Photograph by Brian J. Skerry, Nat Geo Image Collection

Trans-Atlantic movements and behaviour of shortfin mako sharks in the

North Atlantic Ocean

Dulce Cavalheiro Duarte Mestrado em Biodiversidade, Genética e Evolução Departamento de Biologia 2019-2020 Orientador Nuno Queiroz, PhD, Faculdade de Ciências

FCUP 1 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Todas as correções determinadas

pelo júri, e só essas, foram efetuadas. O Presidente do Júri,

Porto, ______/______/______

FCUP 2 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Acknowledgements

I would first like to thank my thesis advisor Doctor Nuno Queiroz of CIBIOInBIO – Research Center in Biodiversity and Genetic Resources at Faculty of Sciences of University of Porto. The door to Prof. Queiroz office was always open whenever I ran into a trouble spot or had a question about my research or writing. He consistently allowed this paper to be my own work but steered me in the right direction whenever he thought I needed it.

Finally, I must express my very profound gratitude to my parents, to my friends, to Miguel and to my pets. To my parents, a thank you for providing me with unfailing support and continuous encouragement throughout my years of study and through the process of researching and writing this thesis. To Inês, I am grateful that you are my other half, my pauper to the princess. Thank you for all the laughs and all the crying. To Monte, thank you for never giving up on me. Also, thank you for liking Avenged Sevenfold. Thank you both, and to Pessegueiros, for all the memories that I will forever treasure. Coimbra é nossa. To Miguel, a special gratitude for always being next to me even on the worst days. Thank you so much for being the calm in the chaos and for loving me when I thought no one could. We will forever be on the same team. Our team. To Lilo, Allie and Olivia, thank you for invariably making me smile. This accomplishment would not have been possible without them. Thank you.

Author,

Dulce Cavalheiro Duarte

FCUP 3 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Resumo

O tubarão anequim, Isurus oxyrinchus, é uma espécie pelágica que apresenta uma distribuição geográfica global. Atualmente, é cada vez mais apanhado tanto em pesca focada à espécie, como é pescado de forma acessória por navios de pesca industrial de palangre, cujo principal alvo são espécies comerciais, como atuns e peixe-espada. Devido ao declínio populacional que esta espécie está a sofrer, resultante da pressão pesqueira, o tubarão anequim foi recentemente classificado pela União Internacional para a Conservação da Natureza (UICN) como “Em Perigo” de extinção. No entanto, o conhecimento atual sobre as características da história de vida da espécie, a sua distribuição espacial, a utilização de habitat e a dinâmica populacional é muito escasso. O principal objetivo deste estudo é contribuir para um aperfeiçoamento da informação que existe, sobre padrões no movimento e distribuição da espécie e compreender o uso de habitat que o tubarão anequim tem no Norte do Oceano Atlântico. Para tal, de 2009 a 2018, observadores de pesca científicos adquiriram dados sobre o tamanho, género e capturas por unidade de esforço (CPUE) de tubarões anequim, apanhados como pesca acessória pela frota Espanhola de palangre de superfície ao longo do Oceano Atlântico, perfazendo um total de 12.940.249 kg de tubarão anequim em 1826 dias de pesca. Os resultados desta investigação confirmaram que esta espécie apresenta uma distribuição geográfica global. Neste estudo, estão descritos três movimentos transatlânticos no Norte do Oceano Atlântico, o que pode sugerir a existência de dois stocks populacionais de tubarão anequim nessa região. Em adição, também foram detetados movimentos horizontais sazonais, mais especificamente, durante o inverno. Os tubarões anequim movem-se para menores latitudes e águas oceânicas, sendo que, nos meses mais quentes, movem-se para latitudes superiores e para águas de menor profundidade, na placa continental. Neste estudo, também foi encontrada alta-fidelidade a regiões específicas, altamente produtivas que representam importantes áreas de alimentação da espécie. O tamanho dos espécimes variou entre 125 cm fork length (FL) a 255 cm FL, sendo que, indivíduos mais pequenos ocorriam em águas mais costeiras e indivíduos maiores ocupavam zonas de oceano aberto. A distribuição de tamanhos encontrada pode indicar a existências de zonas de berçário onde os indivíduos mais pequenos ocorrem. A proporção de géneros revelou a presença de mais fêmeas, com 1.3 fêmeas para cada macho, podendo estes resultados refletir segregação sexual. No Atlântico Norte, valores maiores de CPUE foram encontrados em águas costeiras e no Atlântico Sul, tanto águas costeiras como oceano aberto, apresentam valores elevados de CPUE para o tubarão anequim. A distribuição da CPUE está relacionada com as

FCUP 4 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean preferências do habitat da espécie, e os pesqueiros industriais de palangre tiram vantagem dessas regiões preferenciais para aumentar a taxa de pesca. Além destes resultados, diferenças anuais, sazonais e regionais significativas na CPUE foram reveladas, com uma tendência crescente na média da CPUE, desde 2016, no Sul do Oceano Atlântico. Para investigar a utilização vertical de habitat, de 2008 a 2017, sete tubarões anequim foram marcados com Pop-up Satellite Archival Tags (PSAT), num total de 1.635 dias, no Atlântico Norte. Não foi revelado um padrão de movimento de ciclicidade diária e verificou-se que os tubarões anequim ocupam preferencialmente águas superficiais, de 0-70 m com temperaturas entre os 17º C e os 21º C. Ocasionalmente, para indivíduos mais pequenos, ocorreram mergulhos mais profundos para águas mais frias, seguidos de rápidas ascensões. A profundidade máxima atingida foi de 1888 m e a temperatura mínima registada foi 2.2º C. Adicionalmente, também foram demonstradas diferenças no uso de habitat entre adultos e juvenis, dos quais, os primeiros apresentam uma utilização de habitat vertical expandida em relação aos juvenis, tanto de dia como de noite. Os resultados deste estudo contribuem para uma melhor compreensão sobre as tendências de distribuição, organização populacional e uso de habitat do tubarão anequim, reconhecendo o impacto que esta espécie sofre com a contínua pesca por navios pesqueiros industriais de palangre de superfície no Oceano Atlântico. Com os resultados apresentados nesta investigação, é possível a criação de medidas de gestão e conservação mais eficazes, para garantir a sustentabilidade da espécie.

Palavras-chave: Isurus oxyrinchus, Pesca acessória, Distribuição vertical, Utilização de habitat, Telemetria por satélite

FCUP 5 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Abstract

The shortfin mako, Isurus oxyrinchus, is a pelagic shark with a worldwide distribution that is increasingly harvest both as a target species and as by-catch through commercial pelagic longline vessels in the Atlantic Ocean targeting tunas and swordfish. Due to population decline resulted from fishing pressure, the shortfin mako was recently classified as “Endangered” by the International Union for the Conservation of Nature (IUCN). However, the present knowledge regarding the species life history traits, spatial distribution, habitat use, and population dynamics is very limited. The main goal of this investigation is the enhancement of the information on the species movement and distribution trends and to grasp the habitat use in the North Atlantic Ocean. For this purpose, from 2009 to 2018, scientific observers recovered by-catch data regarding the species length, sex and catch per unit of effort (CPUE) by Spanish longline vessels throughout the Atlantic Ocean, encompassing 12.940.249 kg of shortfin mako sharks in 1826 fishing days. The results from this study confirmed the extensive geographic distribution of the shortfin mako. In this study are described three trans-Atlantic movements in the North Atlantic Ocean which might suggest the existence of two shortfin mako population stocks in that region. Seasonal horizontal movements were also found with mako sharks moving to lower latitudes and oceanic waters in colder months and moving to upper latitudes and into the continental shelf in warmer months. In this research is also displayed high site fidelity to specific regions, extremely productive that represent important feeding grounds to the species. The mako lengths ranged from 125 cm to 255 cm fork length (FL), where smaller individuals occurred in inshore waters and bigger individuals were found in offshore waters and the sex ratio results exposed more females than males, with 1.3 females per male. These results may reflect sexual segregation. The size distribution may indicate the presence of nursery zones where smaller specimens occur. In the North Atlantic, higher CPUE were found in inshore waters and for the South Atlantic, both inshore and offshore regions had high CPUE for the shortfin mako shark. The CPUE distribution is correlated with habitat preferences of the shortfin mako and the longline fishing industry takes advantage of these regions to increase their catches. In addition, significant yearly, seasonal, and regional differences in the CPUE were found with an increasing trend in the mean CPUE for the South Atlantic Ocean since 2016. Moreover, during 1.635 tracking days, from 2008 to 2011 and in 2017, seven shortfin mako sharks were tagged with Pop-up Satellite Archival Tags (PSAT) in the North Atlantic Ocean. There was no clear diel vertical behaviour pattern, with shortfin mako occupying most of its time at surface waters, from 0-70 m, with preferred

FCUP 6 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean temperatures between 17º C and 21º C. Deeper dives followed by fast ascends were recorded for smaller individuals. The maximum depth registered was 1888 m and the minimum temperature was 2.2º C. In addition, different habitat utilization was found among different maturity stages, with adults using an expanded range of vertical habitat than juveniles both in day and nighttime. The findings in this study contribute with a greater comprehension of the shortfin mako shark distribution trends, population organization and habitat use, acknowledging the impact this species suffers with the continued harvest by longline vessels in the Atlantic Ocean. With the present results, it is possible to do improved science-based management and conservation decisions to assure the species sustainability.

Keywords: Isurus oxyrinchus, By-catch, Vertical distribution, Horizontal distribution, Satellite telemetry

FCUP 7 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Index

Acknowledgements, 2 Resumo, 3 Abstract, 5 List of tables, 9 List of figures, 10 List of abbreviations, 12 Chapter One: General Introduction, 13 1.1 The Shortfin Mako, Isurus oxyrinchus, 13 1.2 Geographic Distribution and Habitat, 14 1.3 Movements and Environmental Preferences, 14 1.4 Biology and Ecology, 15 1.4.1 Diet, 15 1.4.2 Prey preferences and variation, 16 1.4.3 Age and Growth, 18 1.4.4 Reproduction,19 1.5 Fisheries and Assessment status, 20 1.5.1 Fisheries, 20 1.5.2 Stock structure and Status, 22 1.6 Pop-up Satellite Archival Tags and Smart Position Only Temperature Tags, 23 References, 25 Chapter two: Horizontal habitat use of the Shortfin Mako shark in the Atlantic Ocean, 34 2.1 Abstract, 34 2.2 Introduction, 34 2.3 Material and Methods, 36 2.4 Results, 39 2.5 Discussion, 48 References, 53

FCUP 8 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Chapter three: Vertical habitat use of the Shortfin mako shark in North Atlantic Ocean, 60 3.1 Abstract, 60 3.2 Introduction, 60 3.3 Material and Methods, 62 3.4 Results, 63 3.5 Discussion, 70

References, 72 Chapter four: Closing examination, 77 Appendix A, 80

FCUP 9 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

List of tables

Table 3.1 – Total number of shortfin mako, Isurus oxyrinchus, individuals, both males and females and maturity stage, juvenile and adult.

Table A.1 – Attributes of Shortfin mako, Isurus oxyrinchus, tagged in this study with both PSAT and SPOT tags, with information on length (cm FL), sex, tagging date, tagging coordinates, final coordinates, and days at liberty. F = Female; M = Male.

FCUP 10 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

List of figures

Figure 1.1 - llustration of a shortfin mako, Isurus oxyrinchus. Image retrieved from fao.org

Figure 1.2 - Geographic distribution of Isurus oxyrinchus. Image retrieved from IUCN SSC Shark Specialist Group 2018. Isurus oxyrinchus. The IUCN Red List of Threatened Species. Version 2019-3.

Figure 2.1 – Trajectories made by the shortfin mako, Isurus oxyrinchus, tracked with PSAT and SPOT tags for this study and respective tag ID’s, between 2009 and 2017. White triangles represent tagging locations and black pentagons represent final locations.

Figure 2.2 - Length distribution (cm FL) and location of the 41 shortfin makos, Isurus oxyrinchus, used for this study from 2009 to 2017. Lighter circles represent smaller sizes and darker circles correspond to bigger sizes.

Figure 2.3 – Sex distribution of the shortfin mako, Isurus oxyrinchus, recorded in 1º x 1º grids, caught between 2009 and 2017.

Figure 2.4 – Spatial distribution of the fishing effort in number of Kg caught of shortfin mako, Isurus oxyrinchus, in the Atlantic Ocean from the Spanish longline fleet between 2013 and 2018.

Figure 2.5 – Seasonal movements of the shortfin mako, Isurus oxyrinchus, tracked in this study between 2009 and 2017. Blue circles correspond to Winter; green circles correspond to Spring; yellow circles correspond to Summer and orange circles correspond to Autumn.

Figure 2.6 – Differences in size distribution (cm FL) of Shortfin mako, Isurus oxyrinchus, caught between 2009 and 2017 in Eastern North Atlantic and Western North Atlantic.

Figure 2.7 – Differences in the number of female and male specimens of shortfin mako, Isurus oxyrinchus, in each season, Winter, Spring, Summer and Autumn. Pink bars represent females and blue bars represent males.

Figure 2.8 – Yearly distribution of the mean CPUE (Kg/Effort) of Shortfin mako, Isurus oxyrinchus, in North Atlantic and South Atlantic, between 2013 and 2018. The error bars are also represented.

FCUP 11 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Figure 2.9 – Seasonal distribution of the mean CPUE (Kg/Effort) of shortfin mako, Isurus oxyrinchus, in North Atlantic and South Atlantic, between 2013 and 2018. The error bars are also represented.

Figure 3.1 – Vertical habitat preferences of the shortfin mako, Isurus oxyrinchus, for time- at-depth (m) and time-at-temperature (°C), during daytime and nighttime.

Figure 3.2 – Detailed diving characterization of two shortfin mako sharks, Isurus oxyrinchus, tagged with pop-up satellite archival (PSAT) tags. The top plot, from shark 86407, a juvenile, displays the most common diving pattern movement from smaller specimens. The bottom plot, from shark 86408, an adult, exhibits the rare diving behaviour where the specimens spent several days in depth (m), common for larger specimens.

