Open Water Lifestyles: Marine Nekton PDF

CHAPTER 5 Open water lifestyles: marine nekton Go for a swim in the sea and you are effectively joining the ocean’s nekton, albeit temporarily. All marine animals that spend their lives actively swimming around in the water column are part of the nekton. Unlike planktonic organisms that drift at t...

CHAPTER 5 Open water lifestyles: marine nekton Go for a swim in the sea and you are effectively joining the ocean’s nekton, albeit temporarily. All marine animals that spend their lives actively swimming around in the water column are part of the nekton. Unlike planktonic organisms that drift at the mercy of ocean currents and waves, nektonic animals are large enough and strong enough to control where they swim. The majority of nektonic animals are vertebrates and fish make up by far the largest group, both numerically and in terms of biodiver- sity. All cetaceans (whales and dolphins) are nektonic as are all pinnipeds (seals, sea lions etc.) although the latter also spend short periods hauled out on the seashore. Sea snakes and marine turtles also form part of the nekton, whilst the Marine Iguana (Amblyrhynchus cristatus) joins the nekton every time it plunges into the sea to forage for seaweed. Of all marine invertebrates only the cephalopods are predominantly nek- tonic and of these, squid make up by far the largest group. Squid live in large shoals and along with many shoaling fishes, form the basis of most of the world’s pelagic fish- eries. It is arguable that birds such as penguins, which spend most of their time under- water, could also be considered as a form of nekton. Whilst it is obvious that a large, fast-swimming fish is nektonic, it becomes more difficult with animals such as jellyfish. Most jellyfish (Scyphozoa) are weak swimmers and although many can reach a large size, they are still usually categorised as mega- plankton, on the basis that they cannot fully control where they go. However, there are exceptions, such as the notoriously dangerous Chironex fleckeri and other box jelly- fish (Cubozoa). The larger species are active predators and C. fleckeri can swim at speeds of up to four knots (Gershwin, 2016). They also have eyes and sensory systems capable of seeing and avoiding obstacles, moving towards prey and staying within a particular habitat (Garm et al., 2011). The majority of nektonic species live their whole lives swimming freely in the water column, albeit some live quite close to the seabed. However, a few primarily nektonic species may temporarily join the benthos on the seabed. For example, in contrast to most gobies (Gobiidae), which are small fish that live on the seabed as part of the benthos, the Two-spotted Goby (Gobiusculus flavescens) lives a nektonic exis- tence up in the water column, where it swims and hovers amongst seaweed. However, in the winter it moves down onto the seabed and takes up a benthic life- style. Working the other way round, some benthic squat lobsters have a swarming juvenile nektonic phase (see Crustaceans in Section 5.1.3). Many nektonic fish and Elements of Marine Ecology r 2022 Elsevier Ltd. DOI: https://doi.org/10.1016/B978-0-08-102826-1.00009-0 All rights reserved. 229 230 Elements of Marine Ecology cephalopods have planktonic larvae that drift on ocean currents and help to disperse the species. In terms of size categories there is an overlap between nekton and the two largest categories of plankton. Macroplankton range from 2 to 20 cm, which is the same size range as the smallest nekton, sometimes known as centimetre nekton. The megaplank- ton category, at 20 200 cm (see Table 4.1), overlaps with many nektonic species. Planktonic (Chapter 4) and nektonic organisms together inhabit the pelagic envi- ronment or the pelagic realm, the water column from the surface to a short distance above the seabed. The physical and chemical conditions under which pelagic organ- isms live vary both with distance from the shore and with depth and the main subdivi- sions are described in Section 1.2. Whilst visible changes may not be apparent, there is nevertheless real variability and patchiness at both large and small scales within the water column. 5.1 Epipelagic nekton The epipelagic zone from the surface down to about 200 m (see Section 1.2) supports a hugely biodiverse community of nektonic animals (Fig. 5.1). By far the largest pro- portion of the world’s pelagic fisheries catch comes from this zone, mainly over the continental shelf and areas of coastal upwelling. This is hardly surprising since these are nutrient-rich areas of the ocean with consequent high productivity from phytoplank- ton. Many of the targeted nektonic species are small to medium-sized fishes, such as herrings and anchovies (Clupeidae) and mackerel (Scombridae) as well as squid. Larger predatory fish such as tuna and sharks are also important commercial fishery species. Figure 5.1 Most octopuses live a benthic existence on the seabed, but Blanket octopuses (Tremoctopus sp.) hunt in the epipelagic zone. Up in the water column, they are vulnerable and so use the scarf-like webbing between their arms to make themselves look larger and deter predators. From Shutterstock Sam Roberts.  Open water lifestyles: marine nekton 231 The world’s populations of seabirds are largely sustained by nektonic fish and squid and along with larger predatory nekton, such as sharks, tunas and seals, seabirds play a significant role as top predators in the pelagic food web. Seabirds also connect terres- trial and ocean ecosystems by feeding at sea and (during the breeding season), defae- cating on land. Deep-diving nekton, such as whales, connect epipelagic surface waters with deeper mesopelagic and bathypelagic zones, by feeding at depth and defaecating at the surface (see Section 3.3.3 Animal vectors of nutrients). Williams et al. (2018) calculate that Grey Reef Sharks (Carcharhinus amblyrhynchos) transfer substantial nutri- ents from offshore epipelagic habitats, where most feeding occurs, onto nearshore coral reefs, by depositing faeces when they visit the reefs. 5.1.1 Fish Fish are the predominant nektonic animals in the epipelagic zone, with a very high bio- diversity of species as well as a high biomass. However, they also form the predominant part of the mesopelagic nekton and an important part of the deep-sea bathypelagic nek- ton as described below in Section 5.2 and Section 5.3.1, respectively. Fish do not make up a single natural class within the phylum of chordates (Chordata), as for instance rep- tiles or mammals do. Instead, there are seven currently recognised classes, not all of which are closely related and which have followed different evolutionary pathways: The elasmobranchs (Elasmobranchii) which comprise approximately 1250 marine species of sharks and rays. Whilst rays live a mainly benthic existence (with some important exceptions), sharks are top predators within the pelagic environment, particularly within the epipelagic zone. The chimaeras (Holocephali), a small class comprising around 55 species of mostly deepwater fishes, living and feeding near the seabed. The ray-finned fishes (Actinopterygii), which are by far the largest class and in which there are about 18,700 marine species. Two classes of jawless fish, the hagfishes (Myxini) and lampreys (Petromyzonti), the 