Using complementary visual approaches to investigate residency, site fidelity and movement patterns of the dusky grouper (Epinephelus marginatus) in a Mediterranean marine protected area

AbstractAssessing individuals' abundance, residency (presence at a site within a certain period) and site fidelity (tendency to return to the same site in subsequent seasons or years) is crucial for evaluating and improving the effectiveness of spatial conservation/management measures regarding ecologically and socio-economically valuable species. Using underwater visual census (UVC) and photo-identification (photo-ID) techniques, we estimated the abundance, residency and site fidelity of the dusky grouper, Epinephelus marginatus, at two protected sites within the Tavolara-Punta Coda Cavallo Marine Protected Area (Sardinia, Italy) in the summers of 2017–2018. The scope and spatio-temporal resolution of the study was extended by involving volunteer recreational divers in the photo collection. Grouper mean densities varied significantly across sampling dates, with a significant variability between the 2 years and the two investigated sites. At least 94 grouper visited the study sites in the summers of 2017–2018 based on the analysis of 968 high-quality photos using a semi-automated software to photo-identify individuals. Overall, the most frequently sighted grouper was recorded on 32 different days and 21 individuals (22%) identified in 2017 were re-sighted in 2018. The participation of volunteer recreational divers helped detect the inter-site (3.5–4 km apart) movements of a female and a male, supporting previous findings regarding the occurrence of reproduction-related movements. This study provides novel insights into the residency and site-fidelity patterns of the dusky grouper, and its small-scale movements probably related to reproduction. Specifically, we provide indications that effective protection from fishing should encompass the entire area used by grouper for reproductive movements

First direct evidence of reproductive behaviour of the white grouper, Epinephelus aeneus (Geoffroy Saint-Hilaire, 1817)

This study describes the first ever reported direct observation of a pair spawning event and the reproductive liveries of the white grouper, Epinephelus aeneus. Spawning took place on a rocky bank located in the Marine Protected Area (MPA) of Tavolara-Punta Coda Cavallo (NE Sardinia, Italy), in the Western Mediterranean Sea. In the evening of August 4th, 2018, the spawning of two large-sized individuals (~90 cm total length), displaying distinct colour patterns, was observed using SCUBA diving. This direct observation is the first record of E. aeneus male reproductive livery, characterized by a darker coloration on the head, the dorsal part of the body and the caudal fin. In addition, information on the environmental conditions in which reproduction occurred was collected. At the study site, relatively high seawater temperatures were recorded at the time of the E. aeneus spawning (24 °C at 24.7 m), as well as over the 2018 summer months (July-September), even in deep waters (>35 m), compared to previous summers. The spawning event occurred in a coralligenous-dominated seascape where fishing is prohibited, while diving activities are allowed. The site hosts abundant populations of ecologically and commercially valuable fish species (e.g., groupers, sparid fishes), with significant proportions of large-sized individuals (i.e. reproducers). Further studies are needed to advance our knowledge of the white grouper, with a particular emphasis on reproduction and the importance of implementing effective protection measures. Prioritizing management actions at key reproductive sites, such as rocky banks, is essential for ensuring the protection and/or recovery of over-exploited species

Multiple indices on different habitats and descriptors provide consistent assessments of environmental quality in a marine protected area

In the last decades, climate change and human pressures have increasingly and dramatically impacted the ocean worldwide, calling for urgent actions to safeguard coastal marine ecosystems. The European Commission, in particular, has set ambitious targets for member states with two major directives, the Water Framework Directive (WFD) and the Marine Strategy Framework Directive (MSFD), both designed to protect the marine environment in EU waters. Diverse biotic indices have accordingly been developed to assess water and habitat quality. The WFD adopts four Biological Quality Elements (BQEs), whereas the MSFD recommends a set of eleven qualitative descriptors. The borderline between water quality and habitat quality is hard to trace and so far most assessments have involved the use of a few indices and were mainly related to a single BQE or qualitative descriptor. In this study, thanks to the availability of a large dataset encompassing a wide array of descriptors, we compared the performance of 11 biotic indices relative to three habitats/biotic components (reefs, seagrass, and fish) of the Marine Protected Area (MPA) of Capo Carbonara (SE Sardinia, Italy). The aim was to assess whether the indices were consistent in defining the environmental status in the MPA investigated. We used the graphical approach RESQUE (REsilience and QUality of Ecosystem), which enabled us to obtain a single and comprehensive measure of the status of the environment by integrating several metrics. This approach was applied here to different habitats for the first time. All indices were consistent with each other in confirming the good status of Capo Carbonara MPA. The use of RESQUE provided insights to interpret the differences between water quality, defined according to the WFD, and habitat quality, defined according to the MSFD. Differences between the two EU directives, in terms of either requirements or goals, have long been discussed but the present study highlights for the first time that they are congruent in their assessment of the environmental status of marine ecosystems