Figure 3.3 – Habitat use of the shortfin mako sharks, Isurus oxyrinchus. The data is classified in 6 hours classes and divided by, depth (m), temperature (°C) and maturity stage. In the plots are depicted the medians, the 95% confidence interval of the medians, the 75th percentile (Q1), 25th percentile (Q3) and the outliers, in red.

Figure 3.4 – Habitat preferences of juveniles and adults of shortfin mako, Isurus oxyrinchus, for time-at-depth (m) and time-at-temperature (°C), during daytime and nighttime.

FCUP 12 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

List of abbreviations

Catch Per Unit Effort (CPUE) Convention on International Trade in Endangered Species (CITES) Fork Length (FL) International Commission for the Conservation of Atlantic Tunas (ICCAT) International Union for the Conservation of Nature (IUCN) “Mako shark” refers to shortfin mako, Isurus oxyrinchus Pop-up Satellite Archival Tags (PSAT) Smart Position Only Temperature (SPOT) Tonnes (t) Total Allowable Catch (TAC) Total Length (TL) União Internacional para a Conservação da Natureza (UICN) Unscented Kalman Filter with Sea-Surface Temperature (UKFSST) Wildlife Computers (WC)

FCUP 13 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Chapter One: General Introduction 1.1 The Shortfin Mako, Isurus oxyrinchus The shortfin mako (Isurus oxyrinchus Rafinesque, 1810) (Figure 1.1), commonly known as shortfin mako shark is an oceanic epipelagic shark species classified among Lamnidae family with a large-scale geographic distribution from temperate areas to tropical waters (Compagno, 2001; Abascal et al., 2011), in addition, this species is very active because it is characterized by being endothermic, using a heat exchanging circulatory system that allows the shark to uphold its body temperature higher than its habitat, making it the fastest swimming fish (Carey et al., 1981; Compagno, 2001). Throughout the entire geographic distribution of mako sharks, from south Pacific Ocean to North Atlantic, this species is caught as bycatch by longliners that target tunas or swordfish (Holts & Bedford, 1993). Furthermore, the shortfin mako is popular among sport fishers and in some countries such as, China there is a demand of shark meat and shark fin exploitation for their traditional cuisine of shark fin soup (Holts & Bedford, 1993; Eriksson & Clarke, 2015). All these factors combined resulted in a persisted harvesting of this species. Even though the shortfin mako has economic relevance, it is also a susceptible species since there is insufficient knowledge of its biology and its population dynamics with disagreement in ages and growth rates (Cailliet et al., 1983; Pratt et al., 1983; Bishop et al., 2006). Analogous to other shark species caught as bycatch, shortfin makos harvesting promoted apprehension regarding what that level of fisheries pressure would impact population stock and size of this species, with some literature stating a population decline since 1986 (Baum, 2003). The poor-quality data regarding bycatch species creates an obstacle in understanding the effects that fisheries have on shortfin makos, as well, on other pelagic sharks. As a result of the decline in population size from fisheries along with shortfin makos life history traits, this species has been recently classified as “Endangered” (Rigby et al., 2019).

Figure 1.1 - llustration of a shortfin mako, Isurus oxyrinchus. Image retrieved from fao.org

FCUP 14 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

1.2 Geographic Distribution and Habitat

Shortfin mako sharks are found worldwide across temperate and tropical oceanic waters (Abascal et al., 2011). In Eastern Atlantic Ocean, this species occurs from north Europe, such as, Norway to South Africa, encompassing the Mediterranean. In Western Atlantic, expands from the Gulf of Maine to southern Brazil and Argentina, inclusive, Gulf of Mexico and Caribbean. In Indo-Pacific, mako sharks are located from East South Africa to Hawaii, Primorskiy Kray in Russia to Australia, across the entire coast with exception of Arafura Sea, Gulf of Carpentaria and Torres Strait and New Zealand. In the Eastern Pacific, this species is spread from south of Aleutian Islands to Washington and California, in USA to Chile (Compagno, 2001; Rigby et al., 2019).

Figure 1.2 - Geographic distribution of Isurus oxyrinchus. Image retrieved from IUCN SSC Shark Specialist Group 2018. Isurus oxyrinchus. The IUCN Red List of Threatened Species. Version 2019-3. 1.3 Temperature and Movements Preferences The shortfin mako is an epipelagic endothermic fish with a widespread distribution and appears from the surface to lower depth limits of 888 m, notwithstanding being an oceanic fish, it occurs sporadically near to the seashore in regions, such as, South Africa, where the continental shelves are narrow (Compagno, 2001; Abascal et al., 2011). Several studies emphasize that shortfin mako vertical movements are closely correlated with ocean temperatures and that it appears this species spends great part of the time in the mixed layer (Holts & Bedford, 1993). According to Abascal et al. (2011), shortfin makos showed preferences for water temperature among 13.4º C and 24.1º C in southern Pacific. Casey & Kohler (1992) recovered analogous temperatures, between 17º C and 22º C, preferred by the shortfin mako in the North Atlantic Ocean and

FCUP 15 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean concluded that shortfin mako harvested as bycatch in swordfish longliners were caught in temperature range between 18.5º C and 20.5º C. In another tracking study of three mako juveniles in southern California, the preferred water temperature was between 20º C and 21º C and the individuals spent 90% of the total time in the mixed layer, above 20 m, with exceptional short-timed dives below the thermocline during daytime periods (Holts & Bedford, 1993). In the same research, shortfin mako specimens presented no horizontal movements tendency, except from the pattern exhibited in the coastal area from late June to July (Holts & Bedford, 1993). In a research by Sepulveda et al. (2004), the authors tracked the movements of seven shortfin mako juveniles and recovered identical conclusion. The peculiarity was of a few mako sharks that did excursions below the thermocline up to 200 m, with the mentioned dives occurring, also, in the daytime. Another study encountered the same results since a mako shark tagged in South California did excursion between 150 m and 400 m during daytime periods (Loefer et al., 2005). At last, an additional investigation in Southern California displayed that of the three mako sharks that were tracked, two of them presented deeper dives in the night- time hours, although, the deepest excursion registered was at 65 m (Klimley et al., 2002). All these studies serve as proof that, regardless of not being a rule, deeper distributions occur over daytime hours. This results are contradictory to the ones obtained in another study in Western Atlantic, where the tracking of one large female shortfin mako showed that it spent most of the tracking time below 100m and reached depths of 400 m seldom going above 100 m, conceivably to stay away from the upper mixed layer (Carey et al., 1981).

1.4 Biology and Ecology 1.4.1 Diet In defiance of the shortfin mako being an apex predator with a regulatory role in marine systems and comparatively to the lack of knowledge regarding this species biology and population dynamics, its feeding habits are, also, poorly known. Although there are a few studies regarding this matter, the studies diverge in time and in space, confined to South Africa (Cliff et al., 1990; Dudley & Cliff, 2010), North-eastern Atlantic (Maia et al., 2006), Northwest Atlantic (Stillwell & Kohler, 1982) and North-eastern Pacific (Preti et al., 2012). Sharks are thought to be cosmopolitan feeders, eating the most abundant prey in the region, in this case, fish being the food available in large number. Teleost items were found to be one of the major prey shortfin makos consumed, with Stillwell & Kohler (1982) stating teleosts as the most important group in makos diet in Northwest Atlantic and being the second most meaningful in South Africa (Cliff et al.,

FCUP 16 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

1990; Dudley & Cliff, 2010). Among the teleosts group, Clupeiformes, garpike, Belone belone (Linnaeus, 1761), Sauries, Scomberesox saurus (Walbaum, 1792), alepisaurids, blue fish, Pomatomus saltatrix (Linnaeus, 1776) and Scombridae family were identified in North Atlantic, with the two latter considered the uttermost significant prey. Swordfish, Xiphias gladius (Linnaeus, 1758), was also identified present in some stomachs (Stillwell & Kohler, 1982; Maia et al., 2006). In the North Pacific, Pacific saury, Cololabis saira (Brevoort, 1856), was found as the most relevant prey regarding teleosts. Further dominant teleost items comprised Pacific sardine, Sardinops sagax (Jenyns, 1842), Pacific mackerel, Scomber japonicus (Houttuyn, 1782), Jack mackerel, Trachurus symmetricus (Ayres, 1855) and Striped mullet, Mugil cephalus (Linnaeus, 1758) (Preti et al., 2012). In relation to cephalopods, this prey group was considered as substantially influential in the shortfin mako diet, being the second most significant group for the North Atlantic (Stillwell & Kohler, 1982; Maia et al., 2006). The jumbo squid, Dosidicus gigas (d'Orbigny, 1835), occurred as the outmost influential cephalopod prey in the North Pacific (Preti et al., 2012). Concerning elasmobranchs in shortfin mako diet, the results are largely dissimilar. In South Africa, elasmobranchs were present in more than half of the stomachs examined with food, representing the most usual item found in the predators’ stomachs, where the milkshark, Rhizoprionodon acutus (Rüppell, 1837) was the most frequent species (Cliff et al., 1990). Discordant to that research, studies from North Atlantic present elasmobranchs as insignificant as a prey category in the shortfin mako diet (Stillwell & Kohler, 1982; Maia et al., 2006). Lastly, relative to Cetaceans, Stillwell & Kohler (1982) found remaining parts of that group in three stomachs and Preti et al. (2012) found one small shortfin mako that ate on a shortbeaked common dolphin, Delphinus delphis (Linnaeus, 1758). Taking into account the immense ricketiness that is present in the shortfin mako diet, it is easy to consider that this species feed opportunistically, however, swordfish is a fast-swimming prey. This suggests that, even though, shortfin makos may feed on abundant preys available, this fish also uses its energy to hunt specific food items.

1.4.2 Prey preferences and variation

Results from several studies with reference to the size of the prey disclosed that the prey consumed by shortfin makos is related to the size of the predator. Cliff et al., (1990) brought to attention that nearly all prey groups in shortfin mako stomachs sized between 23% and 35% of the length of the mako specimens, indicating that the selection that shortfin mako does when feeding is made in relation to the prey size, after all, hunting prey items that are smaller may represent a large investment of energy. In another study

FCUP 17 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean by Preti et al. (2012), results showed that for smaller mako individuals, Pacific sardine was presented in higher portions, along with Pacific saury being the most significant item in medium sized shortfin mako sharks, with one of those medium sized predators having eaten on a Short-beaked common dolphin, Delphinus delphis. For larger mako sharks, the jumbo squid was the most meaningful prey item. In both investigations from North Atlantic, remains of swordfish were found, however, Stillwell & Kohler (1982) declared that sharks over 150 kg could target on swordfish and Maia et al. (2006) found seven medium to large sharks with weights ranging between 18.5 kg and 293 kg with swordfish in the stomachs. This proofs that instead of shortfin mako changing the diet as it grows, this predator expands the prey groups it forages instead of changing the prey it consumes. The shortfin mako performs some of their movements in relation to the prey present in its diet. In coastal waters, this species feeds more out of teleosts, particularly, blue fish in North Atlantic, while cephalopods represented a modest portion of the shortfin mako diet (Stillwell & Kohler, 1982). Seaward, the portion of fish in the diet was less significant on account that blue fish presence in I. oxyrinchus stomachs decreased, notwithstanding, the previous non-abundant cephalopods turn substantial with squids depicting the most significant food in seaward waters (Stillwell & Kohler, 1982). Seasonal variation in the shortfin mako diet is also discernible, where prey abundance or availability fluctuations due to season may alter prey selection (Preti et al., 2012). In North Atlantic, studies from March to May indicated that cephalopds represented an irrelevant group, however, teleosts constituted the main prey group for shortfin mako sharks, with the blue fish being, particularly, the most significant teleosts in Northwest Atlantic and Garpike occurring more frequently in shortfin mako stomachs in North- eastern Atlantic during spring (Stillwell & Kohler, 1982; Maia et al., 2006). Over summer months, from June to August, teleosts were infrequent in the shortfin mako stomachs, while cephalopods exhibited higher significance (Stillwell & Kohler, 1982). Maia et al. (2006) disclosed that, during summer season, crustaceans are highly predated by shortfin mako juveniles and young-of-the-year. A possible justification for that may be the considerable abundance of crustaceans in North Atlantic. Throughout fall season, from September to November, the two aforementioned prey groups represented roughly the same relevance as food items (Stillwell & Kohler, 1982). In North-eastern Pacific, the striped mullet was a very important teleost in the predator’s diet during fall season considering that around fall months, striped mullet initiates the spawning migrations from near coast environments to the open sea (Preti et al., 2012). In regard to variation by sex of shortfin mako and its diet, no differences among sexes were found (Stillwell & Kohler, 1982; Preti et al., 2012). Considering all the studies above cited, teleosts are the most

FCUP 18 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean important prey group to shortfin mako diet. Motta & Wilga (2001) recognized that the shortfin mako shark being an opportunistic feeder, will prey on the most abundant and available food, that is, other fish. A deep understanding of shortfin mako feeding behavior as an apex predator, is crucial to comprehend trophic relations and changes in the ecosystems.