140 or so species of which live a benthic or semiparasitic existence. Coelacanths (Coelacanthi) of which there are only two species. Lungfishes (Dipneusti) comprising six species of exclusively freshwater fishes. Ray-finned fishes and elasmobranchs are the predominant nekton in epipelagic waters. In this well-lit water fish are living in a habitat where there is nowhere for either predator or prey species to hide. Small ray-finned fishes feeding in open water on plank- ton near the surface are particularly vulnerable to larger, fast-swimming fish that hunt primarily through using their vision. In turn, even large predatory fish such as tuna are hunted by top predators including sharks and cetaceans. Camouflage techniques such as counter-illumination are important to both prey and predators, but many small prey species adopt active predator avoidance techniques some of which are described here. 232 Elements of Marine Ecology Predator avoidance Shoaling: Many small epipelagic fish species such as herring (Clupeidae) live in large shoals. Shoaling has distinct advantages and is a major survival strategy for nektonic fish. The majority of small fish species living in the well-lit, upper layers of the ocean, form large shoals. Predators find it difficult to target an individual fish within a shoal and observations and experiments have shown that predators are generally more suc- cessful in capturing prey which have become separated from the shoal (Box 5.1). BOX 5.1 The lateral line. Well-lit epipelagic waters mean that fish can make full use of vision for feeding, hunting for prey and looking out for predators. Fish also use vision to help coordination within a shoal, but this is not sufficient on its own to achieve the spectacular synchronised swimming and predator response such shoals are capable of. The lateral line system plays an important role in maintaining a standard nearest neighbour distance within a shoal. When a shoal is disturbed by the approach of a potential predator, the fish on the outside change direction and speed. The lateral line system that runs along the flanks of the fish detects the vibrations made by the fish swimming nearby. As the incoming vibrations change, the neighbouring fish can detect and follow the new route by maintaining nearest neighbour distance. The lateral line system consists of neuromasts clusters of ‘hair cells’ that lie within a fluid-filled canal running just below the skin and scales of the fish. Cilia project from the tops of the neuromast cells into a jelly-filled cap or cupula, which itself pro- jects into the lateral line canal. Water-borne vibrations carried through the canal deflect the cupula and bend the cilia, sending signals down sensory nerves. This is very like the workings of the inner ear, and the lateral line system and the inner ear together form an acoustico-lateralis system. In some cases it appears that the swim-bladder and acoustico-lateralis system function together for production and detection of vibration (Hawkins, 1973), though this is more to do with sound pro- duction and hearing than it is with shoaling. Fish shoal for protection from predators, such as this Blacktip Reef Shark (Carcharhinus mela- nopterus) whether inshore as here or far offshore. From Shutterstock cbpix.  Open water lifestyles: marine nekton 233 Some predators have developed strategies to break up shoals and overcome this prob- lem by effectively herding and trapping fish shoals between themselves and the surface. As the fish panic, the shoal splits into smaller groups and individuals break away and can be picked off. There is plenty of dramatic underwater film footage of billfishes such as Sailfish (Istiophorus platypterus), lamnid sharks such as the Bronze Whaler (Carcharhinus brachyurus) and seals feeding in this way. Humpback whales (Megaptera novaeangliae) take this a step further by acting cooperatively to encircle fish shoals by blowing ‘bubble-nets’ and then lunging upwards to the surface through the shoal with mouths wide open. Many of the world’s most important commercial fish species are epipelagic shoaling fish. In this instance shoaling is an advantage to the fishermen, who can use sonar to detect shoals and large nets to encircle them, but therefore becomes a disadvantage to the fish. Gliding: Whilst the water surface may act as a dangerous barrier to fish shoals it can also provide an effective means of escape from predators. Flying fishes (Exocoetidae) react to a threat from a predator (or a perceived threat from boat noise) by launching themselves out of the water at speed, using their powerful forked tail. By spreading their large pectoral and pelvic fins they can glide for some distance before re-entering the water, well away from the source of danger. Egg survival: The majority of pelagic ray-finned fishes broadcast large numbers of eggs into the water (see Section 8.1.1) where they and subsequent larval stages become part of the plankton. They have few other options and their survival strategy is purely in terms of producing large numbers. Fish eggs and larvae form an important food source for larger zooplankton as well as other nektonic fish. However, coastal nektonic fish such as Atlantic Herring (Clupea harengus) that live in relatively shallow water can reduce egg losses by gathering together in spawning shoals and depositing enormous numbers of eggs on the seabed. The seabed provides some protection and the volume of eggs quickly satiates the predators. Out over deepwater, floating mats of seaweed such as Sargassum or suitable debris such as palm fronds provide some fish species with a safe hiding place for their eggs. Flying fish live very near the surface and use this strategy, the eggs becoming entangled due to long trailing filaments. Sometimes so many eggs are laid by gatherings of the fish, that the seaweed or debris sinks to the seabed, which can be advantageous or not depending on the depth of the seabed below them. Predatory fish A major problem faced by predatory epipelagic fish is getting close enough to their prey to be able to catch them. Many solve this problem by being fast swimmers and their body shapes are correspondingly streamlined for maximum swimming efficiency (see Section 2.4.2 Swimming rates). Consequently, epipelagic sharks, billfishes and tuna all have similar body shapes (see Blacktip Reef Shark in Box 5.1 and sailfish in 234 Elements of Marine Ecology Fig. 2.13b) and exhibit counter-illumination. However, some epipelagic hunters are the opposite to streamlined, designed to move in stealthily and ambush their prey. The John Dory (Zeus faber) (Fig. 2.13c) is shaped like a thin dinner plate and is almost invisible to its prey when it approaches head on. Ambush predators are much more common amongst benthic fish species. 