Fishbyte. 1984;2:21
  67. 67. Sparre P, Ursin E, Venema SC. Introduction to tropical fish stock assessment, part 1 manual. Rome: FAO Fisheries Technical Paper; 1989. 337 p
  68. 68. Orton JH, Southward AJ, Dodd JM. Studies on the biology of limpets II. The breeding of Patella vulgata L. in Britain. J Mar Biol Assoc UK. 1956;35:149-176. DOI: 10.1017/S0025315400009036
  69. 69. Hyman LH. The invertebrates VI – mollusca I: aplacophora, polyplacophora, monoplacophora, gastropoda (1st ed.). New York: McGraw-Hill Book Company; 1967. 792 p
  70. 70. Fretter V, Graham A. The prosobranch mollucs of Britain and Denmark. I. Pleurotomariacea, Fissurellacea and Patellacea. J Molluscan Stud Supp. 1976;1:1-37
  71. 71. Orton JH. Observations on Patella vulgata. Part III. Habitat and habits. J Mar Biol Assoc UK. 1929;16:277-288. DOI: 10.1017/S0025315400029805
  72. 72. Orton JH, Southward AJ. Studies on the biology of limpets IV. The breeding of Patella depressa pennant on the north Cornish coast. J Mar Biol Assoc UK. 1961;41(3):653-662. DOI: 10.1017/S0025315400016210
  73. 73. Orton JH. Biology of Patella in Great Britain. Nature. 1946;158:173-174
  74. 74. Henninger TO, Hodgson AN. The reproductive cycle of Helcion pruinosus (Patellogastropoda) on two South African boulder shores. J Molluscan Stud. 2001;67:385-394
  75. 75. Hawkins SJ, Côrte-Real HBSM, Pannacciulli FG, Weber LC, Bishop JDD. Thoughts on the ecology and evolution of the intertidal biota of the Azores and other Atlantic Islands. Hydrobiologia. 2000;440:3-17. DOI: 10.1023/A:1004118220083
  76. 76. Boaventura D, Fonseca LC, Hawkins SJ. Size matters: competition within populations of the limpet Patella depressa. J Anim Ecol. 2003;72:435-446. DOI: 10.1046/j.1365-2656.2003.00713.x
  77. 77. Bowman RS, Lewis JR. Annual fluctuations in the recruitment of Patella vulgata L. J. Mar Biol Assoc UK. 1977;57:793-815. DOI: 10.1017/S0025315400025169
  78. 78. Cowen RK, Paris CB, Srinivasan A. Scaling of connectivity in marine populations. Science. 2006;311:522-527. DOI: 10.1126/science.1122039
  79. 79. Cowen RK, Sponaugle S. Larval dispersal and marine population connectivity. Ann Rev Mar Sci. 2009;1:443-466. DOI: 10.1146/annurev.marine.010908.163757
  80. 80. Schmitt RJ, Holbrook SJ, Osenberg CW. Quantifying the effects of multiple processes on local abundance: a cohort approach for open populations. Ecol Lett. 1999;2:294-303. DOI: 10.1046/j.1461-0248.1999.00086.x
  81. 81. Johnson MP. Is there confusion over what is meant by “open population?”. Hydrobiologia. 2005;544:333-338. DOI: 10.1007/s10750-005-1698-8
  82. 82. Orton JH. Observations on Patella vulgata. Part II. Rate of growth of shell. J Mar Biol Assoc UK. 1928;15:863-874. DOI: 10.1017/S0025315400009954
  83. 83. Le Quesne WJF. The response of a protandrous species to exploitation, and the implications for management: a case study with Patellid limpets [thesis]. United Kingdom: University of Southampton; 2005. 203 p
  84. 84. Robson G. Aspects of the biology of a new species of South African Patella. (Mollusca: Gastropoda: Patellidae) [thesis]. Pietermaritzburg: University of Natal; 1986
  85. 85. Lindberg DR. Reproduction, ecology, and evolution of the Indo-pacific limpet Scutellastra flexuosa. Bull Mar Sci. 2007;81(2):219-234
  86. 86. Espinosa F, Rivera-Ingraham G, García-Gómez JC. Gonochorism or protandrous hermaphroditism? Evidence of sex change in the endangered limpet Patella ferruginea. J Mar Biol Assoc Biodiv Rec. 2009;2:153. DOI: 10.1017/S1755267209990790