1.4.3 Age and Growth In order to understand age and growth in Isurus oxyrinchus, diversified investigations used a variety of techniques, nevertheless, those studies produced discordant results regarding age and growth rates estimations as a result of controversy in band deposition rates. In a study (Pratt et al., 1983) determined that two vertebral band pairs were deposited in a year in shortfin mako sharks from North Atlantic. Contrarily, a study from Cailliet et al. (1983) discovered that one band pair was deposited per year in mako specimens from North Pacific. The disagreement between band deposition rates each year resulted in discrepancy in estimations regarding age and growth rates in the different studies. The results from two studies using bomb radiocarbon analysis of vertebras from a shortfin mako in North Atlantic agrees to Cailliet et al. (1983) of one band pair deposition each year (Campana et al., 2002; Ardizzone et al., 2006). In the East Pacific Ocean, Ribot-Carballal et al. (2005) also corroborated with annual band deposition. The vast majority of recent investigations regarding shortfin mako growth validate the hypothesis proposed by Cailliet et al. (1983), where one band symbolizes one year of age. In the same study the longevity estimation of shortfin makos was from 0 to 18 years and another research by Ribot-Carballal et al. (2005) agreed with those age estimations. In a study from Cerna & Licandeo (2009), the maximum age assessment for the shortfin mako in Southeast Pacific was 25 years, similar to the results obtained by Campana et al. (2005) in East Atlantic of 24 years, yet, these results differ from a few studies were the estimation for maximum age was 29 years in shortfin mako specimens from New Zealand (Bishop et al., 2006), 28 years in mako sharks from South Atlantic (Doño et al., 2014) and 29 to 32 years for shortfin mako in North Atlantic (Ardizzone et al., 2006; Natanson et al., 2006) with, to our knowledge, 32 years being the longest longevity documented for both males and females. In regard to shortfin makos length, the results differ in the various studies. Campana et al., (2005) stated that the mean length for females was 138 cm fork length (FL) and for males was 148 cm FL. Moreover, almost all shortfin mako sharks with a length superior to 250 cm FL were females and the authors did not found confirmation of sexual dimorphism in growth for the first 13 years of the species life. In another study, the length of the females was comprehended between 75 cm to 330 cm total length (TL), while for males was in 76 cm

FCUP 19 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean to 285 cm TL. Lastly, Doño et al. (2014) reported that, for South Atlantic waters, female length varied between 101 cm to 330 cm FL whereas males ranged between 81 cm to 250 cm FL. In North Atlantic, this species presents greater growth in summer when comparing to winter months, suggesting an interrelation among growth and season (Maia et al., 2007).

1.4.4 Reproduction Isurus oxyrinchus is an aplacental viviparous species, which means that mother and embryo are not directly connected with embryos in developing stage carrying out oophagy (uterine cannibal), that is, the embryos with about 6 cm TL feed on eggs produced by the mother’s continued ovulation or else feed on other developing embryos (Mollet et al., 2000; Costa et al., 2002). Several studies show that shortfin mako females can have between 4 to 30 young ready to be born shortfin mako per litter, although, litter size is correlated to maternal size (Mollet et al., 2000; Compagno, 2001). According to Mollet et al. (2000) the gestation period is between 15 to 18 months with a three-year reproductive cycle, while Joung & Hsu (2005) stated that gestation occurred between 23 to 25 months in North West Pacific. Mollet et al. (2000) declared that the birth of young shortfin mako sharks happened during late winter to mid-spring worldwide, per contra, Maia et al. (2007) suggested that parturition occurred in early summer or before that season in North Atlantic and the same was proposed by Costa et al. (2002). In North- West Pacific, parturition is from late winter to early summer (Joung & Hsu, 2005). Sexual maturity is reached when shortfin mako males have the capacity to produce feasible sperm and have ways of reaching the female and when the females adequate to produce viable eggs and sustain the embryos (Campana et al., 2005). Measures used in reproductive studies acknowledged the possibility to assess the length at which both males and females mature sexually. Regarding shortfin mako males, previous studies declared that in North-Western Atlantic, males become mature at intervals between 180 cm FL and 199 cm FL (Campana et al., 2005; Maia et al., 2007). For South Pacific, sexual maturity estimations ranged from 180 cm to 185 cm FL (Francis & Duffy, 2005; Conde-Moreno & Galván-Magaña, 2006; Cerna & Licandeo, 2009) whilst in Indic Ocean, length at maturity was determined between 177–188 cm TL (Francis & Duffy, 2005). All these results diverge slightly from the results obtained by Stevens (1983) at which males turned mature at 195 cm TL. For North-Western Pacific, investigations suggest that 50% of the males become mature sexually at 210 cm TL (Joung & Hsu, 2005). With reference to female sexual maturation Mollet et al. (2000) stated that females in North Atlantic Ocean were mature at a size that ranged from 276 cm to 320 cm TL and Campana et al. (2005) showed similar results in North-western Atlantic, with females reaching sexual

FCUP 20 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean maturity at 330 cm FL. In the study from Maia et al. (2007) in the same region, the authors were only able to find one apparent mature female with 290 cm FL, although it was a virgin. In the South Hemisphere, estimations for several studies fall within the same length range, with reports of females from South Atlantic and South Pacific that were sexually mature between 260 cm 285 cm TL (Stevens, 1983; Mollet et al., 2000; Francis & Duffy, 2005; Cerna & Licandeo, 2009). In North West Pacific, length at maturity in females was established between 260 cm to 296 cm TL. All these results proof that females mature at a superior age than males and that length at maturity is dependent of the regions, with females in North Atlantic Ocean may mature at a greater length than females in South waters, as proposed by Mollet et al. (2000). In a Cerna & Licandeo (2009) investigation, length estimations at birth for shortfin mako females was 70 cm TL and for males 79,3 cm TL. Notwithstanding, other studies present size at birth variations between 70 cm TL (Mollet et al., 2000), reaching 77 cm TL in South Pacific (Duffy & Francis, 2001) to 79 cm FL in North West Pacific (Joung & Hsu, 2005). Furthermore, young-of-the-year shortfin mako sharks length fluctuates from 78 and 81 cm FL (Doño et al., 2014). Comparisons in growth rate estimations regarding young-of-the-year also present dissimilarity in different regions, with studies indicating growth rates of 38 cm year−1 in waters from South West Pacific (Bishop et al., 2006), 50 cm year−1 and 40 cm year−1 for North-Western Atlantic (Pratt et al., 1983; Natanson et al., 2006), 61,1 cm year- 1 for North-Eastern Atlantic (Maia et al., 2007) and growth rates between 16 cm and 19 cm year−1 in South-western Pacific (Cerna & Licandeo, 2009). Cailliet et al. (1993) suggested that southern California could be a nursery area for juveniles and new-born pups.

1.5 Fisheries and Assessment status 1.5.1 Fisheries

When fishing for target species, the gear used commonly results in indiscriminate harvest of both target species and non-commercially viable organisms. There are several marine species vulnerable to be caught as by-catch, such as, sea turtles, marine mammals, seabirds and pelagic sharks. Commercial longline fisheries targeting swordfish and tunas represent the biggest threat to sharks caught as by-catch worldwide (Oliver et al., 2015). Encompassed by all pelagic sharks, the shortfin mako is one of the most frequently captured shark species, specially, in North Atlantic, and is distinguished as a species with high commercial interest, forasmuch as its fins and meat have significant market value, hence, this species is less expected to be discarded or released at sea (Campana et al., 2015; Holts & Bedford, 1993). The meat is for consumption and

FCUP 21 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean can be eaten fresh, frozen, smoked and dried-salted; the oils are used to produce vitamins; the fins for shark-fin soup; the skin is transformed into leather and, lastly, its teeth and jaws are employed in the making of embellishments (Compagno, 2001). Babcock & Nakano (2008) stated that, in 1995, 10 000 tonnes (t) of shortfin mako were caught as by-catch by longliners targeting tuna fish in the Atlantic Ocean. In the oceanic area bounded by Azores and the Iberian Peninsula, 366 t and 304 t of shortfin mako were caught in 1983 and 1984, respectively by the Spanish longline vessels (Mejuto & Gárces, 1984; Mejuto, 1985). For the same Spanish longline fishery, Bonfil (1994) forecast that 750 t per year of shortfin makos were landed in the Atlantic Ocean and Mediterranean Sea and that in the North Atlantic 360 t each year of shortfin mako were harvested. Hurley (1998) reported 157 t of shortfin mako landed in 1994 in Western Atlantic. According to Costa et al. (1996) a longline fleet in Brazil harvested 13,3 and 138,3 t in 19 years. Along the West coast of the United States, between 2000 and 2018 an annual average of 40 t of this predator was landed (PFMC, 2020), in addition, in the south coast of California alone, 200 t per year of shortfin mako were landed as by-catch from commercial vessels (Holts & Bedford, 1993). In New Zealand, annual landing reports of shortfin mako estimated 200 t (Francis et al, 2001) and in South Africa, between 1992 and 1994, local longline fisheries caught 133 t of shortfin mako (Kroese & Sauer, 1998). This top predator is also captured offshore by sports anglers because it is one of the fastest swimming and acrobatic fish, making it highly popular for those enthusiasts in the challenge of fight (Babcock, 2008). Australia, New Zealand, and the United States are classic regions for this offshore sport, however, recreational angling also occurs in the Caribbean and Indian Ocean (Babcock, 2008). Moreover, this activity happens from July to October (Hurley, 1998). In Australia, along the coast of New South Wales, between 1961 and 1990, 28% of all elasmobranchs caught recreationally were shortfin mako, around 2206 individuals (Pepperell, 1992). Another study revealed that, for the same region, between 1996 and 2000, 40.1% of the landings were of the above- mentioned species (Murphy et al., 2002). Longline fisheries harvest shortfin mako sharks from 60 cm FL to 338 cm TL (Francis et al, 2001; Bustamante & Bennett, 2013), yet the average length was among 115 and 225 cm FL for both sexes (Arocha et al., 2002; Chang & Liu, 2009; Runcie et al., 2016). A study in New Zealand showed that 96% to 99% of females and 41% to 80% of males landed in longline catches were immature (Francis et al, 2001). Recreational fisheries studies suggest that in this type of offshore fishery, juveniles younger than 3 years comprise the majority of the catch and are probably immature (Hanan et al., 1993; O’Brien & Sunada, 1994).

FCUP 22 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

1.5.2 Stock structure and Status

Heist et al. (1996) and Schrey & Heist (2003) did mitochondrial and microsatellite studies in order to understand the genetic structure of shortfin mako population with samples from North Atlantic, South Atlantic, North Pacific and South Pacific. Both investigations concluded the presence of a single genetic stock with enough genetic exchange to consider mako shortfin mako a worldwide species. However, the results from Heist et al. (1996) showed that de samples retrieved from North Atlantic seemed to be isolated from the other oceanic regions. There is poor information concerning population assessment for shortfin mako and data reflecting long-term catch per unit effort (CPUE) trend is also limited. According to Baum (2003) and Matsunaga (2009), all pelagic sharks except makos (longfin and shortfin), have suffered a 50% decline since 1986, while mako sharks, mainly shortfin makos, have experienced a controlled decline and the stock status did not suffer a notoriously change. In a report for the International Commission for the Conservation of Atlantic Tunas (ICCAT), Babcock & Nakano (2008) concluded that shortfin mako have suffered decline in both North and South Atlantic, in conjunction with probably being below the biomass to assure sustainable harvest. In addition, in the same report is stated that the CPUE pattern indicate that, since 1970, this species had decrease over 50%. North-western Atlantic presented high CPUE of immature shortfin mako, implying that this area may be a nursery area for the species (Matsushita & Matsunaga, 2002). The ICCAT considers the shortfin mako stock one of the most susceptible stocks. Isolating the North and South Atlantic stocks, CPUE data showed a decrease of the North Atlantic stock since 2010 and an increased progression in the South Atlantic stock. For the North Atlantic, the shortfin mako biomass trend from 1950 to 2017, exposed decline rates of 1.2%, leading to 60% decline for three generations, 75 years. In a study of standardized catch rates in South Atlantic Ocean, Barreto et al. (2016) determined extreme declines of 99% in the average CPUE for the shortfin mako in the periods between 1979–1997 and 1998–2007. For the North Atlantic stock status, all models dictate with 90% probability that it is in an overfishing state. Regarding South Atlantic assessment stock, the results showed a 32.5% probability of being in an overfishing state. Globally, the shortfin mako population has suffered a 46.6% decline. The accurate assessment of shortfin mako population status is flawed owing to limited data from longline fisheries, such as, by-catch quantities and omission of mortality of individuals landed and discarded. These factors contribute to a predicament when evaluating fishing stocks and sustainability. Adding the life history traits of shortfin mako, its harvest as target and by-catch by fisheries and global population decline, this species

FCUP 23 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean was classified in 2019 by the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species as “Endangered” (Rigby et al., 2019).

1.6 Pop-up Satellite Archival Tags and Smart Position Only Temperature Tags In recent years, biotelemetry studies have experienced a rapid development due to the enhancement of tracking techniques and satellite tagging. This allowed the scientists to increase largely the information regarding a huge number of species habitat use, geographic distribution, movement patterns, and fisheries impact, especially in marine species such as, sharks (Wilson et al., 2007; Domeier & Nasby-Lucas, 2008; Jewell et al., 2011; Carvalho et al., 2015; Coelho et al., 2015; Queiroz et al., 2016), tunas (Marcinek et al., 2001; Wilson et al., 2005), swordfish (Dewar et al., 2011). The Pop-up Satellite Archival Tags (PSAT) are electronic gears attached to the pelagic sharks with a tether and various anchoring devices (Musyl et al., 2001). The PSAT can be employed from a boat utilizing a tagging lance (Hammerschlag et al., 2011). The PSAT use ARGOS satellite-based system and register data at determined periods of time at depth and time at temperature, as well environment light intensity, enabling geolocations to be computed (Musyl et al., 2001). The Smart Position Only Temperature (SPOT) tags are manually attached drilling across the shark dorsal fin, this means that the shark must be removed from the waters to be worked on (Jewell et al., 2011). SPOT tags use GPS based satellite telemetry and transmit data when the dorsal fin is out of the water. These tags have the ability to work over many years and have associated positioning errors under 1 km (Weng, 2005). Both PSAT and SPOT tags studies effectively provided new detailed knowledge about pelagic marine species. Brunnschweiler et al. (2010) found site fidelity to coastal areas. Ramirez et al. (2017) described that both adult and juvenile whale sharks present different patterns in their movement with juveniles having high site fidelity to the place they are born. Weng (2005) found that the salmon shark is expanding its niche into subartic regions. Previous studies on the shortfin mako tagged with both PSAT and SPOT tags, characterized distribution patterns and habitat use (Abascal et al., 2011; Rogers et al., 2015; Vaudo et al., 2017; Francis et al., 2019; Nasby-Lucas et al., 2019). Although PSAT and SPOT tags have proven to be extremely useful and powerful resources in the need for information on marine pelagic species, tags have considerable limitation, namely, animal mortality, failure due to salt-water switch, battery failure, antenna breakage, environmental conditions or interferences in the Argos satellite system and premature detachment (Hays et al., 2007; Musyl et al., 2011). Premature detachment is thought to have several causes, like the social behaviour of the tagged

FCUP 24 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean animal, infection and tissue degradation around the attached tag site or mechanical failure (Musyl et al., 2011). Hence, it is critical knowing the study species in order to adjust the methodology and the experience design (Musyl et al., 2011).