5.1.2 Cephalopods Whilst the vast majority of molluscs are benthic species living on and within the sea- bed, the highly developed class of cephalopods (Cephalopoda), comprising squid, cut- tlefishes, octopuses and nautiloids, are predominantly nektonic, squid entirely so. However, octopuses are mostly benthic with a few notable nektonic exceptions, including blanket octopuses (Tremoctopus spp.) (see Fig. 5.1), the Vampire ‘squid’ (Vampyroteuthis infernalis) and umbrella octopuses (Grimpoteuthis spp.). The latter two live in deepwater and are described in Section 5.3.2. Nektonic squid are particularly common in the epipelagic zone and many are extremely abundant, supporting extensive fisheries (Section 8.3.2). The total world catch of cephalopods, predominantly squid, was 3.6 million tonnes in 2018. One of the commonest oceanic species is the Common Clubhook Squid Onychoteuthis banksii, which has a circumglobal distribution in tropical and warm temperate waters, but many other squid species are fished commercially. Excepting Nautilus and its relatives (Nautiloidea), cephalopods have no heavy, external shell and so are well-suited to a nektonic existence. Squid and cuttlefish (Fig. 5.2) do have a lightweight, supportive internal shell, which in cuttlefish is modi- fied as a buoyancy aid (see Section 2.5.4). Nautilus has retained a spirally coiled, cham- bered shell and can control the gas content of each sealed chamber to provide appropriate buoyancy. It occupies the last and largest chamber, maintaining a thin strand of secretive tissue that extends to all chambers (Fig. 5.2). Predator avoidance Out in the open with no protective shell, cephalopods are at high risk of predation and indeed are a major food source for a wide variety of epipelagic predators, including dol- phins and other toothed cetaceans, seals and sea lions, seabirds and many predatory fish. Out in the open ocean, squid form enormous shoals, providing protection in numbers, although they do not have the synchronised schooling abilities of many prey species of nektonic fish. However, they are extremely fast and manoeuvrable, can move forwards and backwards using their fins and have excellent vision. Jet propulsion provided by a sudden contraction of the internal mantle (a muscular sheet enclosing both viscera and mantle cavity) forces water out of a funnel beneath the head and allows the animal to shoot away backwards. These abilities also mean that squid themselves are efficient pre- dators of fish and other squid.  Open water lifestyles: marine nekton 235 Figure 5.2 Examples of nektonic cephalopods: (A) Nautilus shell; (B) Cuttlefish (Sepia officina- lis); (C) squid laying eggs on the seabed. Courtesy Paul Naylor (B); From Shutterstock Julian Gunther (C). Gliding: Using jet propulsion, squid can launch themselves into the air when threatened. Some species have developed this into a sophisticated escape mecha- nism with the ability to glide for several metres, using outstretched fins and fan- ning out their webbed head tentacles. During flight they can control their flight and re-entry, by changing body posture (Muramatsu et al., 2013). Several species of Ommastrephes have been observed to glide, along with various species in other genera (Maciá et al., 2004). Camouflage: All cephalopod groups except Nautiloidea can secrete a dark liquid ‘ink’ screen to confuse potential predators and behind which to make their getaway. Mesopelagic and bathypelagic species tend not to have this ability, because they live in darkness anyway. However, some such species including the Odd Bobtail (Heteroteuthis dispar) produce luminescent ink. Cuttlefish live mainly in coastal waters, hunting over the seabed and like benthic octopuses, they are experts at colour change. They use this ability both for camouflage and for communication. 236 Elements of Marine Ecology 5.1.3 Other invertebrates Crustaceans Whilst the vast majority of crustaceans are either benthic species, such as crabs and lobsters, or planktonic species, such as copepods, there are a few decapod crustaceans that live a pelagic life and are large and mobile enough to be considered as true nek- ton. In ecological terms the most important of these are species of squat lobsters (Galatheoidea) variously known as ‘lobster krill’ (e.g. Munida gregaria and M. subrugosa) and ‘red tuna crab’ or ‘pelagic red crab’ (Pleuroncodes planipes). Growing up to about 12 cm long and found in large swarms, they form an important part of the diet of vari- ous other open water nektonic species, particularly migratory fish such as tuna. Around the Falkland Islands, ‘lobster krill’ are actively hunted by Gentoo Penguins (Pygoscelis papua), which eat them in preference to other available foods, because of their high calorific value. Cetaceans, pinnipeds, seabirds and turtles will also feast on swarms that drift inshore. Only a few species of squat lobsters, including those mentioned above, form large swarms as part of their life cycle. The swarming stage consists of postlarval juveniles that actively swim inshore in order to find suitable shallow rocky areas in which to set- tle and spend their adult life. Whilst these animals can swim quite strongly, they are prone to being washed ashore in large numbers when migrating inshore. In this respect they straddle the boundary between large plankton and small nekton. In sum- mer months, shores and water along the eastern coasts of South Island in New Zealand can be turned red by large swarms of M. gregaria. This species is widely dis- tributed across southern hemisphere oceans at this latitude. Similarly, colourful strand- ings of P. planipes occur along the shores of California, USA. Adults of these squat lobsters are benthic detritus feeders, but during the swarming phase they are eaten by a wide variety of nektonic top predators and so link and recycle nutrients between the seabed and open waters. Shrimp-like mysids (Mysidacea) and euphausiids (Euphausiacea) also occur in huge swarms, particularly Antarctic Krill (Euphausia superba), but are only a few centimetres long and generally considered as plankton (see Section 4.3.1 and Fig. 4.12). Cnidarians True jellyfish (Scyphozoa) are extremely common in epipelagic waters, but in spite of the relatively large size of some species, they are generally considered as plankton (see Table 4.1). Although many can swim quite efficiently, their powers of locomotion are too weak for them to be classed as truly nektonic. However, as mentioned in the introduction to this chapter, some box jellyfish (Cubozoa) can swim strongly enough to direct where they are going.  Open water lifestyles: marine nekton 237 5.2 Mesopelagic nekton The mesopelagic zone extends from around 200 to 1000 m depth (see Fig. 1.9) and is sometimes known as the twilight zone, because sunlight can still be detected here at low levels. We might not be able to see anything at these depths, but many of the fish and squid that predominate have large eyes and other, sometimes extreme adaptations to increase their visual acuity. Some of these adaptations and more information on mesopelagic macrofauna are given in Section 2.6.4 particularly under Vision, Colouration and Bioluminescence. These sections can usefully be read in conjunction with this current section. These medium depths are well within reach of many apex predators, including those living predominantly within the epipelagic and making feeding forays to greater depths. This includes many sharks, cetaceans and some pinnipeds, such as elephant seals (Mirounga spp.), with extreme diving capabilities. Small and medium-sized meso- pelagic fish and squid are a fundamental part of the diet of such predators. One of the most abundant groups of small fishes in this zone is the lanternfishes or myctophids (Myctophiformes), of which there are over 