From sea monsters to charismatic megafauna: changes in perception and use of large marine animals

Marine megafauna has always elicited contrasting feelings. In the past, large marine animals were often depicted as fantastic mythological creatures and dangerous monsters, while also arousing human curiosity. Marine megafauna has been a valuable resource to exploit, leading to the collapse of populations and local extinctions. In addition, some species have been perceived as competitors of fishers for marine resources and were often actively culled. Since the 1970s, there has been a change in the perception and use of megafauna. The growth of marine tourism, increasingly oriented towards the observation of wildlife, has driven a shift from extractive to non-extractive use, supporting the conservation of at least some species of marine megafauna. In this paper, we review and compare the changes in the perception and use of three megafaunal groups, cetaceans, elasmobranchs and groupers, with a special focus on European cultures. We highlight the main drivers and the timing of these changes, compare different taxonomic groups and species, and highlight the implications for management and conservation. One of the main drivers of the shift in perception, shared by all the three groups of megafauna, has been a general increase in curiosity towards wildlife, stimulated inter alia by documentaries (from the early 1970s onwards), and also promoted by easy access to scuba diving. At the same time, environmental campaigns have been developed to raise public awareness regarding marine wildlife, especially cetaceans, a process greatly facilitated by the rise of Internet and the World Wide Web. Currently, all the three groups (cetaceans, elasmobranchs and groupers) may represent valuable resources for ecotourism. Strikingly, the economic value of live specimens may exceed their value for human consumption. A further change in perception involving all the three groups is related to a growing understanding and appreciation of their key ecological role. The shift from extractive to non-extractive use has the potential for promoting species conservation and local economic growth. However, the change in use may not benefit the original stakeholders (e.g. fishers or whalers) and there may therefore be a case for providing compensation for disadvantaged stakeholders. Moreover, it is increasingly clear that even non-extractive use may have a negative impact on marine megafauna, therefore regulations are needed.SFRH/BPD/102494/2014, UID/MAR/04292/2019, IS1403info:eu-repo/semantics/publishedVersio

Reproductive behaviours of groupers (Epinephelidae) in the Tavolara-Punta Coda Cavallo Marine Protected Area (NW Mediterranean Sea)