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References

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Hays, G. C., Bradshaw, C. J. A., James, M. C., Lovell, P., & Sims, D. W. (2007). Why do Argos satellite tags deployed on marine animals stop transmitting? Journal of Experimental Marine Biology and Ecology, 349(1), 52–60. https://doi.org/10.1016/j.jembe.2007.04.016 Heist, E. J., Musick, J. A., & Graves, J. E. (1996). Genetic population structure of the shortfin mako (Isurus oxyrinchus) inferred from restriction fragment length polymorphism analysis of mitochondrial DNA. Canadian Journal of Fisheries and Aquatic Sciences, 53(3), 583–588. https://doi.org/10.1139/f95-245 Holts, D. B., Julian, A., Sosa-Nishizaki, O., & Bartoo, N. W. (1998). Pelagic shark fisheries along the west coast of the United States and Baja California, Mexico. Fisheries Research, 39(2), 115–125. https://doi.org/10.1016/S0165-7836(98)00178-7 Holts, D., & Bedford, D. (1993). Horizontal and vertical movements of the shortfin mako shark, Isurus oxyrinchus, in the Southern California Bight. Marine and Freshwater Research, 44(6), 901. https://doi.org/10.1071/MF9930901 Hurley, P. C. F. (1998). A review of the fishery for pelagic sharks in Atlantic Canada. Fisheries Research, 39(2), 107-113. Jewell, O. J. D., Wcisel, M. A., Gennari, E., Towner, A. V., Bester, M. N., Johnson, R. L., & Singh, S. (2011). Effects of Smart Position Only (SPOT) Tag Deployment on White Sharks Carcharodon carcharias in South Africa. PLoS ONE, 6(11), e27242. https://doi.org/10.1371/journal.pone.0027242 Joung, S. J., & Hsu, H. H. (2005). Reproduction and embryonic development of the shortfin mako, Isurus oxyrinchus Rafinesque, 1810, in the northwestern Pacific. ZOOLOGICAL STUDIES-TAIPEI-, 44(4), 487. Klimley, P. A., Beavers, S. C., Curtis, T. H., & Jorgensen, S. J. (2002). Movements and swimming behavior of three species of sharks in La Jolla Canyon, California. Environmental Biology of Fishes, 63(2), 117–135. https://doi.org/10.1023/A:1014200301213 Kroese, M., & Sauer, W. H. H. (1998). Elasmobranch exploitation in Africa. Marine and Freshwater Research, 49(7), 573. https://doi.org/10.1071/MF97122 Loefer, J. K., Sedberry, G. R., & McGovern, J. C. (2005). Vertical Movements of a Shortfin Mako in the Western North Atlantic as Determined by Pop-up Satellite Tagging. Southeastern Naturalist, 4(2), 237–246. https://doi.org/10.1656/1528- 7092(2005)004[0237:VMOASM]2.0.CO;2

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Maia, A., Queiroz, N., Cabral, H. N., Santos, A. M., & Correia, J. P. (2007). Reproductive biology and population dynamics of the shortfin mako, Isurus oxyrinchus Rafinesque, 1810, off the southwest Portuguese coast, eastern North Atlantic. Journal of Applied Ichthyology, 23(3), 246–251. https://doi.org/10.1111/j.1439-0426.2007.00849.x Maia, Anabela, Queiroz, N., Correia, J. P., & Cabral, H. (2006). Food habits of the shortfin mako, Isurus oxyrinchus, off the southwest coast of Portugal. Environmental Biology of Fishes, 77(2), 157–167. https://doi.org/10.1007/s10641-006-9067-7 Marcinek, D. J., Blackwell, S. B., Dewar, H., Freund, E. V., Farwell, C., Dau, D., Seitz, A. C., & Block, B. A. (2001). Depth and muscle temperature of Pacific bluefin tuna examined with acoustic and pop-up satellite archival tags. Marine Biology, 138(4), 869– 885. https://doi.org/10.1007/s002270000492 Matsunaga, H. (2009). Standardized CPUE for blue shark and shortfin mako caught by the Japanese tuna longline fishery in the Atlantic Ocean. Collect. Vol. Sci. Pap. ICCAT, 64(5), 1677-1682. Matsushita, Y., & Matsunaga, H. (2002). Species composition and CPUE of pelagic sharks observed by Japanese observers for tuna longline fisheries in the Atlantic Ocean. ICCAT Collective Volume of Scientific Papers, 54(4), 1371-1380. Mejuto, J., & Garcés, A. G. (1984). Shortfin mako, Isurus oxyrinchus, and porbeagle, Lamna nasus, associated with longline swordfish fishery in NW and N Spain. ICES CM. Mejuto, J. (1985). Associated catches of sharks, Prionace glauca, Isurus oxyrinchus, and Lamna nasus, with NW and N Spanish swordfish fishery, in 1984. In International Council for the Exploration of the Sea, Council Meeting (p. 16). Mollet, H. F., Cliff, G., Pratt Jr, H. L., & Stevens, J. (2000). Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin, (2). Motta, P. J., & Wilga, C. D. (2001). Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environmental Biology of Fishes, 60(1/3), 131– 156. https://doi.org/10.1023/A:1007649900712 Musyl, M., Domeier, M., Nasby-Lucas, N., Brill, R., McNaughton, L., Swimmer, J., Lutcavage, M., Wilson, S., Galuardi, B., & Liddle, J. (2011). Performance of pop-up satellite archival tags. Marine Ecology Progress Series, 433, 1–28. https://doi.org/10.3354/meps09202 Murphy, J. J., Lowry, M. B., Henry, G. W., & Chapman, D. (2002). The gamefish tournament monitoring program–1993 to 2000. NSW Fisheries Final Report Series, 38, 93pp.

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Musyl, M. K., Brill, R. W., Curran, D. S., Gunn, J. S., Hartog, J. R., Hill, R. D., Welch, D. W., Eveson, J. P., Boggs, C. H., & Brainard, R. E. (2001). Ability of Archival Tags to Provide Estimates of Geographical Position Based on Light Intensity. In Electronic Tagging and Tracking in Marine Fisheries (Vol. 1, pp. 343–367). Springer Netherlands. https://doi.org/10.1007/978-94-017-1402-0_19 Nasby-Lucas, N., Dewar, H., Sosa-Nishizaki, O., Wilson, C., Hyde, J. R., Vetter, R. D., Wraith, J., Block, B. A., Kinney, M. J., Sippel, T., Holts, D. B., & Kohin, S. (n.d.). Movements of electronically tagged shortfin mako sharks (Isurus oxyrinchus) in the eastern North Pacific Ocean. Animal Biotelemetry, 7(1), 12. https://doi.org/10.1186/s40317-019-0174-6 Natanson, L. J., Kohler, N. E., Ardizzone, D., Cailliet, G. M., Wintner, S. P., & Mollet, H. F. (2006). Validated age and growth estimates for the shortfin mako, Isurus oxyrinchus, in the North Atlantic Ocean. Environmental Biology of Fishes, 77(3–4), 367–383. https://doi.org/10.1007/s10641-006-9127-z O’Brien, J. W., & Sunada, J. S. (1994). A review of the southern California experimental drift longline fishery for sharks, 1988–1991. California Cooperative Oceanic Fisheries Investigations Report, 35, 222-229. Oliver, S., Braccini, M., Newman, S. J., & Harvey, E. S. (2015). Global patterns in the bycatch of sharks and rays. Marine Policy, 54, 86–97. https://doi.org/10.1016/j.marpol.2014.12.017 Pepperell, J. G. (1992). Trends in the distribution, species composition and size of sharks caught by gamefish anglers off south-eastern Australia, 1961-90. Marine and Freshwater Research, 43(1), 213-225. Pratt Jr., H. L., & Casey, J. G. (1983). Age and Growth of the Shortfin Mako, Isurus oxyrinchus, Using Four Methods. Canadian Journal of Fisheries and Aquatic Sciences, 40(11), 1944–1957. https://doi.org/10.1139/f83-224 Preti, A., Soykan, C. U., Dewar, H., Wells, R. J. D., Spear, N., & Kohin, S. (2012). Comparative feeding ecology of shortfin mako, blue and thresher sharks in the California Current. Environmental Biology of Fishes, 95(1), 127–146. https://doi.org/10.1007/s10641-012-9980-x Queiroz, N., Humphries, N. E., Mucientes, G., Hammerschlag, N., Lima, F. P., Scales, K. L., Miller, P. I., Sousa, L. L., Seabra, R., & Sims, D. W. (2016). Ocean-wide tracking of pelagic sharks reveals extent of overlap with longline fishing hotspots. Proceedings of the National Academy of Sciences, 113(6), 1582–1587. https://doi.org/10.1073/pnas.1510090113

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Ramírez-Macías, D., Queiroz, N., Pierce, S. J., Humphries, N. E., Sims, D. W., & Brunnschweiler, J. M. (2017). Oceanic adults, coastal juveniles: Tracking the habitat use of whale sharks off the Pacific coast of Mexico. PeerJ, 5, e3271. https://doi.org/10.7717/peerj.3271 Ribot-Carballal, M. C., Galván-Magaña, F., & Quiñónez-Velázquez, C. (2005). Age and growth of the shortfin mako shark, Isurus oxyrinchus, from the western coast of Baja California Sur, Mexico. Fisheries Research, 76(1), 14–21. https://doi.org/10.1016/j.fishres.2005.05.004 Rigby, C. L., Barreto, R., Carlson, J., Fernando, D., Fordham, S., Francis, M. P., Jabado, R. W., Liu, K. M., Marshall, A., Pacoureau, N., Romanov, E., Sherley, R. B., & Winker, H. (2019). Isurus oxyrinchus. International Union for Conservation of Nature. https://doi.org/10.2305/IUCN.UK.2019-1.RLTS.T39341A2903170.en Rogers, P. J., Huveneers, C., Page, B., Goldsworthy, S. D., Coyne, M., Lowther, A. D., Mitchell, J. G., & Seuront, L. (2015). Living on the continental shelf edge: Habitat use of juvenile shortfin makos Isurus oxyrinchus in the Great Australian Bight, southern Australia. Fisheries Oceanography, 24(3), 205–218. https://doi.org/10.1111/fog.12103 Runcie, R., Holts, D., Wraith, J., Xu, Y., Ramon, D., Rasmussen, R., & Kohin, S. (2016). A fishery-independent survey of juvenile shortfin mako (Isurus oxyrinchus) and blue (Prionace glauca) sharks in the Southern California Bight, 1994–2013. Fisheries Research, 183, 233–243. https://doi.org/10.1016/j.fishres.2016.06.010 Schrey, A. W., & Heist, E. J. (2003). Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Canadian Journal of Fisheries and Aquatic Sciences, 60(6), 670–675. https://doi.org/10.1139/f03-064 Sepulveda, C. A., Kohin, S., Chan, C., Vetter, R., & Graham, J. B. (2004). Movement patterns, depth preferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrinchus, in the Southern California Bight. Marine Biology, 145(1). https://doi.org/10.1007/s00227-004-1356-0 Stevens, J. D. (1983). Observations on Reproduction in the Shortfin Mako Isurus oxyrinchus. Copeia, 1983(1), 126. https://doi.org/10.2307/1444706 Status of the U.S. west coast fisheries for highly migratory species through 2019 (2020). Pacific fishery management council. https://www.pcouncil.org/documents/2020/02/status-of-the-u-s-west-coast-fisheries-for- highly-migratory-species-through-2019-stock-assessment-and-fishery-evaluation.pdf/

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Stillwell, C. E., & Kohler, N. E. (1982). Food, Feeding Habits, and Estimates of Daily Ration of the Shortfin Mako (Isurus oxyrinchus) in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences, 39(3), 407–414. https://doi.org/10.1139/f82- 058 Vaudo, J. J., Byrne, M. E., Wetherbee, B. M., Harvey, G. M., & Shivji, M. S. (2017). Long- term satellite tracking reveals region-specific movements of a large pelagic predator, the shortfin mako shark, in the western North Atlantic Ocean. Journal of Applied Ecology, 54(6), 1765–1775. https://doi.org/10.1111/1365-2664.12852 Weng, K. C. (2005). Satellite Tagging and Cardiac Physiology Reveal Niche Expansion in Salmon Sharks. Science, 310(5745), 104–106. https://doi.org/10.1126/science.1114616 Wilson, S. G., Lutcavage, M. E., Brill, R. W., Genovese, M. P., Cooper, A. B., & Everly, A. W. (2005). Movements of bluefin tuna (Thunnus thynnus) in the northwestern Atlantic Ocean recorded by pop-up satellite archival tags. Marine Biology, 146(2), 409–423. https://doi.org/10.1007/s00227-004-1445-0 Wilson, S. G., Stewart, B. S., Polovina, J. J., Meekan, M. G., Stevens, J. D., & Galuardi, B. (2007). Accuracy and precision of archival tag data: A multiple-tagging study conducted on a whale shark (Rhincodon typus) in the Indian Ocean. Fisheries Oceanography, 16(6), 547–554. https://doi.org/10.1111/j.1365-2419.2007.00450.x

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Chapter two: Horizontal habitat use of the Shortfin Mako shark in the Atlantic Ocean

2.1 Abstract The shortfin mako, Isurus oxyrinchus, is a commonly pelagic shark caught as target and by-catch by commercial longline fisheries in the Atlantic Ocean, since this species has huge commercial value. From 2009 to 2018, scientific observers recovered by-catch data regarding the species length, sex and catch per unit of effort (CPUE) by Spanish longline vessels throughout the Atlantic Ocean, encompassing 12.940.249 kg of shortfin mako sharks in 1826 fishing days. The results from this study confirmed the extensive geographic distribution of the shortfin mako. In this study are described three trans- Atlantic movements in the North Atlantic Ocean which might suggest the existence of two shortfin mako population stocks in that region. Seasonal horizontal movements were also found with mako sharks moving to lower latitudes and oceanic waters in colder months and moving to upper latitudes and into the continental shelf in warmer months. High site fidelity is also displayed in the research. The mako lengths ranged from 125 to 255 cm FL, where smaller individuals occurred in inshore waters and bigger individuals were found in offshore waters and the sex ratio results exposed more females than males, with 1.3 females per male. In the North Atlantic, higher CPUE were found in inshore waters and for the South Atlantic, both inshore and offshore regions had high CPUE for the shortfin mako shark. In addition, significant yearly, seasonal, and regional differences in the CPUE were found with an increasing trend in the mean CPUE for the South Atlantic Ocean since 2016. This research contributes with a better understanding of the horizontal distribution and population dynamic of the shortfin mako shark in the Atlantic Ocean and can be useful tools to practice informed management and conservation decisions for the species.