250 species. During the day many remain at the lower levels down to about 1200 m, but swim up towards the surface layers at night to feed on planktonic animals, which may themselves have risen upwards simi- larly (see Section 2.6.3 Diel vertical migration). Such movements result in considerable energy flow between the epipelagic and mesopelagic zones. A second very large group of mesopelagic fishes, both in terms of biomass and biodiversity, is the order Stomiiformes. This includes viperfishes (Stomiidae) which extend well down into the bathypelagic, hatchetfishes (Sternoptychidae) and gonostmatids (Gonostomatidae). Of the latter, Cyclothone is believed to be the most abundant fish genus, or for that matter vertebrate, on Earth. It is these and other small mesopelagic fish that are responsible for the deep-scattering layer often visible on ships’ echo sounders (see Section 2.6.3). The total biomass of mesopelagic fishes has been estimated as at least 1000 million tonnes and they play a large role in oceanic ecosystems. For example, by feeding near the surface, but defaecating well down in the mesopelagic zone, particulate organic matter is given a ‘helping hand’ on its long journey from productive surface waters to the deep seabed. Using acoustic data and modelling Irigoien et al. (2014) calculate that mesopelagic fish biomass may actually be much higher than previously thought. Whilst the largest and fastest hunting sharks are to be found in the epipelagic zone, where there is plenty of prey, a wide variety of usually smaller and slower species live in the mesopelagic zone. Lantern sharks are one of the largest families of small sharks found at these depths. Whilst many lantern sharks are benthic, living on or near the seabed, some are semioceanic. Numerous photophores on the belly, sides and fins pro- vide camouflage in the form of counter-illumination, which helps hide their silhouette from predators swimming below them. A few unusual large shark species have adapted 238 Elements of Marine Ecology their morphology and developed unusual feeding methods to cope with a relative lack of food at the deeper levels. The long, snake-like body of frilled sharks (Chlamydoselachidae) allow them to eat prey at least half as long as themselves. Whilst they often feed near the seabed, they also hunt in water as much as 1000 m above it. Goblin sharks (Mitsukurinidae) are flabby-bodied, slow swimmers, but have the ability to shoot their highly specialized jaws forwards and catch unsuspecting prey, detected using their blade-like snout. 5.3 Bathypelagic nekton Whilst the majority of epipelagic fish and other nektonic animals are fast swimmers with good eyesight, these characteristics are not suited to living in perpetual darkness and in an environment where food is less readily available. Instead, nektonic animals living at these depths have developed complex and sometimes extreme adaptations of body form, physiology and behaviour, particularly with respect to lack of light and extremes of pressure (Box 5.2). Such adaptations are described in Chapter 2 and Section 2.5 (Water pressure) and Section 2.6.4 (Adaptations for life in darkness) cover these sometimes surprising aspects, including the vital role of bioluminescence. The bathypelagic or dark zone (see Fig. 1.9) provides an immense living space, but one with no natural light at all, and extends from around 1000 to 4000 m depth. Below this is the abyssopelagic zone with similar but even more extreme conditions. Ray- finned fishes and cephalopods are the predominant nekton in the bathypelagic and a brief account of these two groups is given below. BOX 5.2 Extreme adaptation. Sea cucumbers (Holothuroidea, Echinodermata) are one of the predominant benthic taxa found on the seabed at abyssal depths (see Section 7.4.5). Here they exploit organic material that has descended through the water column and accumulated on the sediment surface. However, one species is now known to live a pelagic existence well above the seabed, within the meso- and bathypelagic zones. Pelagothuria natatrix has adapted to this way of life by taking on the approximate shape and way of life of a jellyfish. With its body hanging down beneath a canopy of webbed oral tentacles, it resembles an inverted umbrella. Film footage taken from submersibles shows that this translucent, pale mauve animal can swim by up and down movements of its web of tentacles. With the mouth and feeding tentacles on the upper side, it may collect particulate matter within the umbrella, though its way of life remains mostly unknown. Whether it should be considered as nekton or plankton is ques- tionable. Other swimming holothurians are known (e.g. Paelopatides and Enypniastes), but these are benthic feeders with some swimming abilities.  Open water lifestyles: marine nekton 239 5.3.1 Deep-sea fishes Elasmobranchs, chimaeras and ray-finned fishes are all represented in the bathypelagic zone. Hagfish are found as deep as 5000 m, but these are benthic fishes. Chimaeras are generally deepwater species and are found from around 200 to 3000 m, where they live near the seabed hunting for invertebrates and fish. Most sharks are found in coastal waters and over continental slopes, down to about 2000 m. Both pelagic and benthic species are effectively absent below about 3000 m (Priede et al., 2006), probably mainly due to a scarcity of food which cannot match their high metabolic requirements. However, above this depth there are many small pelagic species especially lantern sharks (Etmopteridae), which as their name suggests, produce bioluminescent light (see Bioluminescence in Section 2.6.4) from photo- phores on the underside of their bodies. Bathypelagic ray-finned fishes have developed numerous ways of minimizing their energy requirements and have evolved specialised methods for hunting, finding a mate, and so on (Section 2.6.4). In many species this has entailed bizarre changes in body form, away from the ‘classic’ idea of fish shape and anatomy. Collecting and bringing fish up intact from such depths is difficult and it is only now that we are start- ing to obtain sufficient photographs and film footage to show the full structure and function of these animals. The number and diversity of ray-finned fishes decline with depth and is lower within the bathypelagic than it is within the mesopelagic, with epi- pelagic species the most diverse. Nevertheless, ray-finned fishes are an important and diverse part of deep-sea pelagic communities throughout the ocean. Anglerfishes (Lophiiformes), particularly the family Oneirodidae are probably the commonest bathypelagic fishes. Flabby whalefishes (Cetomimidae) are also frequent at these depths. Whilst sampling is obviously extremely difficult and expensive within the dee- pest parts of the ocean, known as the hadal or ocean trench zone, a variety of fish spe- cies are known from below 6000 m. Jamieson (2015) lists 14 species identified from deeper than 6000 m, some from in situ photographs. This includes what is still consid- ered to be the deepest recorded fish, Abyssobrotula galatheae collected from 8370 m in the Puerto-Rico Trench (Nielsen, 1977). This is probably about the physiological depth limit for fish (the fleeting glimpse of a ‘flatfish’ seen through silt-laden water during the record-breaking decent of the bathyscape Trieste to the deepest part of the ocean in 1960, is thought to have been of a flattened bathypelagic holothurian). 