  87. 87. Guallart J, Calvo M, Acevedo I, Templado J. Two-way sex change in the endangered limpet Patella ferruginea (Mollusca, Gastropoda). Invertebr Reprod Dev. 2013;57(3):247-253. DOI: 10.1080/07924259.2012.754794
  88. 88. Branch GM, Odendaal F. The effects of marine protected areas on the population dynamics of a South African limpet, Cymbula oculus, relative to the influence of wave action. Biol Conserv. 2003;114:255-269. DOI: 10.1016/S0006-3207(03)00045-4
  89. 89. Coe WR. Conditions influencing change of sex in mollusks of the genus Crepidula. J Exp Zool. 1938;77:401-424. DOI: 10.1002/jez.1400770305
  90. 90. Hoagland KE. Protandry and the evolution of environmentally-mediated sex change: a study of the mollusca. Malacologia. 1978;17:365-391
  91. 91. Wright WG. Intraspecific density mediates sex-change in the territorial patellacean limpet Lottia gigantea. Mar Biol. 1989;100:353-364. DOI: 10.1007/BF00391151
  92. 92. Warner RR, Fitch DL, Standish JD. Social control of sex change in the shelf limpet, Crepidula norrisiarum: size-specific responses to local group composition. J Exp Mar Biol Ecol. 1996;204:155-167. DOI: 10.1016/0022-0981(96)02582-8
  93. 93. Munday PL, Buston PM, Warner RR. Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol. 2006;21:89-95. DOI: 10.1016/j.tree.2005.10.020
  94. 94. Marra S, de Lucia GA, Camedda A, Esinosa F, Coppa S. New records of the distribution and conservation status of the endangered limpet Patella ferruginea in Sardinia (Italy, W Mediterranean). Aquat Conserv Mar Freshw Ecosys. 2015;26(3):607-612. DOI: 10.1002/aqc.2615
  95. 95. Durán LR, Castilla JC. Variation and persistence of the middle rocky intertidal community of central Chile, with and without human harvesting. Mar Biol. 1989;103:555-562. DOI: 10.1007/BF00399588
  96. 96. Lasiak TA. Multivariate comparisons of rocky infratidal macrofaunal assemblages from replicate exploited and non-exploited localities on the Transkei coast of South Africa. Mar Ecol Prog Ser. 1998;167:15-23. DOI: 10.3354/meps167015
  97. 97. Sagarin RD, Ambrose RF, Becker BJ, Engle JM, Kido J, Lee SF, Miner CM, Murray SN, Raimondi PT, Richards DV, Roe C. Ecological impacts on the limpet Lottia gigantea populations: human pressure over a broad scale on islands and mainland intertidal zones. Mar Biol. 2007;150:399-413. DOI: 10.1007/s00227-006-0341-1
  98. 98. Fenberg PB, Roy K. Ecological and evolutionary consequences of size-selective harvesting: how much do we know? Mol Ecol. 2008;17:209-220. DOI: 10.1111/j.1365-294X.2007.03522.x
  99. 99. Eekhout S, Raubenheimer CM, Branch GM, Bosman AL, Bergh MO. A holistic approach to the exploitation of intertidal stocks: limpets as a case study. Afr J Mar Sci. 1992;12:1017-1029
  100. 100. Griffiths CL, Branch GM. The exploitation of coastal invertebrates and seaweeds in South Africa: historical trends, ecological impacts and implications for management. Trans R Soc S Afr. 1997;52:121-148. DOI: 10.1080/00359199709520619
  101. 101. Pombo OA, Escofet A. Effect of exploitation on the limpet Lottia gigantea: a field study in Baja California (Mexico) and California (U.S.A.). Pac Sci. 1996;50:393-403. DOI: 10125/2914
  102. 102. Turrero P, Munoz Colmenero AM, Prado A, García-Vázquez E. Long-term impacts of human harvesting on shellfish: North Iberian top shells and limpets from the upper palaeolithic to the present. J Mar Syst. 2014;139:51-57. DOI: 10.1016/j.jmarsys.2014.05.011