Reproductive behaviours, alongside peculiar biological traits (e.g., large size, late sexual maturity, hermaphroditism), make some species particularly susceptible to overfishing. Groupers (Epinephelidae), ecologically and economically valuable species, are among the most vulnerable of all teleost fish worldwide. Due to their life-history traits, particularly reproductive ones, and their high commercial value, many grouper populations have undergone serious declines due to overexploitation and some species are even at great risk of extinction. Effectively enforced Marine Protected Areas (MPAs) have proven crucial for reversing this trend and promoting the recovery of depleted grouper populations by prohibiting fishing activities. Groupers are regarded as flagship species since more large-sized individuals can be found within fully protected areas compared to unprotected areas. Therefore, besides being commercially important as fishing resources and ecologically relevant as high-level predators, groupers are increasingly considered as important attractions for diving ecotourism in many effective MPAs. While multiple studies have demonstrated MPAs’ effectiveness in recovering depleted fish populations, little is known about the extent to which MPAs protect the integrity of fish reproductive behaviours. In this thesis, the reproductive biology of the most iconic grouper species in the Mediterranean Sea - the dusky grouper, Epinephelus marginatus - was investigated. The goal of this project was to evaluate the effectiveness of protection measures on the reproductive behavioural traits of this species. For this research, a combination of multiple, complementary and non-invasive study approaches was employed within a North-Western Mediterranean MPA, the Tavolara-Punta Coda Cavallo MPA (TPCC MPA). More specifically, to locate potential spawning aggregation sites both inside and outside the TPCC MPA, the local ecological knowledge of spear-fishers about past and present occurrences of the dusky grouper was surveyed. Then, to assess whether the selected protected and unprotected sites could be likely to host spawning aggregations, Underwater Visual Census (UVC) surveys were conducted to collect size and abundance data of E. marginatus both inside and outside the TPCC MPA. Results indicate that very few and small-sized individuals were recorded at unprotected sites, as opposed to protected ones, making the occurrence of spawning aggregations less likely outside the TPCC MPA. Therefore, by focusing only on protected sites, data about the abundance, sex, residency patterns and inter-site movements of individuals were collected by combining UVC and photo-identification approaches. Besides having intentionally collected photos while carrying out research fieldwork, local recreational photographers-divers were engaged in a correlated citizen science initiative and significantly contributed to broaden this research both in time and space. Finally, dusky grouper reproductive behaviours were observed during in situ diver surveys and the associated sound production was recorded through passive acoustic monitoring (PAM). Audio-recordings analyses helped not only to validate the courtship calls of the dusky grouper for the first time in the wild, but also to determine the temporal patterns of its courtship activity. Altogether, these results provide further evidence that effective protection measures (fully protected areas) are crucial in ensuring the occurrence of the study species aggregation and reproduction, and, ultimately, the long-term viability of its populations. This research also provides support for using PAM as a useful tool for monitoring dusky grouper reproduction and supporting decision makers in setting effective conservation and management measures. Finally, this thesis provides new insights into the reproductive behaviours of two other grouper species that were documented at the same reproductive sites of the dusky grouper

Catch of the day: Abundance and size data of groupers (Epinephelidae) and combers (Serranidae) from Middle to Late Holocene Levantine archaeological contexts

Groupers (Epinephelidae) are ecologically, commercially, and culturally important carnivorous fishes found throughout the world’s tropical, subtropical, and temperate coastal marine waters. Due to various life history traits (e.g., late maturity, sequential hermaphroditism) and behavior (e.g., sedentary, small home ranges) groupers are susceptible to overfishing, including small-scale and recreational fishing (especially spearfishing), and their populations are declining worldwide. The eastern Mediterranean coast, home to some of the world’s longest continuously occupied urban settlements, hosts important but declining grouper populations. This paper investigates how grouper and comber (fishes in the Serranidae family with similar ecology and osteomorphology, but smaller in size) abundance and catch size changed in the eastern Mediterranean from the Middle to Late Holocene, coinciding with early coastal urbanization, by estimating their relative frequency and reconstructing their size. Size reconstructions have been done from a large sample of bones (Number of Identified Specimens = 1851) recovered from Kinet Höyük in Turkey, and Tell Fadous-Kfarabida and Tell el-Burak in Lebanon, habitation sites along the Levantine coast. Our results imply that groupers in the past reached >100 cm more often than is observed today in areas open to commercial fishing. Furthermore, the apparent lack of large groupers by the Hellenistic Period at Kinet Höyük suggests fishing efforts were intense enough to have either had an appreciable effect on the size structure of local grouper populations or brought about a behavioral change to the fishes of moving to deeper waters

Reproductive Behaviours and Potentially Associated Sounds of the Mottled Grouper <i>Mycteroperca rubra</i>: Implications for Conservation