5.3.2 Cephalopods: giant squid and octopuses Whilst squid are the predominant cephalopods in epipelagic waters, both in terms of biodiversity and numbers, these fast-paced and short-lived species have few deep-sea representatives. Humboldt Squid (Dosidicus gigas) are a large species that can reach weights of around 50 kg and are abundant at some times and places in the eastern 240 Elements of Marine Ecology Pacific. However, they live mostly at mesopelagic depths down to around 700 m. Those squid that have adapted to living at bathypelagic depths are exceptionally large species that have caught the public imagination. The Giant Squid (Architeuthis dux) is the largest species, reaching mantle lengths of 2.5 m and a total length of at least 13 m. Many reported lengths are unreliable since most data are from dead and usually incomplete specimens. The tentacles are also somewhat elastic, making accurate mea- surement difficult. The Colossal Squid (Mesonychoteuthis hamiltoni) is the heaviest known species with a similar mantle length of around 2.5 m, but shorter tentacles and a recorded weight of nearly 500 kg. Both species are targeted by deep-diving Sperm Whales (Physeter macrocephalus). Unsurprisingly there is not much recorded data on how these nektonic, giant invertebrates live and whether they are active predators or catch their prey passively. The extremely long tentacles of Giant Squid may act as a curtain trap, with the animal hanging with head and tentacles trailing downwards in the water. Colossal Squid on the other hand have powerful caudal fins and hooked suckers on the eight arms and on the two longer, extendible feeding tentacles. In spite of this, they may not be the active hunters that such an anatomy suggests. Instead, they may have a slow pace of life (Rosa and Seibel, 2010), but there is still much to learn about these enigmatic animals and their role in the ecology of the bathypelagic zone (Fig. 5.3). The majority of octopus species live a benthic existence in shallow coastal waters. Unlike squid and cuttlefish, they do not have body fins and adjustable buoyancy aids that allow both of the former to hover in mid-water (see Cephalopod buoyancy devices in Section 2.5.4). However, a few octopodids (Octopoda) such as Stauroteuthis have partial or completely webbed arms and sometimes fins and have adapted to a Figure 5.3 This Colossal Squid was brought up from Antarctic waters firmly clasping fish caught on long lines at around 1500 m depth. It was frozen intact and is now on display at the Te Papa museum in Wellington, New Zealand. Its frozen weight was 495 kg.  Open water lifestyles: marine nekton 241 pelagic existence at mesopelagic and bathypelagic depths. Little is known of their biol- ogy and ecology as they are rarely seen or collected intact. Umbrella octopuses, popu- larly known as dumbo octopuses (Grimpoteuthis spp.), lead a semipelagic existence. They have two large protruding fins either side of the body that resemble large ears and by flapping these up and down, these octopuses swim gently just above the sea- bed, searching for benthic invertebrate prey. Most are under 30 cm long. In spite of its name, the Vampire Squid (V. infernalis) is more closely related to octopuses (Octopoda) than it is to squid, but this single species appears to be unique and is placed in a separate order Vampyromorpha. This is a truly pelagic species that feeds mainly on organic debris that sinks down from the upper layers of the ocean. Analysis of video footage has shown that when feeding, it extends one of a pair of very long, thin retractile filaments from pockets between the first and second arms. The trailing filament intercepts food particles and is then effectively reeled in and food wiped off using the arm tips, enveloped in mucus and pushed inside the space enclosed by a fine webbing between the arms, eventually reaching the mouth (Hoving and Robison, 2012). 5.4 Sampling nekton Commercial pelagic fishing uses a variety of nets designed for capturing different spe- cies at different depths (see Pelagic mid-water trawls in Section 8.3.2). Acoustic meth- ods are often used to find and target shoals of fish. Similar mid-water nets are used by research scientists, but mostly on a smaller scale and aimed at obtaining representative samples of the species present, rather than making large catches. Over the years various types and sizes of mid-water trawl have been designed and improved for both com- mercial and research purposes and well-equipped, modern boats mean that sampling is now possible at much greater depths than was previously possible. In commercial terms this has led to the exploitation of once unobtainable fish stocks, such as redfish (Sebastes spp.), but in terms of research ships, it has accelerated knowledge of deepwa- ter nektonic species. One of the problems of sampling nekton with nets is that many fish, cephalopods and other mid-water and especially deepwater animals are rather fragile. Bumped against the net meshes and squeezed together at the cod end, their bodies can be dam- aged, fins torn and features such as barbels and lures pulled off. Gelatinous species such as large jellyfish (whether considered as plankton or nekton) rarely survive intact. This problem can be addressed by net modifications such as adding an aquarium-like box at the cod end, which retains water and keeps the sampled animals alive. This is known as a cod-end aquarium. This obviously adds weight and makes the net more difficult to deploy. 242 Elements of Marine Ecology Mid-water trawl nets can be towed horizontally for a distance at one chosen depth, but as they are deployed open, they will also catch animals on the way down to the planned tow depth and on the way back up again. This makes it diffi- cult to record the natural vertical distribution of the animals brought up. To deter- mine this, a vertical haul can be made using a multinet or multisampler in which an opening closing system directs samples into separate nets and cod ends. Hauled up from the starting depth, one of the nets is opened and closed between each depth layer, using acoustic signals. Although this could be done using a single opening closing net and making several tows starting at the different depths, a multinet saves considerable time. Opening closing mid-water trawl nets are not new and simple models were used in the 1960s. Clarke (1969) describes a (then) new type developed for use from the RRS Discovery (1962), in Antarctic waters. Operated to depths of over 1500 m, it had a mouth that was opened and closed by remote control. With the mouth closed the net was lowered to the required depth, as indicated by the pulse frequency of a pressure-sensitive sound-emitter on the net. The mouth was then opened by a release mechanism activated by an acoustic signal from the ship. At the end of sampling a sec- ond acoustic signal from the ship caused the mouth of the net to close before hauling. Today the fourth RRS Discovery is a high tech, multidisciplinary ship operated by the National Oceanography Centre in the UK. As a general rule, nektonic animals become scarcer with depth and mid-water trawls for sampling mesopelagic nekton tend to be quite large. An opening (door spread) around 100 m wide and a vertical extent of around 20 m is fairly typical. Trawls used in commercial fisheries for bathypelagic fish such as redfish (Sebastes spp.) can be much larger, with a door spread of up to 150 m and a vertical extent up to nearly 200 m. A research ship of considerable size would be needed to operate similar- sized nets. However, large nets like these were used on an expedition to the middle of the North Atlantic Ocean in 2004, on the research vessel RV G.O. Sars. Nets of this size are able to sample large active bathypelagic fish and cephalopods, which previously have proved extremely difficult to catch. 