  103. 103. McCoy M. Hawaiian limpet harvesting in historical perspective: a review of modern and archaeological data on Cellana spp. From the Kalaupapa Peninsula, Moloka‘i Island. Pac Sci. 2008;62(1):28-38. DOI: 10.2984/1534-6188(2008)62[21:HLHIHP]2.0.CO;2
  104. 104. Keough MJ, Quinn GP, King A. Correlations between human collecting and intertidal mollusc populations on rocky shores. Conserv Biol. 1993;7:378-390
  105. 105. Lasiak TA. The susceptibility and/or resilience of rocky littoral molluscs to stock depletion by the indigenous coastal people of Transkei, southern Africa. Biol Cons. 1991;56:245-264. DOI: 10.1016/0006-3207(91)90060-M
  106. 106. Moreno CA, Sutherland JP, Jara HF. Man as a predator in the intertidal zone of southern Chile. Oikos. 1984;42:155-160. DOI: 10.2307/3544787
  107. 107. Santos SR, Hawkins SJ, Monteiro LR, Alves M, Isidro EJ. Marine research, resources and conservation in the Azores. Aquat Conservat Mar Freshwat Ecosyst. 1995;5:311-354. DOI: 10.1002/aqc.3270050406
  108. 108. Moro L, Herrera R. Las lapas, un recurso en extincíon. Medio Ambiente Canarias. 2000;16:3
  109. 109. Levitan DR. Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol Bull. 1991;181:261-268. DOI: 10.2307/1542097
  110. 110. Tegner MJ, Basch LV, Dayton PK. Near extinction of an exploited marine invertebrate. Trends Ecol Evol. 1996;11:278-280. DOI: 10.1016/0169-5347(96)30029-3
  111. 111. Dye AH. The effects of excluding limpets from the lower balanoid zone of rocky shores in Transkei, South Africa. S Afr J Mar Sci. 1995;15:9-15. DOI: 10.2989/025776195784156313
  112. 112. Davies AJ, Johnson MP, Maggs CA. Limpet grazing and loss of Ascophyllum nodosum canopies on decadal time scales. Mar Ecol Prog Ser. 2007;339:131-141. DOI: 10.3354/meps339131
  113. 113. Lindberg K, Estes JA, Warheit KI. Human influences on trophic cascades along rocky shores. Ecol Appl. 1998;8:880-890. DOI: 10.2307/2641274
  114. 114. Ramírez R, Tuya F, Haroun R. Efectos potenciales del marisqueo sobre moluscos gasterópodos de interés comercial (Osilinus spp. y Patella spp.) en el Archipiélago Canario. Rev Biol Mar Oceanogr. 2009;44(3):703-714
  115. 115. Martins GM, Thompson RC, Hawkins SJ, Neto AI, Jenkins SR. Rocky intertidal community structure in oceanic islands: scales of spatial variability. Mar Ecol Prog Ser. 2008;356:15-24. DOI: 10.3354/meps07247
  116. 116. Núñez J, Brito MC, Riera R, Docoito JR, Monterroso Ó. Distribución actual de las poblaciones de Patella candei D’Orbigny, 1840 (Mollusca, Gastropoda) en las islas Canarias. Una especie en peligro de extinción. Bol Inst Esp Oceanog. 2003;19(1-4):371-377
  117. 117. Guerra-García JM, Corzo J, Espinosa F, García-Gómez JC. Assessing habitat use of the endangered marine mollusk Patella ferruginea (Gastropoda, Patellidae) in the northern Africa: preliminary results and implications for conservation. Biol Cons. 2004;16:319-326. DOI: 10.1016/S0006-3207(03)00201-5
  118. 118. Espinosa F. Population status of the endangered mollusc Patella ferruginea Gmelin, 1791 (Gastropoda, Patellidae) on Algerian islands (SW Mediterranean). Anim Biodivers Conserv. 2009;32(1):19-28
  119. 119. Alonzo SH, Mangel M. The effects of size selective fisheries on the stock dynamics of and sperm limitation in sex-changing fish. Fish Bull. 2004;102:1-13