2.2 Introduction Shortfin mako, Isurus oxyrinchus, inhabits temperate to warm waters within extensive geographic regions, between 50º N and 50º S, reaching 60º N in North-eastern Atlantic (Compagno, 2001; Abascal et al., 2011). Despite the fact that this species is mainly oceanic, occurring in offshore waters, it can explore inshore waters where the continental shelves that are more compressed to the surface (Compagno, 2001). Comparatively to other pelagic species, shortfin mako is a frequent by-catch species in longline fisheries targeting commercial species, representing a persistent harvest in North Atlantic Ocean (Holts et al., 1998; Campana et al., 2015). The shortfin mako

FCUP 35 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean harvest is not and “accidental” by-catch, indeed, the fishery strategies aim to magnify shark catches (Gilman, 2007). This species has huge commercial appeal forasmuch as the fins are used for shark fin soup and the meat can be consumed fresh, frozen, smoked, and dried salted, in addition, the oils, skin and teeth are also used for various applications from vitamins to make embellishments (Compagno, 2001). Notwithstanding being a frequent captured species, the information regarding population structure is very limited. The International Commission for the Conservation of Atlantic Tunas (ICCAT) is an intergovernmental organization answerable for conservation and management of tunas and tuna-like species, such as, pelagic elasmobranchs, including I. oxyrinchus in the Atlantic Ocean waters and adjoining seas. In order to protect shortfin makos, ICCAT took on various actions, just as, a stronger ban on shark finning and annihilate possible loopholes that may exist (finning is the process in which shark’s fins are cut aboard vessels, rejecting the carcass into the sea); a binding measure with the goal to promote the releasing of live shortfin makos in North Atlantic. The 2019 ICCAT report, states that stablishing a catch threshold for shortfin makos is not possible since, regardless of total allowable catch (TAC), even a TAC of 0 t, the shortfin mako stock will maintain a decline until 2035, until a biomass growth can occur. Yet, with a TAC of 0 t, by 2045, the species stock has a 53% probability of rebuilding without overfishing, making shortfin mako stock one of the most problematic. Additionally, both ICCAT and The International Union for the Conservation of Nature (IUCN) recognizes that further research is needed to describe probable spawning areas and regions where there is high density and interactions of shortfin mako in North Atlantic. In order to achieve this, efforts have to be made for proper data collection, like, total catch and dead discard estimations, limits on shortfin mako catches established by scientists, development of release protocols and estimation of CPUEs to assess future stock status. In 2010, in an Ecological Risk Assessment for sharks, the authors concluded that shortfin mako is particularly vulnerable to harvest in the ICCAT Convention Area, mostly due to low reproductive ability and high harvest of juveniles (Matsushita & Matsunaga, 2002; Cortés et al., 2010). Even though the future of shortfin makos in highly uncertain, calculations illustrate that there is a lag time of 20 years between the implementation of management and conservation measures and the rebuilding of the stock, as a result of the species biology characteristics (SCRS, 2019). Due to the shortfin mako life history traits, like low productivity of offspring and late age at sexual maturity, an overfishing state as target or by-catch fisheries, an overexploitation, and a global median decline in population of 46.6%, led the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species to classify the shortfin mako as globally “Endangered” in 2019 and

FCUP 36 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean recommended shortfin mako landings to be banned for as long as this species is considered “Endangered” (Rigby et al., 2019). In order to progress and improve the conservation and management plan of action, is essential to investigate the spatial and temporal fluctuations and the population dynamics of marine organisms. This concedes to comprehend how the shortfin mako is distributed and forecast the impacts that may arise from fishing this predator, with several studies reporting acute declines in shortfin mako population, with the North Atlantic stock having 90% probability of being in an overfishing state (Babcock & Nakano, 2008; Matsushita & Matsunaga, 2002; SCRS, 2019). Nevertheless, these findings may be not represent the rigorous population stock, since the data is impaired, either by omission of mortality of individuals caught and discarded or failing in reporting by-catch quantities, leading to faulty shortfin mako population assessments.

The main goal of the present study is to contribute with information relative to distribution patterns of shortfin mako sharks and hopefully, provide answers where previous information was lacking for the species above-mentioned, in the North Atlantic Ocean. Toward the achievement of that goal, between 2008 and 2018 observer fishery data was collected in the North Atlantic Ocean and a total of 41 shortfin mako shark were tracked through satellite telemetry and analysed. In more detail, in this investigation, research was made regarding the catch per unit of effort (CPUE) from a Spanish pelagic longline vessel, temporal patterns of the CPUE, sex ratio distribution and size distribution of shortfin mako in longline fisheries in the North Atlantic Ocean.

2.3 Material and Methods The data in this study was acquired over the Atlantic Ocean with a total of 41 shortfin mako sharks tagged via satellite telemetry, between 2008 and 2018. From the total sample, 24 individuals were tagged with ARGOS PTTs and 17 specimens were tagged with PSAT. The tagging was performed aboard of pelagic longline fishery fleets, during commercial harvestings. The shortfin mako sharks were caught with the employment of baited longlines and placed upright, perpendicular to the boat. The ARGOS tags were set in the first dorsal fin with stainless steel bolts, neoprene, steel washers and steel screw-lock nuts (Queiroz et al., 2016).

For all individuals captured, scientific observers recovered data regarding fork length (FL), sex, capture coordinates (latitude and longitude) and date (Appendix A). Information regarding size and sex ratio was available between 2008 and 2017, however, there is no size and sex data from the year 2012. Catch and effort data of the Spanish

FCUP 37 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean longline vessels was possible from 2013 to 2018. In that period, the information retrieved resulted in a total effort of 1826 fishing days and 12.940.249 kg of shortfin mako sharks.

Concerning ARGOS PPTs position estimation, outlier locations detected through a 3 m s-1 speed filter and failed attempts to obtain a position, were removed from the dataset. Lastly, a daily time-series for both ARGOS and PSAT locations was estimated applying a continuous-time correlated random walk (CTCRW) Kalman filter (Jonsen et al., 2005). The position estimation of the PSAT tags was checked through a software supplied by the manufacturer, Wildlife Computers, WC-GPE: Global Position Estimator Program Suite software, where the longitude assessment was based on the local time of midnight or mid-day, per daily maximal rate of change in light intensity, whereas latitude was established over day-length approximate calculations (Wilson et al., 1992) . In addition, position estimations that were contradictory, produced by dive-induced modifications in the predicted timing of dawn and dusk from light curves were removed by the WC-GPE software. An integrated state-space models using the sea surface temperature, unscented Kalman filter with sea-surface temperature (UKFSST) data was performed in order to increase PSAT location estimation quality, and so, recover the most likely tracks (Lam et al., 2008). Still, the final geolocations from Argos and PSAT tags had an associated error of approximately 0.2º and 1º, respectively.

The horizontal movements, the CPUE (kg/effort) = mako catches in kg / number of days fishing and size data were tested for normality using the Anderson-Darling test (Anderson & Darling, 1954), for homogeneity of variances with Levene test (Levene, 1961). Since the data was presented a non-normal distribution, the Kruskal-Wallis non- parametric test was used to evaluate seasonal differences in the latitude, and, for CPUE and size data, two non-parametric statistical tests, Kruskal-Wallis Test and Mann- Whitney U Test, were performed to scrutinize yearly, seasonal, and regional differences. Regional differences in sex distribution was studied through the Pearson's Chi-squared proportion test. For all statistical analyses, the significant p-value was settled in p-value = 0.05.

For CPUE, the regions were divided as North Atlantic, between 0º and 50º N, and South Atlantic, between 0º and 43º S, proximately. For size and sex information, since there is only data in North Atlantic, the regions were divided in East, between 20º W and 43º W, and West, between 44º W and 80º W North-Atlantic, using the Mid-Atlantic Ridge as reference. As regards seasonal differences, seasons were grouped as it follows: Winter, from December to February; Spring, from March to May; Summer, from June to August and, finally, Autumn, from September to November (Lea et al., 2015).

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The CPUE, sex and size distributions were geographically displayed by 1º x 1º cell size of latitude and longitude, doing a sum of the values from each point belonging within each cell size for CPUE and sex data, using the ArcGIS Desktop 10.6.1. The plots for statistical comparisons were created using Excel.

All statistical analyses in this work were carried out with the R Project for Statistical version 1.2.5001 (RStudio Team, 2020) and the packages used were “nortest” (Gross & Ligges, 2015) , “car” (Fox & Weisberg, 2019), “crawl” (Johnson et al., 2008; Johnson et al., 2016).

FCUP 39 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

2.4 Results Horizontal Movements The movement data of the specimens tagged occurred in the North Atlantic Ocean between 12º N and 50º N, approximately (Figure 2.1), with average daily distance travelled between 7.36 km/day and 116.68 km/day. In the western North Atlantic, most shortfin mako specimens tagged locations occur in inshore waters, specifically, in the Newfoundland Basin and Cape Hatteras. In the eastern North Atlantic region, tagged locations concentrate in the ashore area of the Cape Verde Basin. Here are also recorded three trans-Atlantic movements, from the specimens 78680, 96030 and 107089.

Figure 2.1 – Trajectories made by the shortfin mako, Isurus oxyrinchus, tracked with PSAT and SPOT tags for this study and respective tag ID’s, between 2009 and 2017. White triangles represent tagging locations and black pentagons represent final locations.

Length Distribution In order to access size distribution, the data used was from 41 shortfin mako sharks caught at latitude intervals roughly bounded by 9º N to 45º N (Figure 2.2). The average size of the individuals was 176 cm FL, fluctuating from 125 cm FL, the smallest specimen, to the largest individual with 255 cm FL. Smaller specimens are found in regions closer to the shore, in shallow waters. In opposition, individuals bigger in size

FCUP 40 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

occur in offshore waters, specially, near the Mid-Atlantic Ridge. Curiously, the trans- atlantic 78680, 96030 and 107089 specimens tracked in this study had, in size, 175 cm, 130 cm and 220 cm FL, respectively.

Figure 2.2 - Length distribution (cm FL) and location of the 41 shortfin makos, Isurus oxyrinchus, used for this study from 2009 to 2017. Lighter circles represent smaller sizes and darker circles correspond to bigger sizes.

Sex Distribution Sex data distribution was based in 41 shortfin mako speciemens caught in the geographic area within 9º N to 45º N (Figure 2.3). From the total specimens in the data, 23 were females and 18 were males, corresponding to 56,9% and 43,1%, respectively, with a proportion of 1.3 females for one male. Surprisingly, all trans-atlantic individuals were females. Both females and males are present in inshore and offshore waters, homogeneously. However, it appears that in the continental shelf and slope regions north of Hatteras Plain (40º N) and near Cape Verde (20º W-30º W), there is a higher incidence of females.

When performing the Pearson's Chi-squared test between East and West, the result was non significant (X-squared = 0.43843, df = 1, p-value > 0.05).

FCUP 41 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Figure 2.3 – Sex distribution of the shortfin mako, Isurus oxyrinchus, recorded in 1º x 1º grids, caught between 2009 and 2017.

FCUP 42 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

CPUE Distribution The catch effort data of 5 years from Spanish longline fleets record occurred all over de Atlantic Ocean, from 43º S to 51º N, loosely (Figure 2.4). Throughout the Atlantic Ocean, the CPUE unveil to be somewhat heterogeneous. It is possible to distinguish three clear regions where the impact of Spanish longline vessels was more pronounced, specifically, in the North Atlantic, between 35º N and 45º N, in the Newfoundland Basin, and another region, between 15º N and 20º N around Cape Verde Islands. In the South Atlantic there is a larger area, between 20º S and 43º S, that expands from the East coast of South Africa to the South-West coast of South America. Interesting to note that in the North Atlantic, CPUE values seem to be higher in inshore waters, whereas in South Atlantic, the fishing effort occurs both in inshore and offshore waters. It is important to take into consideration that only about 1% of all catches corresponded to zero kilos caught of shortfin mako shark.

Figure 2.4 – Spatial distribution of the catch per unit of effort in number of Kg caught of shortfin mako, Isurus oxyrinchus, in the Atlantic Ocean from the Spanish longline fleet between 2013 and 2018.

FCUP 43 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Seasonal differences in the horizontal movements The seasonal data had a non-normal distribution, according to the Anderson- Darling test for normality (A = 262.99, p-value < 0.05). The results of the Levene test for homogeneity of variances revealed that the data was heterogeneous between seasons (Df = 3, F value = 434.66, p-value < 0.05). To detect seasonal differences in the shortfin mako horizontal movements, the Kruskal-Wallis non-parametric test was applied and exhibited seasonal differences in latitude and longitude (Kruskal-Wallis chi-squared = 1080.1, df = 3, p-value < 0.05).