5.5 Air-breathers 5.5.1 Marine mammals Marine mammals evolved from terrestrial ancestors, but have considerable morpholog- ical and physiological adaptations for living a marine existence. They retain the defini- tive mammalian characteristics of suckling their young on milk and having bodily hair, though in cetaceans the latter is extremely sparse. Only about 130 mammals are truly marine (out of a total of over 5000) but they are hugely important as top ocean preda- tors and in the case of the baleen whales, as plankton feeders. There are three main  Open water lifestyles: marine nekton 243 groups of marine mammals, cetaceans (Cetacea), pinnipeds (Pinnipedia) and sirenians (Sirenia), each of which has evolved and adapted to a marine existence independently (Fig. 5.4). The cetaceans comprise whales, dolphins and porpoises, pinnipeds are seals, sea lions and Walrus (Odobenus rosmarus) and sirenians (also called sea cows) are mana- tees and Dugong (Dugong dugon). The Sea otter (Enhydra lutris) and Polar Bear (Ursus maritimus) are also marine mammals because, like the other groups, they source their food from the ocean (though Polar Bears will also scavenge on land in the absence of sea ice from which to hunt). All mammals are endothermic (warm-blooded) and so are able to remain active, even in water at and below freezing point. However, to maintain their core tempera- ture, marine mammals must have effective insulation and most have large stores of fat (blubber) and/or thick layers of fur. Sirenians are the only herbivorous group of marine mammals. Figure 5.4 Marine mammals: (A) Bryde’s Whale (Balaenoptera edeni) feeds by lunging up through shoals of small bait fish and straining them out with its baleen plates; (B) the Indo-Pacific Bottlenose Dolphin (Tursiops aduncus) has peg-like teeth typical of fish-eating toothed whales; (C) Harbour Seals (Phoca vitulina) haul out regularly to rest and digest their latest meal; (D) Cape Fur Seal (Arctocephalus pusillus) colony in Namibia numbering many thousand individuals. (A) From Shutterstock aDam Wildlife; (D) Courtesy Alison Hitchens. 244 Elements of Marine Ecology Cetaceans Cetaceans are completely adapted to the marine environment and no longer have any connection to the land. They swim, feed and reproduce in the ocean, living an entirely nektonic existence and soon die if stranded on the shore. They are the most numerous marine mammal group, with nearly 90 species and are divided into two main groups, the baleen whales (Mysticeti) and the toothed whales (Odontoceti). There are only 14 species of baleen whales but these are all ocean giants, reaching between 10 and 30 m in length. In spite of their large size, these huge animals are fil- ter feeders, taking in huge mouthfuls of water and straining out euphausiids (Euphausiacea), tiny shrimp-like crustaceans only a few centimetres long (sometimes called krill), other zooplankton and small fish. The filtering mechanism consists of a series of brush-like plates called baleen, made of keratin, that hang down from the upper jaw (Fig. 5.4A). The largest whale of all, the Blue Whale (Balaenoptera musculus), which can reach 33 m in length and 190 tonnes in weight, is testament to the effi- ciency of this feeding method. Antarctic Krill (E. superba) (see Section 8.3.5) is vital for southern populations of Blue Whales and other giants such as Humpback Whale (Megaptera novaeangliae). With their immense bulk, baleen whales do not have the speed and manoeuvrability needed to be open water predators. Unsurprisingly toothed whales have teeth and this versatile group are top predators, found in all oceans (Box 5.3). The majority are less than 10 m in length and belong to the ocean dolphin family (Delphinidae) and the largest of these is the Orca or Killer Whale (Orcinus orca). Highly intelligent and with a complex social structure, these are apex ocean predators (i.e. they have no natural predators). The largest of all toothed whales is the Sperm Whale (Physeter macrocephalus), with males up to 16 m long and 24 tonnes in weight and is BOX 5.3 Echolocation. As top predators, toothed cetaceans play an important role in the open ocean ecosystem. They are extremely successful hunters, with a sophisticated echolocation system for finding their way around and for targeting and homing in on their prey. This acts on a similar princi- ple to the echo sounders and sonar systems (Section 1.1.7) used by ships. High-frequency pulses of sound generated via air sacs in the upper respiratory system are focused as they pass through a fatty organ within the head, termed the melon. The sound vibrations reflect back from objects and pass through the lower jaw to the auditory system. The detail within the reflected sound is such that these cetaceans can find, chase and catch fast-moving prey even in darkness and detect fish buried within a sediment seabed. Unfortunately, human activities such as shipping have made the ocean a very noisy place. More significantly for cetaceans, seismic survey noise and military sonar can directly interfere with their echoloca- tion, increasing the likelihood of losing their way and standing on the shore and decreasing their hunting abilities.  Open water lifestyles: marine nekton 245 the only living species in its family (Physeteridae). Sperm whales are renowned for their deep-diving abilities (see Section 2.5.2 Physiological effects of pressure on marine life) and are able to exploit food resources, such as deep-sea fish and Giant Squid (Section 5.3.2), from much deeper than most other cetaceans. However beaked whales are also deep divers, with the current record documented dive of just short of 3000 m, held by Cuvier’s Beaked Whale (Ziphius cavirostris). Although records of stomach contents are few, this and other deep-diving beaked whales also appear to target deep-sea squid. After decades of intense exploitation the commercial hunting of the great baleen whales and of Sperm Whales was effectively stopped in 1986, when the International Whaling Commission finally decreased catch quotas to zero. Major commercial whal- ing has a long history starting in the 1700s and reaching a crescendo in the mid-1900s. There has been some recovery of populations since then, but this is a very slow pro- cess and a few countries still practise commercial hunting of some species. Those large species that were most intensively hunted remain endangered, including Blue, Sei (Balaenoptera borealis), Fin (B. physalus) and especially the North Atlantic Right Whale (Eubalaena glacialis), which is critically endangered (IUCN, 2020). Pinnipeds Unlike cetaceans, pinnipeds (Pinnipedia) seals, sea lions, fur seals and Walrus (O. ros- marus) retain a vital connection with the land. Whilst superbly adapted to an aquatic existence, they must return to land (or ice) to have their young, to moult and to rest. For this reason they are restricted to coastal areas and so cannot make use of the immense open ocean. The majority of species and the largest numbers are found in cold polar regions and cold-temperate waters. There are currently 33 recognised species of pinnipeds (WoRMS, 2021), divided into three families, the eared seals (Otaridae), the true seals (Phocidae) and the Walrus, which is the only living representative in its family (Odobenidae). The eared seals are the sea lions and fur seals, all of which have tiny exter- nal ear flaps called pinnae, a feature that is lacking in true seals. Perhaps more importantly, eared seals have the ability to swing their hind limbs forward beneath their body when on land, something that true seals cannot do. Sea lions and fur seals, therefore, have greater mobility on land and in general can move much faster. When on the shore many pinnipeds gather in huge colonies numbering hundreds or thousands of individuals, especially during pupping (Fig. 5.4D). As pinnipeds are predators, particularly of fish and squid, they play an important role in the ecology of the nearshore areas where they hunt. Walrus are the most gregarious species and regu- larly haul out on sea ice, gaining purchase with their tusks and from which they make feeding forays. Unlike most pinnipeds, they feed mainly on the seabed, snuffling out benthic invertebrates and slow-moving fish. Large numbers, therefore, have a signifi- cant influence on the structure of Arctic and subarctic seabed communities. With their heavy bodies, these animals cannot spend long periods out at sea and the continued 246 Elements of Marine Ecology retreat of sea ice as a result of global warming is concentrating North Pacific herds onto shore-based haulouts. This means greater numbers feeding in smaller areas with potential impacts on local prey populations. Pinnipeds are themselves an important prey for top marine predators such as Orca (Orcinus orca) and White Shark (Carcharodon carcharias). There are a number of recognised types of Orca, which may eventually be shown to be different species or at least subspe- cies. Some of these specialise in feeding on marine mammals including pinnipeds. Off the west coast of Scotland, Orca migrate close inshore during the Grey Seal (Halichoerus grypus) breeding season, when they can catch inexperienced pups in the water. Polar Bears rely on catching Ringed (Pusa hispida), Bearded (Erignathus barbatus) and Harp (Pagophilus groenlandicus) seals, ambushing them when they surface through breathing holes, or digging them out from their pupping dens under the snow. Pinnipeds have been heavily exploited in the past, particularly northern hemisphere populations from the late 1700s through to the late 1900s. Hunting pressure has less- ened or ceased for most species, but additional pressures mean that five species remain endangered and two have become extinct within historical times. Sirenians Of the four living sirenians, the Dugong (D. dugon) is the only entirely marine species and has a wide distribution in the tropical and subtropical Indo-Pacific region. Dugong feed mainly on seagrasses and their grazing activities play a signifi- cant role in the community structure of the seagrass beds they frequent (see Section 7.4.2 Seagrass beds). Their dependence on seagrass makes them vulnerable to ongoing, human-caused degradation and loss of this habitat. The remaining three sirenians are all manatees, of which the West Indian (Trichechus manatus) and African (T. senegalensis) species live both in coastal marine waters and adjoining rivers, whilst the Amazonian (T. inunguis) manatee is an entirely freshwater species. All sirenians are entirely aquatic and the young are born, suckle and are raised in the water. Living in easily accessible inshore areas and being slow and placid animals, sirenians have been extensively hunted and both their numbers and range are much smaller than in the past. A fifth species, Steller’s Sea Cow (Hydrodamalis gigas) was hunted to extinction in the mid-1700s. 5.5.2 Marine reptiles Reptiles are an extremely successful class of vertebrate animals that evolved and diversified on land and there are at least 8000 species. However they are not well- suited to ocean-living and few have returned to live there, with only around  Open water lifestyles: marine nekton 247 90 marine species. Their characteristic tough, scaly skin provides good protection and water retention on land but can be an encumbrance to fast swimming in the pelagic environment. Reptiles are also ectothermic and unlike mammals they can- not regulate their body temperature more than a few degrees above ambient. This is a problem in cold ocean water and with the exception of the Leatherback Turtle (Dermochelys coriacea) marine reptiles are restricted to warm, mostly tropical waters. They, therefore, play a relatively small, but nevertheless important, role in the ecology of the pelagic environment. Reptiles are represented in the ocean by seven species of turtle (Testudines), two crocodiles (Crocodilia), one iguana (A. cristatus) and about 80 snakes (Serpentes) (Fig. 5.5). A number of other snakes and crocodilians can be found at least Figure 5.5 Examples of marine reptiles: (A) Green Turtle (Chelonia mydas) resting underwater; (B) Marine Iguana; (C) Yellow-lipped Sea Krait (Laticauda colubrina). (B) From Shutterstock Andy Deitsch; (C) Courtesy Elizabeth Wood. 248 Elements of Marine Ecology temporarily, in estuaries, mangroves and similar areas and may swim along coastlines. With the exception of true sea snakes (Hydrophiinae), all marine reptiles retain a con- nection with land, whereby they must lay their amniotic eggs on the shore as these cannot survive underwater. True sea snakes are viviparous and give birth to live young in the water, at depths from which the young can swim easily to the surface to take their first breath. When they can get them, the eggs and young of marine reptiles pro- vide a source of food for seabirds, terrestrial reptiles, mammals and even crabs. Sea turtles Sea turtles are truly pelagic species, able to travel long distances between feeding and breeding grounds. Their incredible migrations are described in Section 5.6.4. Of the seven species the Leatherback can be considered the most oceanic in that it’s diet of jellyfish and other gelatinous plankton allows it to feed well away from any coastline. Tagging has shown that when travelling over deep ocean, Leatherbacks make dives to at least 1000 m. Houghton et al. (2008) suggest that these may be exploratory dives to locate jellyfish. Green Turtles (Chelonia mydas) are herbivores, grazing on seagrasses and algae, whilst the remaining species feed mainly on benthic invertebrates. Jellyfish may also form part of their diet. Crocodiles The Saltwater Crocodile (Crocodylus porosus) is the only crocodilian that can survive long journeys out at sea and has been found as far as 1000 km from the nearest coast. They are, however, not confined to saltwater and travel far up rivers. When in saltwa- ter, the American Crocodile (C. acutus) tends