**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 [129–131]. 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, 132–134]. 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 [137–139].

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 [153–155], 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].

leading to greater production of larvae that would eventually settle outside of the protected area [88, 132–134]. 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,

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

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 [153–155], 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

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

as well as act as a conservation tool [137–139].

80 Organismal and Molecular Malacology

significantly higher in MPAs regardless of their size.

response to MPA protection [53] (P. Henriques, pers. comm.).

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 [162–164]. 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, 165–167]. 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.