Evaluating figure 2.5, the horizontal movements in Winter and Autumn display a scattered shortfin mako horizontal movement, however there is greater concentration of individuals West of the Gulf Stream, north of Cape Hatteras and in the Cape Verde Islands in Winter months. In Autumn there is a higher occupation of shortfin mako in the Newfoundland Basin and the region between Cape Hatteras and Georges Bank. Nonetheless, it appears that in both Winter and Autumn seasons, the shortfin mako swims to offshore waters and south of the North Atlantic. In the Spring, there is a period where there shortfin mako are in offshore waters, along the Mid-Atlantic Ridge and south of the Cape Verde Basin and another period where the species moves to the continental shelf, in the Gulf Stream, between Cape Hatteras and Georges Bank in West North Atlantic and into the Cape Verde Islands shelf in eastern North Atlantic. Finally, in the Summer, practically there was no movement in East North Atlantic and in the West North Atlantic, shortfin mako move into inshore waters between Cape Hatteras and Georges Bank and into offshore to the Gulf Stream, bounded by the Newfoundland Basin and the Mid-Atlantic Ridge. Mind that the trans-Atlantic movements occur mainly in the Winter and Autumn.

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Figure 2.5 – Seasonal movements of the shortfin mako, Isurus oxyrinchus, tracked in this study between 2009 and 2017. Blue circles correspond to Winter; green circles correspond to Spring; yellow circles correspond to Summer and orange circles correspond to Autumn.

Regional differences in Length The Anderson-Darling test for normality showed that size information was not normally distributed (A = 0.75197, p-value < 0.05). Regarding homogeneity of variances, the Levene test was homogenous between years (Df = 7, F value = 2.0261, p-value > 0.05), seasons (Df = 3, F value = 0.0324, p-value > 0.05) and regions (Df = 1, F value = 0.2644, p-value > 0.05). Using two non-parametric tests, yearly (Kruskal-Wallis chi- squared = 13.454, df = 7, p-value > 0.05), seasonal (Kruskal-Wallis chi-squared = 3.03, df = 3, p-value > 0.05) and regional (Mann-Whitney U test W = 1681, p-value < 0.05) tendencies were studied and only regional differences were found.

Analysing figure 2.6 all individuals caught in the Eastern North Atlantic were bigger than the specimens in the Western North Atlantic, with an average size for the East of 183 cm FL and for the West of 168 cm FL.

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)

cm FL cm (

Figure 2.6 – Differences in size distribution (cm FL) of shortfin mako, Isurus oxyrinchus, caught between 2009 and 2017 in Eastern North Atlantic and Western North Atlantic. Seasonal differences in sex ratio The Anderson-Darling normality test showed a non-normal distributed sex data (A = 7.3489, p-value < 0.05). Regarding homogeneity of variances, the data was homogenous between seasons (Df = 3, F value = 1.8865, p-value > 0.05). The Kruskal- Wallis non-parametric test revealed significant seasonal differences between gender (W = 340, p-value > 0.05).

The Winter was the season with the highest ratio between females and males, with 2.5 females for one male (Figure 2.7). Next, the Summer months had 1.2 females per male and Spring and Autumn had a 1:1 ratio.

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Figure 2.7 – Differences in the number of female and male specimens of shortfin mako, Isurus oxyrinchus, in each season, Winter, Spring, Summer and Autumn. Pink bars represent females and blue bars represent males.

Yearly, seasonal, and regional differences in CPUE The results from the Anderson-Darling normality test concluded that the CPUE data was not normally distributed (A = 655.63, p-value < 0.05). Using the Levene test for homogeneity of variances, there was homogeneity between seasons (Df = 3, F value = 1.048, p-value > 0.05) but heterogeneity between years (Df = 2, F value = 5.81, p-value < 0.05) and between regions (Df = 1, F value = 143.21, p-value < 0.05). Applying the Kruskal-Wallis and Mann-Whitney U non-parametric tests, yearly (Kruskal-Wallis chi- squared = 18.372, df = 5, p-value < 0.05), seasonal (Kruskal-Wallis chi-squared = 8.7155, df = 3, p-value < 0.05) and regional (Mann-Whitney U test W = 63464130, p- value < 0.05) tendencies were investigated and significant differences were found in all three.

Throughout the years, it is possible to discern fluctuations in the mean CPUE for both North Atlantic and South Atlantic (Figure 2.8). Notwithstanding, the mean CPUEs for South Atlantic were much bigger when comparing to the North Atlantic where the values are well below, yearly and globally, with an increase trend in the CPUE since 2016 in South Atlantic.

FCUP 47 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

Figure 2.8 – Yearly distribution of the mean CPUE (Kg/Effort) of shortfin mako, Isurus oxyrinchus, in North Atlantic and South Atlantic, between 2013 and 2018. The error bars are also represented.

It is also apparent that CPUE is dependent of seasons (Figure 2.9). In North Atlantic the mean CPUE values were maximum in Spring and from that, tend to decrease whereas, in South Atlantic, the CPUE peak occurs in Autumn and presents the lower value in Spring.

Figure 2.9 – Seasonal distribution of the mean CPUE (Kg/Effort) of shortfin mako, Isurus oxyrinchus, in North Atlantic and South Atlantic, between 2013 and 2018. The error bars are also represented.

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2.5 Discussion Shortfin mako population stocks are suffering a worldwide decline, with by-catch and target species fisheries representing the predominant procedures of harvest for oceanic elasmobranchs (Dulvy et al., 2008). Hence, providing knowledge regarding the shortfin mako is of great importance for this endangered species in order to better create sustainable conservation and management measures for this apex-predator. In this study, it was investigated the distribution and the population condition of the shortfin mako in space and time in the Atlantic Ocean, more accurately, the present study focused on the size and sex distribution when caught and the catch per unit of effort (CPUE). The data used was retrieved from the Spanish longline fleet in the Atlantic Ocean, from 2009 to 2018. Furthermore, when possible, yearly, seasonal, and regional differences were also performed. The Spanish longline fishery vessels harvest in an extensive range, from the Mediterranean Sea, Indian Ocean, Pacific Ocean, and Atlantic Ocean (García-Córtes & Mejuto, 2002; Megalofonou et al., 2005; Mejuto et al., 2013). In the Atlantic Ocean, the Spanish fleet displays intense fishing effort in South Atlantic, Cape Verde Islands and Northwest Atlantic. The distribution of the Spanish longline vessels corresponds to the swordfish distribution, which is the commercial target species. Pelagic sharks consist of 70% of the European Union (EU) harvest in the Atlantic Ocean, whereas, of these, 10% are shortfin mako, Isurus oxyrinchus (Fowler et al., 2010). In addition, Spain longline fisheries is 1 of the 10 pelagic fishing countries, being this country the main importer of shark meat for the EU since 2000, representing 43% of all the shark meat imports (Fowler et al., 2010).

The shortfin mako specimens tagged in this study, travelled great distances in the North Atlantic Ocean, extending to 116.68 km per day and it is considered a species with a worldwide geographic distribution, inhabiting tropical to temperate latitudes (Compagno, 2001). Notwithstanding, trans-Atlantic movements are not commonly reported. Here, we report three trans-Atlantic movements that occurred from the western to eastern North Atlantic. All three shortfin mako individuals were juvenile females, however, since our data did not provide any trans-Atlantic adult female migration, it is not possible to make assumptions regarding trans-Atlantic movements and the maturity stage. To our knowledge, only another trans-Atlantic movement was described for a single shortfin mako (Casey & Kohler, 1992). This suggests that shortfin mako movements across the Mid-Atlantic Ridge may not be common as for other species, such as, the Atlantic Bluefin Tuna, Thunnus thynnus (Block, 2001) or blue sharks, Prionace glauca (Casey, 1985). Despite these results might indicate the existence of two shortfin mako stocks in North Atlantic Ocean, it is premature to accept the existence of two

FCUP 49 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean separate population stocks. A genetic population structure study by (Heist et al., 1996) merged the genetic samples of the western North Atlantic and central North Atlantic, in the Azores region due to no statistical differences resulting in the conclusion that the North Atlantic Ocean is a single stock. Per contra, another study also in the Azores area characterized specimens of shortfin mako with having peculiar pigmentation patterning and proposed that those mako sharks were distinctive and endemic to the region (Moreno & Morón, 1992). Further research is urgently needed to acknowledge or refuse the two-population stock for the shortfin mako in the North Atlantic since this can have huge implications in conservation and management of the species.

The mako shark displayed a wide geographical range of horizontal movements in Autumn and Winter months and along the four seasons used, at different extents, both continental shelves, offshore waters, and slope regions. In the North Atlantic Ocean, this species appears to follow the previous described seasonal North-South migration where the specimens move to lower latitudes and offshore waters in colder months and in the warmer months of Summer and Spring migrate to upper latitudes and to the continental shelf and inshore regions (Casey & Kohler, 1992). Regardless of seasonal migration, there is, to some extent, a constant presence of mako sharks in the Continental shelf and slope regions from North Carolina to New York states and in the Newfoundland Basin in the eastern Atlantic and in the Cape Verde Islands in the western Atlantic. The above-mentioned regions meet important ocean currents, namely, the Gulf Current and Labrador Current in the north-eastern Atlantic and the Atlantic North-eastern Tropical Upwelling System. The Gulf Stream, particularly, in continental shelf areas and inshore waters, and the Atlantic North-eastern Tropical Upwelling System are regions in the North Atlantic Ocean, with major upwelling activity, shelf-edge fronts or tidal thermal fronts (Sims et al., 2000; Sims et al., 2003; McGregor et al., 2007). The intersection between the Labrador Current and the Gulf Stream presents sharp oceanographic differences, with the interaction of warm and cold waters from the Gulf Stream and Labrador Current, respectively (Vinogradov et al., 1998). As a result, such regions are remarkably productive, favouring the development of phytoplankton and zooplankton biomass (Casey & Kohler, 1992; Vinogradov et al., 1998; Ndour et al., 2018). Consequently, these areas represent important feeding grounds for most fish and large pelagic predators, just as the shortfin mako in the North Atlantic. The Shortfin mako shark preys on teleosts and cephalopods in the North Atlantic, where occurs seasonal availability of both groups during warmer months (Stillwell & Kohler, 1982; Maia et al., 2006). All this evidence suggests that shortfin mako might have high degree site fidelity to highly productive regions all through the year.

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The size distribution of the individuals caught varied from 125 cm to 255 cm FL and all females were juveniles and only five males were considered mature according to the length at maturity for the North Atlantic (Mollet et al., 2000; Campana et al., 2005). Moreover, smaller shortfin mako occur near to the inshore areas, whereas larger specimens were found in offshore waters. The smallest specimens occur, mostly, in the inshore waters of the Newfoundland Basin. When analysing the size differences between eastern and western North Atlantic, all individuals in the East were bigger than in the West. A congruent trend was observed for another investigations, one with Spanish longline vessels which also concluded that shortfin mako individuals in the eastern North Atlantic are bigger in length than in the north-western Atlantic and smallest range of mako sharks are found in the continental shelf near Newfoundland Basin (Mejuto, 1985; Mejuto & Iglesias, 1987; Casey & Kohler, 1992) . The size distribution can be explained by the presence of likely nursery areas where smaller individuals are found, such as, the inshore waters from North Carolina to New York states, Newfoundland Basin and Cape Verde Islands. The literature suggested that the same locations could possibly be nursery areas for the shortfin mako (Matsushita & Matsunaga, 2002) and other species, for instance, the Thresher shark, Alopias vulpinus (Natanson, 2001), Angel shark, Squatina oculate (Capapé et al., 2002) or Cod fish, Gadus morhua (Lear & Wells, 1984). A distinct interpretation for the length distribution could be the fishing gear selectivity (Thorson & Simpfendorfer, 2009). However, taking into account that the gear used by the Spanish longline vessels targeting swordfish reaches low depths (Mejuto et al., 2008) with no probable size constraints, in light of the number of the smaller specimens in the sample study, we can exclude gear selectivity as a as a limiting factor of the individuals caught.

Concerning the sex data in this study, the ratio displayed more abundance of females than males in the North Atlantic Ocean, with 1.3 females per male. Further, Mucientes et al., (2009) found sexual segregation in the shortfin mako, suggesting social aspects during mating periods as a possible explanation. Again, gear selectivity can represent another explanation for the female prevalence due to bait preference, habitat occupancy or other trait. Also, can explain the lack of mature females (Maia et al., 2007). The sex ratio seasonality, with winter having the biggest ratio of 2.5 females per male, could justify migrations due to reproductive behaviour (Maia et al., 2007).

In this research, the catch per unit of effort distribution varied between 40º S to 50º N, approximately. This acknowledged the species large-scale distribution in the Atlantic Ocean (Compagno, 1984; Abascal et al., 2011). In the North Atlantic Ocean,

FCUP 51 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean higher CPUE values befall in the seaward limit of Newfoundland Basin and in the inshore waters of Cape Verde Islands. In the South Atlantic Ocean, both in inshore and open- ocean waters, from the East coast of South Africa to the South-West coast of South America, are relevant regions with high CPUE for the shortfin mako shark. Inshore waters, frontal areas with increased productivity and islands are regions that tend to attract and agglomerate different pelagic shark species, and shortfin mako sharks are likely using these locations as nursery areas, feeding or protection grounds (Casey & Kohler, 1992; Holts & Bedford, 1993; Cartamil et al., 2010; Queiroz et al., 2012; Bustamante & Bennett, 2013; Queiroz et al., 2019). Therefore, it is feasible that the CPUE distribution is correlated with the habitat preferences of the mako shark. In addition, fishers take advantage of these preferred regions to increase their catches of this species, with the shortfin mako presenting greater risk in the North Atlantic Ocean (Queiroz et al., 2019). It is also important to note that an ecological risk assessment study concluded that the shortfin mako was among highly vulnerable pelagic sharks (Cortés et al., 2010) and the fact that the CPUE data present in this investigation had 1% of zero catches, corroborates the previous assessment. Furthermore, significant yearly, seasonal, and regional differences were found, with an increasing trend in the mean CPUE for the South Atlantic Ocean since 2016, concordant with the SCRS (2019) report that stated increased tendencies in the South Atlantic since 2008. In the same report, it is declared that the shortfin mako population growth rate in the North Atlantic Ocean is half of what was thought in previous assessments, indicating that this species is declining abruptly in that region, unanimous with other studies that suggest a decline of the shortfin mako population in the Atlantic Ocean (Baum, 2003; Babcock & Nakano, 2008; Barreto et al., 2016).