Most grouper species worldwide are threatened by overfishing. Effective marine protected areas (MPAs) are known to enable population recovery, and consideration of vulnerable species’ reproductive behaviours is fundamental to monitoring and management plans. Many groupers produce sounds associated with reproductive behaviours. Recording these sounds helps to locate spawning sites and improve management efforts to ensure reproduction and viability. This study focuses on a poorly studied yet likely vulnerable grouper species, Mycteroperca rubra, providing novel insights into its reproductive biology by combining underwater visual census surveys, direct visual observations and passive acoustic monitoring within a Mediterranean MPA during two consecutive summers (2017 and 2018). Results indicate that M. rubra individuals were more abundant and larger at one of the protected study sites, where they also occasionally formed unusual aggregations (M. rubra spawns in the surroundings of this study site. Moreover, grouper-like unknown sounds were recorded exclusively at this site, suggesting they are associated with M. rubra courtship behaviours. Therefore, this study provides a basis for validating M. rubra sound production and supports the monitoring of its spawning sites via passive acoustics to improve MPA conservation effectiveness

Reproductive Behaviours and Potentially Associated Sounds of the Mottled Grouper Mycteroperca rubra: Implications for Conservation

Most grouper species worldwide are threatened by overfishing. Effective marine protected areas (MPAs) are known to enable population recovery, and consideration of vulnerable species&rsquo; reproductive behaviours is fundamental to monitoring and management plans. Many groupers produce sounds associated with reproductive behaviours. Recording these sounds helps to locate spawning sites and improve management efforts to ensure reproduction and viability. This study focuses on a poorly studied yet likely vulnerable grouper species, Mycteroperca rubra, providing novel insights into its reproductive biology by combining underwater visual census surveys, direct visual observations and passive acoustic monitoring within a Mediterranean MPA during two consecutive summers (2017 and 2018). Results indicate that M. rubra individuals were more abundant and larger at one of the protected study sites, where they also occasionally formed unusual aggregations (&lt;30 individuals), likely for spawning. These aggregations and the observation of courtship behaviours suggest that M. rubra spawns in the surroundings of this study site. Moreover, grouper-like unknown sounds were recorded exclusively at this site, suggesting they are associated with M. rubra courtship behaviours. Therefore, this study provides a basis for validating M. rubra sound production and supports the monitoring of its spawning sites via passive acoustics to improve MPA conservation effectiveness

Grouping groupers in the Mediterranean:Ecological baselines revealed by ancient proteins

Marine historical ecology provides a means to establish baselines to inform current fisheries management. Groupers (Epinephelidae) are key species for fisheries in the Mediterranean, which have been heavily overfished. Species abundance and distribution prior to the 20th century in the Mediterranean remains poorly known. To reconstruct the past biogeography of Mediterranean groupers, we investigated whether Zooarchaeology by Mass Spectrometry (ZooMS) can be used for identifying intra-genus grouper bones to species level. We discovered 22 novel, species-specific ZooMS biomarkers for groupers. Applying these biomarkers to Kinet Höyük, a Mediterranean archaeological site, demonstrated 4000 years of regional Epinephelus aeneus dominance and resiliency through millennia of fishing pressures, habitat degradation and climatic changes. Combining ZooMS identifications with catch size reconstructions revealed the Epinephelus aeneus capacity for growing 30 cm larger than hitherto documented, revising the maximum Total Length from 120 to 150 cm. Our results provide ecological baselines for a key Mediterranean fishery which could be leveraged to define and assess conservation targets.</p

Grouping groupers in the Mediterranean:Ecological baselines revealed by ancient proteins

Marine historical ecology provides a means to establish baselines to inform current fisheries management. Groupers (Epinephelidae) are key species for fisheries in the Mediterranean, which have been heavily overfished. Species abundance and distribution prior to the 20th century in the Mediterranean remains poorly known. To reconstruct the past biogeography of Mediterranean groupers, we investigated whether Zooarchaeology by Mass Spectrometry (ZooMS) can be used for identifying intra-genus grouper bones to species level. We discovered 22 novel, species-specific ZooMS biomarkers for groupers. Applying these biomarkers to Kinet Höyük, a Mediterranean archaeological site, demonstrated 4000 years of regional Epinephelus aeneus dominance and resiliency through millennia of fishing pressures, habitat degradation and climatic changes. Combining ZooMS identifications with catch size reconstructions revealed the Epinephelus aeneus capacity for growing 30 cm larger than hitherto documented, revising the maximum Total Length from 120 to 150 cm. Our results provide ecological baselines for a key Mediterranean fishery which could be leveraged to define and assess conservation targets.</p