  120. 120. Baskett ML, Levin SA, Gaines SD, Dushoff J. Marine reserve design and the evolution of size at maturation in harvested fish. Ecol Appl. 2005;15:882-901. DOI: 10.1890/04-0723
  121. 121. Heppell SS, Heppell SA, Coleman FC, Koenig CC. Models to compare management options for a protogynous fish. Ecol Appl. 2006;16:238-249. DOI: 10.1890/04-1113
  122. 122. Hamilton SL, Caselle JE, Standish JD, Schroeder DM, Love MS, Rosales-Casian JA, Sosa-Nishizaki O. Size-selective harvesting alters life histories of a sex-changing fish. Ecol Appl. 2007;17:2268-2280. DOI: 10.1890/06-1930.1
  123. 123. Martins GM, Jenkins SR, Hawkins SJ, Neto AI, Medeiros AR, Thompson RC. Illegal harvesting affects the success of fishing closure areas. J Mar Biol Assoc UK. 2011;91:929-937. DOI: 10.1017/S0025315410001189
  124. 124. Costello C, Gaines SD, Lynham J. Can catch shares prevent fisheries collapse? Science. 2008;321:1678-1681. DOI: 10.1126/science.1159478
  125. 125. Baxter JM. Establishing management schemes on marine special areas of conservation in Scotland. Aquat Conserv Mar Freshw Ecosys. 2001;11:261-265. DOI: 10.1002/aqc.465
  126. 126. Thompson RC, Crowe TP, Hawkins SJ. Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environ Conserv. 2002;29:168-191. DOI: 10.1017/S0376892902000115
  127. 127. Ballantine B. Marine reserves for New Zealand. Leigh Laboratory bulletin (Vol. 25). Auckland: University of Auckland; 1991. pp. 1-196
  128. 128. Zann LP. Our sea, our future. Major findings of the state of the marine environment report for Australia (1st ed.). QLD: Great Barrier Reef Marine Park Authority; 1995
  129. 129. Halpern BS. The impact of marine reserves: do reserves work and does reserve size matter? Ecol Appl. 2003;13:117-137. DOI: 10.1890/1051-0761(2003)013[0117:TIOMRD]2.0.CO;2
  130. 130. Roberts CM, Hawkins JP. Extinction risk in the sea. Trends Ecol Evol. 1999;14:241-246
  131. 131. Lubchenco J, Palumbi SR, Gaines SD, Andelman S. Plugging a hole in the ocean: the energy science of marine reserves. Ecol Appl. 2003;13:S3–S7. DOI: 10.1890/1051-0761(2003)013[0003:PAHITO]2.0.CO;2
  132. 132. Gell FR, Roberts CM. Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol Evol. 2003;18:448-455. DOI: 10.1016/S0169-5347(03)00189-7
  133. 133. Halpern BS, Warner RR. Matching marine reserve design to reserve objectives. Proc R Soc Lond Ser B Biol Sci. 2003;270:1871-1878. DOI: 10.1098/rspb.2003.2405
  134. 134. Pelc RA, Baskett ML, Tanci T, Gaines SD, Warner RR. Quantifying larval export from South African marine reserves. Mar Ecol Prog Ser. 2009;394:65-78. DOI: 10.3354/meps08326
  135. 135. Pelc RA, Warmer RR, Gaines SD, Paris CB. Detecting larval export from marine reserves. Proc Natl Acad Sci USA. 2010;107:18266-18271. DOI: 10.1073/pnas.0907368107
  136. 136. Cole VJ, McQuaid CD, Nakin MDV. Marine protected areas export larvae of infauna, but not of bioengineering mussels to adjacent areas. Biol Conserv. 2011;144:2088-2096. DOI: 10.1016/j.biocon.2011.04.030
  137. 137. Stobutzki IC. Marine reserves and the complexity of larval dispersal. Rev Fish Biol Fish. 2001;10:515-518
  138. 138. Gaylord B, Gaines SD, Siegel DA, Carr MH. Marine reserves exploit population structure and life history in potentially improving fisheries yields. Ecol Appl. 2005;15:2180-2191. DOI: 10.1890/04-1810