Nonetheless, this study presents limitations, mainly, the specific fishery-data since multiple variables can influence the conclusions obtained. Among those variables are gear selectivity or gear saturation, area coverage by the vessels, effectiveness of the fleet, environmental conditions, and the targeting species structure (Maunder et al., 2006). The data provided in this study was retrieved from North and South Atlantic Ocean by Spanish pelagic longline vessels targeting swordfish. Thus, the results displayed are hopefully to contribute with a clearer picture regarding the shortfin mako shark population in the areas where it is most present and more vulnerable of catch by longliners. It is necessary to acknowledge the likelihood that the Isurus oxyrinchus can occur in areas not included in the study.

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Although performance was not optimal due to fishery dependent data limitations, we nevertheless believe that the knowledge acquired in this research can provide useful tools to better understand the spatial distribution and population dynamic of the shortfin mako shark in the Atlantic Ocean in order to practice enlightened management and conservation decisions for the species, realizing that further research is needed, since there are a lot of gaps regarding the biology of this important predator.

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Mollet, H. F., Cliff, G., Pratt Jr, H. L., & Stevens, J. (2000). Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin, (2).

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Chapter three: Vertical habitat use of the Shortfin mako shark in North Atlantic Ocean

3.1 Abstract The shortfin mako shark, Isurus oxyrinchus, is a pelagic shark with a worldwide geographic distribution that is highly affected by pelagic longline fisheries since it is caught as bycatch by longliners targeting swordfish and tunas. During 1.635 tracking days, from 2008 to 2011 and in 2017, seven shortfin mako sharks were tagged with Pop- up Satellite Archival Tags (PSAT) in the North Atlantic Ocean. There was no clear diel vertical behaviour pattern, with shortfin mako occupying most of its time at surface waters, from 0-70 m, with preferred temperatures between 17º C and 21º C. Deeper dives followed by fast ascends were recorded for smaller individuals. The maximum depth registered was 1888 m and the minimum temperature was 2.2º C. In addition, different habitat utilization was found among different maturity stages, with adults using an expanded range of vertical habitat than juveniles both in day and nighttime. The findings in this study can be employed to create powerful management and conservation measures for the species sustainability and can deliver relevant information for assessments for the shortfin mako shark harvested by longline fisheries in the North Atlantic Ocean.

3.2 Introduction Due to the hasty development of fishing fleets and overexploitation of marine habitats, several pelagic sharks confront significant declines over the past years (Dulvy et al., 2014). Shortfin mako sharks, Isurus oxyrinchus, are fast-swimming and highly migratory fish and occupy both the epipelagic zone and inshore regions of a wide-ranging geographic distribution within tropical and temperate waters (Casey & Kohler, 1992; Compagno, 2001; Loefer et al., 2005). It is one of the most affected species by recreational and longline fisheries, since is caught as by-catch of longline fleets that target commercial valuable species, namely, swordfish and tunas which have analogous distribution patterns to the shortfin mako (Compagno, 1984; Holts et al., 1998; Campana et al., 2015; Oliver et al., 2015; Queiroz et al., 2016). The shortfin mako is an apex- predator in marine habitats and huge ecosystems regulator since occupy high trophic levels in the food webs (Cortes, 1999) regulating the abundance of lower trophic level species (Bascompte et al., 2005; Shepherd & Myers, 2005; Ferretti et al., 2010). Furthermore, due to the species life history traits, such as, slow growth, late maturity and low fecundity (Musick et al., 2000; García et al., 2008) pelagic sharks are vulnerable to

FCUP 61 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean overfishing (Stevens, 2000; Baum, 2003), reinforcing uncertainty about the consequences for the marine ecosystems and sustainability of the species.

Considering the fast rate at which is occurring biodiversity loss, recognizing the risk of species is crucial to settle conservation endeavours and management decisions (Butchart et al., 2010; Hoffmann et al., 2008). The International Union for Conservation of Nature's (IUCN) Red List of Threatened Species is an information source indicator of the global biodiversity status and evaluate the extinction risk (Hoffmann et al., 2008; Mace et al., 2008). In marine habitats, overexploitation is the main factor of biodiversity loss (McClenachan et al., 2012), and the IUCN Red List of Threatened Species is used when deciding the conservation status of marine vertebrates (Dulvy et al., 2014). In 2019, the International Union for Conservation of Nature's assessed the shortfin mako as “Endangered”, with population declines worldwide and abrupt population loss in North and South Atlantic Ocean (Rigby et al., 2019). Seeing that the sustainability of this species is of great concern, the shortfin mako is encompassed by the Convention on Migratory Species (CMS) Memorandum of Understanding for Migratory Sharks that aims to simplify and promote conservation. In 2017, the International Commission for the Conservation of Atlantic Tunas (ICCAT) acknowledged a measure which aimed to increase the number of live individuals that are released through restricting the circumstances at which shortfin mako sharks can be landed. In 2018, Mexico declared its objective to add the shortfin mako to the Appendix II of the Convention on International Trade in Endangered Species (CITES). In the 2019 CITES Conference, the proposal was accepted meaning that the international trade of the predator meat and fins must obey to regulations and permits.

Information regarding the species horizontal, and more relevant, vertical tendencies is of high priority to comprehend the species ecological role and to anticipate the consequences that climate change can bring to the movement and distribution of pelagic sharks (Hays et al., 2016). Furthermore, the movement trends and habitat use pattern knowledge is key create adequate management and conservation decisions and powerful strategies that diminish shortfin mako bycatch that could improve, not only the sustainability of fisheries, but also, the species viable preservation (Mucientes et al., 2009). Therefore, investigating the vertical dynamics of the shortfin mako movement is advantageous to assess depth and temperature preferences and evaluate changes in behaviour at some geographic scale. To accomplish that, Pop-up satellite archival tags (PSAT) have proven to be useful in tracking both horizontal and vertical species movements (Brunnschweiler et al., 2009; Stevens et al., 2010; Saunders et al., 2011),

FCUP 62 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean nonetheless, that information is poor and deficient for pelagic sharks what are experiencing increased fishing pressure globally (Nuno Queiroz et al., 2016).

Prior vertical utilization studies using satellite telemetry of shortfin mako are very limited, but the available research showed that in South Pacific the shortfin mako preferred waters with temperatures ranging between 13.4º C and 24.1º C (Casey & Kohler, 1992; Abascal et al., 2011). In addition, shortfin mako juveniles were found to spend 90% of the time in the mixed layer, with temperatures between 20º C and 21º C, with occasional short-timed dives below the thermocline during daytime periods in western North Atlantic (Holts & Bedford, 1993; Sepulveda et al., 2004).

Given the limited information currently available regarding the vertical use of the shortfin mako and the urgency in such information to assure informed management and conservation decisions for the species conservation, this study aims at evaluating vertical habitat utilization and diel movements of shortfin mako in the North Atlantic Ocean to provide relevant spatial ecology information of this species.

3.3 Materials and Methods In this investigation, 17 PSAT tags were used and the tagging process occurred over commercial fishing on board of pelagic longline vessels. The shortfin mako captured with baited longlines were put in vertical, perpendicular to the vessel. The PSAT tags were secured to a monofilament tether (250 lb test) covered with silicone tubing and looped across a small cavity in the base of the first dorsal fin (Queiroz et al., 2016). The pelagic longliners used J-style hooks and steel leaders, which were cut or removed whenever was possible. Prior to the tagging attachment, the PSAT tags were set to gather information with the duration between 30 and 180 days, that were assuredly tested for ocean water fluctuation. For the tagging procedures, shortfin mako were lifted perpendicular to the vessel. Furthermore, the fork length (FL), tagging latitude and longitude, date and time were registered. The PSAT model used was MiniPAT tags fabricated by Wildlife Computers (WC). Daily and every 6 hours, the tags recorded depth, minimum and maximum temperatures, also, the light levels were detected, establishing sunrise and sunset. The depth range of the MiniPAT is 0 m to 1700 m, with a resolution of 0.5 m ±1% of reading. The temperature range is -40° C to +60° C, with a resolution of 0.05° C ±0.1° C. After pop-up, the MiniPAT tags try to transmit calculations of depth and temperature at 10-minute breaks to assure full description of the time series. If the tag is recaptured, the complete data is retrieved and can be downloaded to a personal computer, which was the case with tag 86408 that was physically recaptured.

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The vertical habitat use of the shortfin mako was studied as the percentage of time-at-depth (TAD) and time-at-temperature (TAT) for both daytime, settled from 06:00 am to 17:59:59 pm and nighttime from 18:00:00 pm to 05:59:59 am. In addition, the vertical distribution was separately evaluated for adults and juveniles shortfin mako individuals. The length at maturity was established according to the literature for the shortfin mako in North Atlantic, that is, male individuals were considered mature at 180 cm FL (Campana et al., 2005) while female specimens were treated as mature at 276 cm FL for females (Mollet et al., 2000). For the time-at-depth were used 17 individuals and the data was combined from 0-5 m; 5-10 m; 10-20 m; 20-30 m; 30-50 m; 50-70 m; 70-100 m. Regarding the time-at-temperature, 13 specimens were used for the analysis and the data was combined in 2º C bins, except the temperature intervals 2º C-5º C and above 25º C. The data bins were averaged throughout all shortfin mako sharks within each category. The TAT and TAD data were tested for normality using the Anderson- Darling test for normality (Anderson & Darling, 1954), for homogeneity of variances with Levene test (Levene, 1961), and since both TAD and TAT present non-normal distributions, the time-at-depth and time-at-temperature were compared between circadian periods (daytime and nighttime) and maturity stages (juveniles and adults). The non-parametric Mann-Whitney U Test was applied to analyse TAD and TAT differences between daytime and nighttime and among adults and juveniles.

For all statistical analyses, the significant p-value was settled in p-value = 0.05. All statistical analyses in the present study were performed using the R Project for Statistical Computing. The plots were created through Excel and R Project for Statistical version 1.2.5001 (RStudio Team, 2020) using the libraries “ggplot2” (Wickham, 2009) and “viridis” (Garnier, 2018).

3.4 Results Seventeen PSAT tags were used in this research, totalling 1.635 tracking days for both males and females, specifically, 784 days for males and 851 days for females. Of all the individuals tracked, nine were males and eight were females (table 3.1).

Table 3.1 – Total number of shortfin mako, Isurus oxyrinchus, individuals, both males and females and maturity stage, juvenile and adult.

Maturity Gender Total Adult Juvenile

Female 0 8 8

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Male 2 7 9

17

Vertical habitat preferences The Anderson-Darling normality test revealed that the time-at-depth (TAD) data was not normally (A = 2.2345, p-value < 0.05) and was homogenous according to the Levene Test (Df = 1, F value = 0.4318, p-value > 0.05). The time-at-temperature (TAT) data presented a non-normal distribution with homogeneity of variances (A = 1.6007, p- value < 0.05; Df = 1, F value = 0.023, p-value > 0.05). Significant day and night time differences were found in both time-at-depth and time-at-temperature with the non- parametric Mann-Whitney's tests (TAD: W = 196, p-value < 0.05; TAT: W = 408, p-value < 0.05).

The shortfin mako vertical movements did not display diel vertical migration. Mako sharks had a relatively homogenous depth distribution in both day and nighttime, however, showing preference to the surface, from 0 m to 10 m and to deeper waters, between 50 m and 70 m. The favoured temperature clearly ranged from 17º C to 21º C during both day and night periods (Figure 3.1).

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Figure 3.1 – Vertical habitat preferences of the shortfin mako, Isurus oxyrinchus, for time-at-depth (m) and time-at-temperature (°C), during daytime and nighttime.

Deeper dives succeed by fast ascends to lower depths were common for smaller specimens. However, larger individuals spent continued days in-depth. The maximum depth reached was 1888 m and the minimum temperature was 2.2º C (Figure 3.2).

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Figure 3.2 – Detailed diving characterization of two shortfin mako sharks, Isurus oxyrinchus, tagged with pop-up satellite archival (PSAT) tags. The top plot, from shark 86407, a juvenile, displays the most common diving pattern movement from smaller specimens. The bottom plot, from shark 86408, an adult, exhibits the rare diving behaviour where the specimens spent several days in depth (m), common for larger specimens.

Shortfin mako adult specimens exhibited a preference for deeper waters when comparing to juveniles, in addition, adults displayed different habitat utilization during daytime and nighttime periods. Accurately, the adults inhabit an expanded range of vertical occupancy than juveniles both in day and nighttime (Figure 3.3). During daylight, the mean depth for adults was 453.95 m and for juveniles was 315.36 m (Mann- Whitney's tests: W = 4007680, p-value < 0.05). At nighttime, the mean depth for adults was 444. 11 m and for juveniles was 289.71 m (Mann-Whitney's tests: W = 13544820, p-value < 0.05). The mean temperature at daytime for adults was 11.98º C while for juveniles was 15.63º C (Mann-Whitney's tests: W = 4080400, p-value < 0.05). During

FCUP 67 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean

nighttime, mean temperature for adults was 12.01º C while for juveniles was 16.06º C (Mann-Whitney's tests: W = 13808656, p-value < 0.05).

Adults Juveniles

Adults Juveniles

Figure 3.3 – Habitat use of the shortfin mako sharks, Isurus oxyrinchus. The data is classified in 6 hours classes and divided by depth (m), temperature (°C) and maturity stage. In the plots are depicted the medians, the 95% confidence interval of the medians, the 75th percentile (Q1), 25th percentile (Q3) and the outliers, in red.

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Time-at-depth and time-at-temperature statistically significant differences were also found among juveniles and adults with the Mann-Whitney's tests (TAD: W = 784, p- value < 0.05; TAT: W = 1632, p-value < 0.05).

The time-at-depth information according to the maturity stage revealed that juveniles presented a more homogenous vertical distribution, spending approximately 16% of the time between 5 m and 10 m and 18% of the total time between 50 m and 70 m during daytime and nighttime. Regarding adults, there is a clear preference for depths closer to the surface, spending 24% of the daily hours and 25% of the night periods between 0 m and 5 m. In addition, the time-at-temperature data unveiled that shortfin mako juveniles spend more time in warmer water temperatures, between 19º C and 21º C, 26% during daytime and 28.5% during nighttime while adults utilize preferably colder waters, spending 28% of the day and 25% of the night in temperatures between 17º C and 19º C (Figure 3.4).