  139. 139. Sale PF, Cowen RK, Danilowicz BS, Jones GP, Kritzer JP, Lindeman KC, Planes S, Polunin NV, Russ GR, Sadovy YJ, Steneck RS. Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol. 2005;20:74-80. DOI: 10.3410/f.1024416.288798
  140. 140. Fenberg PB, Caselle JE, Claudet J, Clemence M, Gaines SD, García-Charton JA, Gonçalves EJ, Grorud-Colvert K, Guidetti P, Jenkins SR, Jones PJS, Lester SE, McAllen R, Moland E, Planes S, Sørensen TK. The science of European marine reserves: status, efficacy, and future needs. Mar Policy. 2012;36:1012-1021. DOI: 10.1016/j.marpol.2012.02.021
  141. 141. Weber LI, Hawkins SJ. Evolution of the limpet Patella candei d’Orbigny (Mollusca: Patellidae) in the Atlantic archipelagos: human intervention and natural processes. Biol J Linn Soc. 2002;77:341-353. DOI: 10.1046/j.1095-8312.2002.00102.x
  142. 142. Navarro PG, Ramírez R, Tuya F, Fernández-Gil C, Sánchez-Jerez P, Haroun RJ. Hierarchical analysis of spatial distribution patterns of patellid limpets in the Canary Islands. J Molluscan Stud. 2005;71:67-73. DOI: 10.1093/mollus/eyi009
  143. 143. Ramos MA. Implementing the habitats directive for mollusc species in Spain. J Conchol Spec Publ. 1998;2:125-132
  144. 144. Feinman GM, Nicholas LM. High-intensity household-scale production in ancient Mesoamerica – a perspective from Ejutla, Oaxaca. In: Feinman GM, Mazilla L, editors. Cultural evolution: contemporary viewpoints (1st ed.). New York: Kluwer Academic/Plenum Publisher; 2000. pp. 119-142
  145. 145. Melgar-Tísoc E. Las ofrendas de concha de moluscos de la Pirámide de las Serpientes Emplumadas, Xochicalco, Morelos. Rev Mex Biodivers. 2007;78:83-92
  146. 146. Simison WB. Evolution and phylogeography of new world gastropod faunas [thesis]. Berkeley: University of California; 1985. 214 p
  147. 147. Ríos-Jara E, Pérez-Peña M, López-Uriarte E, Enciso-Padilla I, Juárez-Carillo E. Biodiversidad de moluscos marinos de la costa de Jalisco y Colima, con anotaciones sobre su aprovechamiento en la región. In: Jiménez-Quiroz MC, Espino-Barr E, editors. Los Recursos Pesqueros y Acuícolas de Jalisco, Colima y Michoacán. Sagarpa, México: Instituto Nacional de la Pesca, CRIP-Manzanillo; 2006. pp. 103-120
  148. 148. Bastida-Zavala JR, García-Madrigal MS, Rosas-Alquicira EF, López-Pérez RA, Benítez-Villalobos F, Meraz-Hernando JF, Torres-Huerta M, Montoya-Márquez A, Barrientos-Luján NA. Marine and coastal biodiversity of Oaxaca. Mexico Check List. 2013;9:329-390. DOI: 10.15560/9.2.329
  149. 149. Halpern BS, Warner RR. Marine reserves have rapid and lasting effects. Ecol Lett. 2002;5:361-366. DOI: 10.1046/j.1461-0248.2002.00326.x
  150. 150. Hockey PAR, Bosman AL. Man as an intertidal predator in Transkei: disturbance, community convergence and management of a natural food resource. Oikos. 1986;46:3-14. DOI: 10.2307/3565373
  151. 151. Roberts C. Marine fishery reserves for the Caribbean. Caribbean Parks Protect Area Bull. 1995;5(2):8-11
  152. 152. Russ G, Alcala A. Natural fishing experiments in marine reserves 1983-1993: community and trophic responses. Coral Reefs. 1998;17:383-397. DOI: 10.1007/s003380050144
  153. 153. Polacheck T. Year around closed areas as a management tool. Nat Resour Model. 1990;4:327-353
  154. 154. Carr MH, Reed DC. Conceptual issues relevant to marine harvest refuges: examples from temperature reef fishes. Can J Fish Aquat Sci. 1993;50:2019-2028. DOI: 10.1139/f93-226
  155. 155. Rowley RJ. Marine reserves in fisheries management. Aquat Conserv Mar Freshw Ecosys. 1994;4:233-254. DOI: 10.1002/aqc.3270040305
  156. 156. Palumbi SR. Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour. 2004;29:31-68. DOI: 10.1146/annurev.energy.29.062403.102254
  157. 157. Hockey PAR, Branch GM. Conserving marine biodiversity on the African coast: implications of a terrestrial perspective. Aquat Conserv Mar Freshw Ecosys. 1994;4:345-362. DOI: 10.1002/aqc.3270040406
  158. 158. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA. Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst. 1996;27:477-500. DOI: 10.1146/annurev.ecolsys.27.1.477
  159. 159. Coppa S, Lucia GA, Massaro G, Magni P. Density and distribution of Patella ferruginea in a marine protected area (western Sardinia, Italy): constraint analysis for population conservation. Mediterr Mar Sci. 2012;13(1):108-117. DOI: 10.12681/mms.27
  160. 160. Carr MH. Marine protected areas: challenges and opportunities for understanding and conserving coastal marine ecosystems. Environ Conserv. 2000;27:106-109
  161. 161. Claudet J, Guidetti P, Mouillot D, Shears NT, Micheli F. Ecological effects of marine protected areas: conservation, restoration and functioning. In: Claudel J, editor. Marine protected areas: a multidisciplinary approach (1st ed.). Cambridge, UK: Cambridge University Press; 2011. DOI: 10.1017/CBO9781139049382.005
  162. 162. Boersma DP, Parrish JK. Limiting abuse: marine protected areas, a limiting solution. Ecol Econ. 1999;31:287-304. DOI: 10.1016/S0921-8009(99)00085-3
  163. 163. Coppa S, de Lucia GA, Massaro G, Camedda A, Marra S, Magni P, Perilli A, Di Bitetto M, García-Gómez JC, Espinosa F. Is the establishment of MPAs enough to preserve endangered intertidal species? The case of Patella ferruginea in the Mal di Ventre Island (W Sardinia, Italy). Aquat Conserv Mar Freshw Ecosys. 2015. DOI: 10.1002/aqc.2579
  164. 164. Sciberras M, Jenkins SR, Mant R, KaiserMJ, Hawkins SJ, Pullin AS. Evaluating the relative conservation value of fully and partially protected marine areas. Fish Fish. 2015;16:28-77. DOI: 10.1111/faf.12044
  165. 165. Jameson SC, Tupper MH, Ridley JM. The three screen doors: can marine ‘protected’ areas be effective? Mar Pollut Bull. 2002;44:1177-1183. DOI: 10.1016/S0025-326X(02)00258-8
  166. 166. Guidetti P, Milazzo M, Bussotti S, Molinari A, Murenu M, Pais A, Spanò N, Balzano R, Agardy T, Boero F, Carrada G, Cattaneo-Vietti R, Cau A, Chemello R, Greco S, Manganaro A, di Sciara GN, Russo GF, Tunesi L. Italian marine reserve effectiveness: does enforcement matter? Biol Conser. 2008;141:699-709. DOI: 10.1016/j.biocon.2007.12.013
  167. 167. Camargo C, Maldonado JH, Alvarado E, Moreno-Sanchez R, Mendosa S, Manrique N, Mogollon A, Osorio JD, Grajales A, Sanchez JA. Community involvement in management for maintaining coral reef resilience and biodiversity in southern Caribbean marine protected areas. Biodivers Conserv. 2009;18:935-356. DOI: 10.1007/s10531-008-9555-5
  168. 168. Clark SA, Richardson BJ. Spatial analysis of genetic variation as a rapid assessment tool in the conservation management of narrow-range endemics. Invertebr Syst. 2002;16:583-587. DOI: 10.1071/IT01041
  169. 169. Guallart J, Peña JB, Pérez-Larruscain J. Primeras imágenes de una forma juvenil de la lapa ferruginosa. Quercus. 2013;325:52-53

Written By

Paulo Henriques, João Delgado and Ricardo Sousa

Submitted: 03 November 2016 Reviewed: 14 February 2017 Published: 16 August 2017