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Figure 3.4 – Habitat preferences of juveniles and adults of shortfin mako, Isurus oxyrinchus, for time-at- depth (m) and time-at-temperature (°C), during daytime and nighttime.

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3.5 Discussion Knowledge in vertical habitat preferences of the shortfin mako is greatly important to establish prosperous conservation action plans and powerful management decisions. The purpose of the present study was to provide detailed information on the vertical habitat use of shortfin mako in the North Atlantic Ocean. In this investigation it was possible to tag juveniles and adult shortfin makos, therefore, it was possible to assess differences in the habitat use of different maturity stages, to our knowledge, for the first time. The vertical data results demonstrated that the shortfin mako occurred mainly at surface waters (0-50 m), above the thermocline and, at temperatures that ranged from 17º C to 21º C. Within that temperature interval, adults showed preference for temperatures between 17º C to 19º C, both in day and nighttime. However, the minimum temperature recorded was 2.2º C. There was no clear diel pattern in vertical behaviour, nonetheless, the mean vertical distribution was deeper in daytime hours, similar to what was previously reported (Casey & Kohler, 1992; Holts & Bedford, 1993; Abascal et al., 2011). Frequently, deeper dives, down to 1888 m, succeed by fast ascends were reported. Sporadically, continued days in-depth behaviour occurred, however, this was a pattern observed only for larger specimens. Carey et al. (1990) reported a large female shortfin mako that spent the majority of the time in depths from 100 m to 400 m. In other studies, deeper dives patterns were proposed to be associated with energy conservation, navigation or foraging behaviour and prey hunting in other pelagic sharks, such as, the white shark, Carcharodon carcharias, blue shark, Prionace glauca, tiger shark, Galeocerdo cuvier, whale shark, Rhincodon typus or the oceanic whitetip, Carcharhinus longimanus (Nasby-Lucas et al., 2009; Queiroz et al., 2010; Nakamura et al., 2011; Brunnschweiler & Sims, 2011; Papastamatiou et al., 2018). Despite both adults and juveniles show predilection for shallow waters, when investigating habitat use of distinct maturity stages, differences were found with juveniles occurring in shallower and warmer waters during daytime and nighttime, comparing to adults that preferred deeper waters during daytime periods. However, deeper distributions during daytime were found at both maturity stages, these results being corroborated by other investigations (Sepulveda et al., 2004; Loefer et al., 2005). These results reflect the impact that both juveniles and adults might suffer by the longline fishing vessels, with juveniles likely being the most affected. In a study analysing the overlap between the species occurrence and the longliners presence, Queiroz et al. (2016) found that approximately 80% of the time that shortfin mako were tracked, this species overlapped with both Portuguese and Spanish longline fishing vessels. In

FCUP 71 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean addition, the overlap coincided with regions of intense fishing effort and with shortfin mako hotspots. In the 2019 CITES conference, the acceptance of the proposal to regulate the international trade of the shortfin mako meat and fins will motivate the countries fishing management organisations to undertake in conservation actions of shortfin mako caught as both target and bycatch fisheries. However, the success of the conservation actions employment is dependent of each country commitments to work locally facing conservation. The IUCN recommends that, in order to grant the species a chance for recovery, that all landings must be prohibited while the species conservation status is defined as “Endangered” (Rigby et al., 2019). Also, quality scientific catch and discard data based on scientific procedures is critically required, as well, implementation of international conservation regulations.

It must be acknowledged that geolocation estimations present restraints given that are calculated from the light-level irradiance that can be affected by natural atmospheric conditions or the animal behaviour, for instances, pelagic sharks can spend a portion of the day at considerable depths where the habitat light can be close to the threshold of the tag perceptiveness, making it difficult to assess the time as day or night (Musyl et al., 2003; Nielsen et al., 2006). Nonetheless, the preference of the shortfin mako for surface waters at sunset and sunrise concedes a degree of confidence regarding the data used in this investigation. In summary, our research showed that the shortfin mako did not demonstrate diel cyclicity, using most of the time surface waters in the North Atlantic Ocean. Despite that, it was possible to find differences in the vertical habitat use for juveniles and adults, with juveniles spending more time in shallower and warmer waters than adults. This can indicate that juveniles of shortfin mako might be more susceptible to being caught by longline fisheries. Hence, it is critical to embrace conservation and management decisions so the results can be powerful and efficient in the protecting and assuring the species sustainability. To achieve this, further research on the shortfin mako is needed, specially, understanding the species hotspots and nursery areas, primarily, to juveniles. We hope that the findings in this investigation represent an improvement to the existing comprehension on the vertical habitat use of the shortfin mako shark. Even though the sample size, specially, in adults was lacking to deliver comprehensive results, the conclusions in the present study can be used to implement sustainable conservation and management measures to decrease shortfin mako bycatch and can provide useful tools for assessing the species conservation status in the Atlantic Ocean.

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Chapter four: Closing examination

The purpose of the present dissertation was to address shortcomings in knowledge of the shortfin mako shark distribution tendencies and habitat preferences in the Atlantic Ocean. In order to achieve the objective, fishery observer data was investigated. With the catch and effort data was possible to determine catch-per-unit effort (CPUE) and with the biological information, such as size and sex, it was attainable to understand wide-ranging distribution trends. In addition, depth and temperature data was used to analyse the vertical distribution patterns and acknowledge depth and temperature preferred habitats.

The results we obtained verified the extensive distribution and migratory patterns of the shortfin mako in the Atlantic Ocean. In this study we also describe one of the few trans-Atlantic movements reported, to the present date, in the North Atlantic, with all trans-Atlantic specimens being females and the movements occurring from western to eastern North Atlantic. Our results might demonstrate the presence of two shortfin mako stocks in North Atlantic Ocean, nonetheless, additional research is needed to either confirm or refute the two-population stock hypothesis, considering the implications that this information can have in conservation and management decisions. Even though shortfin mako sharks occupy continental shelves, offshore waters, and slope regions, seasonal migration was also present in our results, with specimens moving to lower latitudes and offshore waters in colder months and migrating to upper latitudes and to the continental shelf and inshore regions in warmer months. In addition, disregarding seasonality, there was a loyalty of mako sharks to the continental shelf and slope regions from North Carolina to New York states; to the Newfoundland Basin and to the Cape Verde Islands, suggesting high fidelity to productive areas. The size distribution of the individuals in this study divulged that smaller shortfin mako occur near to the inshore areas, whereas larger specimens were found in offshore waters, moreover, all individuals in the eastern were bigger than in the western North Atlantic. The size variation can be attributed to the presence of possible nursery areas in inshore waters, explaining the occurrence of smaller individuals. Our findings indicate unequal sex ratio against males, with 1.3 females for each male, suggesting gender habitat preference in the Atlantic Ocean, this can be explained by social or habitat linked causes. The thorough scrutiny regarding catch-per-unit-effort (CPUE) proved that CPUE values were higher in inshore regions for the North Atlantic, while the South Atlantic Ocean, both inshore and offshore waters had high CPUE for the shortfin mako. In addition, yearly, seasonal, and regional differences in CPUE were analysed, with growing CPUE in South Atlantic since 2016.

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For the seasonal differences in the CPUE, it was clear that, for the North Atlantic, the CPUE peak occurs in Summer and Spring, whereas, for the South Atlantic, the peak in the CPUE happens in Autumn and Winter. These findings encounter the North-South migration that was previously reported in the literature for this species.

The vertical habitat use of the shortfin mako was also investigated from 17 specimens tagged with Pop-up Satellite Archival Tags (PSATs) in the North Atlantic Ocean. Our findings do not support clear diel pattern in vertical behaviour and demonstrate that shortfin mako vertical habitat tendencies are surface waters. Withal, differences between day and nighttime and maturity stages were found, with deeper vertical dispersion in daytime for juveniles and adults, but with and overall preference of juveniles for shallower and warmer waters than adults. These results brought to our attention the fact that juveniles are more likely affected by longline fisheries bycatch.

The findings in this study are beneficial additions to the understanding of shortfin mako behaviour and its habitat preferences. Indeed, our results are exploratory, and the analysis are necessarily indefinite, however, we hope that this study can invoke questions about the sustainability of the species in the future. Furthermore, it is worthwhile noting that the present study has inherent limitations. In particular, the data for this research was dependent of fishery observers and contemplated a portion of the Spanish pelagic longline vessels. In addition, the shortfin mako geolocation estimations by PSATs are not entirely precise and have related estimation errors. Thereby, forthcoming studies are needed to comprehend the vertical and horizontal habitat use and distribution of the shortfin mako in the Atlantic Ocean.

Considering that the present study was limited to the areas that the Spanish longline fisheries cover, and the chance that the shortfin mako might occur in regions not included in the research cannot be rejected, its privileged that further investigations should be able to encompass a broader geographical area. Moreover, models for a standardized CPUE data shall be enforced to assure that the tendency to assume the CPUE as an index of abundance is eliminated. Regardless of the limitation that electronic tagging has, it has proven to be an advantageous mechanism to comprehend the horizontal and vertical ecology of the shortfin mako shark. Hence, it is necessary to begin attempting long-term monitorization of the species and increment the number of specimens. In order to endorse efficient conservation and management actions, we recommend that future studies should focus on determining hotspot regions for the shortfin mako and distinguishing behavioural trends regarding gender and maturity stages. Notwithstanding, satellite telemetry can be a powerful tool for assessing post

FCUP 79 Trans-Atlantic movements and behaviour of shortfin mako sharks in the North Atlantic Ocean release mortality for the I. oxyrinchus, seeing that there is a retention ban but there are no present studies that conclude on whether that conservation measure is successful.

Conclusively, our findings contribute with an improvement of the existing information for the shortfin mako in the Atlantic Ocean and, hopefully, can be used for better assessing the species conservation status and for the implementation of accomplished scientific based conservation decisions for this apex-predator.

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Appendix A Table A.1 – Attributes of Shortfin mako, Isurus oxyrinchus, tagged in this study with both PSAT and SPOT tags, with information on length (cm FL), sex, tagging date, tagging coordinates, final coordinates, and days at liberty. F = Female; M = Male.

Length Tag Tagging Tagging Tagging Days at Final Final Tag ID Sex (cm FL) Type Date Latitude Longitude Liberty Latitude Longitude

78680 175 F PSAT 17/10/2008 45.03 -47.48 119 26.52 -14.54 78682 167 M PSAT 13/10/2008 45.05 -46.96 80 43.86 -27.54 78683 151 M PSAT 09/10/2008 44.79 -48.03 143 33.67 -50.80 86399 140 M PSAT 25/06/2010 42.37 -44.25 59 47.74 -31.38 86400 125 M PSAT 23/04/2009 39.45 -43.17 29 40.75 -48.99 86401 220 M PSAT 30/06/2010 40.8 -48.42 87 46.31 -40.53 86402 170 F PSAT 24/04/2009 40.12 -44.42 59 26.07 -50.39 86407 130 M PSAT 03/07/2010 40.92 -48.55 89 44.75 -43.18 86408 180 M PSAT 27/06/2010 42.68 -45.67 114 40.58 -50.27 96030 130 F PSAT 04/07/2010 42.28 -48.73 117 38.65 -10.62 96031 165 F PSAT 05/07/2010 41.27 -48.47 119 42.36 -39.81 107089 220 F PSAT 21/08/2011 42.34 -28.36 117 20.64 -24.68 107090 255 F PSAT 22/08/2011 42.39 -29.43 117 37.48 -30.19 107091 245 F PSAT 08/11/2011 34.92 -45.96 49 28.34 -48.35 107092 170 M PSAT 03/09/2011 34.15 -36.45 113 39.34 -43.29 148786 170 M PSAT 27/01/2017 14.17 -28.26 17 13.91 -21.41 164446 160 F PSAT 24/01/2017 13.4 -29.07 37 18.98 -17.51 40392 210 F SPOT 05/09/2011 34.37 -36.58 58 18.90 -52.79 40393 200 M SPOT 08/09/2011 35.21 -36.41 50 42.35 -44.59 135931 185 M SPOT 23/08/2015 42.02 -39.49 39 41.38 -43.75 135932 195 F SPOT 23/08/2015 41.36 -39.43 225 32.41 -43.36 135933 160 F SPOT 09/06/2014 42.03 -43.4 66 42.86 -38.08 135934 180 M SPOT 09/06/2014 42.11 -43.58 54 41.56 -40.33 132343 152 F SPOT 27/07/2013 40.85 -71.72 37 40.45 -73.17 132344 152 M SPOT 27/07/2013 38.21 -73.6 325 39.79 -72.27 132345 152 F SPOT 28/07/2013 40.84 -71.52 185 33.65 -45.69 141194 160 M SPOT 12/07/2014 40.69 -71.51 11 40.09 -70.98 141197 183 F SPOT 13/07/2014 40.66 -71.51 29 40.83 -69.79 141198 198 F SPOT 13/07/2014 40.6 -71.62 301 37.74 -73.14 141198a 206 F SPOT 18/07/2015 40.79 -71.54 40 43.66 -60.24 149238 140 M SPOT 27/08/2015 41.32 -39.14 36 41.37 -38.30 149240 160 F SPOT 27/08/2015 41.26 -39.42 102 40.13 -38.53 149242 170 F SPOT 28/08/2015 41.11 -39.38 191 41.11 -39.38 149243 160 M SPOT 28/08/2015 41.02 -39.41 33 46.40 -42.24 149244 150 M SPOT 30/08/2015 39.47 -40.43 103 37.53 -43.42 149245 170 F SPOT 03/10/2015 40.83 -40.94 23 39.51 -40.44 149246 210 F SPOT 26/12/2015 38.87 -40.93 77 36.16 -55.41 160390 220 M SPOT 16/01/2017 11.07 -24.13 87 13.60 -20.94 160391 210 F SPOT 17/01/2017 10.13 -22.42 32 7.68 -20.67 160392 160 F SPOT 20/01/2017 12.47 -28.03 61 14.23 -18.09 160393 150 F SPOT 28/01/2017 15.15 -28.41 69 17.79 -17.38

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