to stay near the coast. Marine Iguana Endemic to the Galapagos Islands, Marine Iguanas occur in large numbers on some of the islands and are important marine grazers. Making short excursions into the water and diving down to at least 10 m depth, they graze on seaweeds, clinging onto the rocks with their long, sharp claws. The water is cold and the animals need to bask in the sunshine after each dive to warm up. Basking is a type of behavioural thermal reg- ulation common amongst terrestrial reptiles, which often need to warm up after cold nights in order to become active. Sea snakes Sea snakes are morphologically adapted to swimming relatively long distances, through having a sideways flattened tail. However, in spite of this, the majority cannot swim fast enough to catch pelagic fish. Hence most are restricted to coastal habitats including coral reefs, where they search the seabed for sedentary fish, such as crevice-living gobies. In the way of terrestrial snakes, they mainly use taste and smell to locate their  Open water lifestyles: marine nekton 249 prey. The Yellow-bellied Sea Snake (Hydrophis lapemoides) is an exception and leads a pelagic existence, floating and drifting on the surface out at sea, sometimes forming large ‘rafts’. The snakes feed on small pelagic fish that are attracted to such rafts and any floating debris. 5.6 Migration Nektonic marine animals with strong swimming abilities are in a good position to undertake extensive geographical migrations on a regular basis. Whilst some inverte- brates have this ability, long-distance migrations are mainly undertaken by vertebrates, including ray-finned fishes, sharks, marine turtles, whales and other cetaceans and some pinnipeds. Migration involves a considerable use of energy and for some species there are additional risks from exposure to predators and poor conditions, so the bene- fits must outweigh the disadvantages. The main driver behind migrations is the need to make the best use of available resources, particularly food and safe areas for breed- ing. Temperature changes are another important factor, with many temperate species moving seasonally between geographical locations to avoid winter cold. Seasonal onshore and offshore movements are also largely connected with water temperature. Shallow coastal waters may be ideal for a species in the warm summer months, but too cold in winter, whereas more stable temperatures may be found in deeper water. Long-distance migrations such as those made by some species of baleen whales can involve journeys of many thousands of kilometres, easily matching those made by ter- restrial mammals. However, not all marine migrations involve either long distances or very precise routes and timings. Neither does a whole population have to be involved. A common strategy amongst pelagic ray-finned fishes is to move inshore to spawn. Productive coastal waters provide greater supplies of planktonic food for fish larvae, whilst bays and estuaries provide sheltered nursery areas. In a species such as Atlantic Mackerel (Scomber scombrus) different stocks within a population may migrate to differ- ent spawning areas (see Section 8.1.4). Conserving energy can be key to a successful migration and many fish make use of ocean currents during their migrations. North Atlantic Blue Sharks (Prionace glauca) use Atlantic gyre currents to help carry them between mating and feeding areas off north- east USA and pupping grounds off Spain, Portugal and the eastern Mediterranean. In general, only the females make this journey and whilst it is known that some females return, details of their route back remain sketchy. Mass migrations move resources, sometimes across entire oceans, introducing a temporal aspect to the ecology of an area (Box 5.4), through seasonal influxes of prey species. Some small species of clupeid fish, variously known as sardines and pilchards, make migrations in immense shoals that can number millions of individuals. Triggered by seasonal changes in water temperature, the largest so-called ‘sardine run’ occurs off 250 Elements of Marine Ecology BOX 5.4 Pacific salmon support terrestrial forests. It is difficult to imagine that a marine fish could influence the ecology of a terrestrial forest. However, that is the case with several species of Pacific salmon. Salmon are anadromous (see Section 8.1.3), returning from the ocean into freshwater rivers to spawn. Extensive areas of coastal temperate rainforest are found along the Pacific coast of Canada and each year salmon make spawning runs up rivers that wind from the coast and deep into the forests via numerous small streams and creeks. After spawning in the upper reaches, the fish die and their bodies contribute nutrients to the riverside vegetation. Scavengers carry carcasses deep into the forest providing the trees with essential nutrients. In the Great Bear Rainforest, British Columbia, many fish are caught on their way upriver by brown bears (Ursus arctos) which rely on the salmon as a calorific source of food to help fatten up for winter hiberna- tion. The bears frequently carry their catch into the forest to feed, but are messy and waste- ful, leaving carcasses and remains strewn around and faeces amongst the trees. This is the largest temperate rainforest system in the world and its biodiversity, health and rates of growth are all linked to this major marine input of nitrogen and other nutrients (Temple, 2005) from the very high numbers of spawning salmon. Wild Pacific salmon stocks are heavily exploited and also threatened by changes in land use and escapees from salmon farms (see Section 8.6.3). This has implications both for fisheries and forestry management. the coast of South Africa’s eastern seaboard, but others have been documented and filmed off Mexico, the Philippines and into and away from the extensive fjord systems of Norway. Pacific Sardine (Sardinops sagax) prefer cooler water between about 10 and 20 C and one possibly genetically distinct population, uses a seasonal thin counter- current branch of the Benguela current to carry them northwards on their spawning migration up the east coast of South Africa towards the province of KwaZulu Natal. Further offshore the warm Agulhas current runs southwards, effectively keeping the fish channelled close inshore. This condensed flow of fish attracts and sustains large numbers of predators including Bryde’s Whale, dolphins, Cape Fur Seal (Arctocephalus pusillus), seabirds, sharks and many other predatory fishes. Whilst this and other such runs vary naturally in their intensity and timing with natural changes in current flows, alterations in currents caused by climate change are now likely to have further effects on these migration phenomena. The mechanisms behind migration that allow animals as diverse as spiny lobsters, fish and whales to find their way over long distances, are complex and by no means yet fully understood. Whatever the species, the animal needs to know where it is when it starts out in relation to where it wants to go. In other words both a map and a compass. An ability to detect and use the Earth’s magnetic field has been demon- strated experimentally in some birds, ray-finned fishes, turtles and sharks. Sharks may use their electro-sensory system to detect distortions in the Earth’s magnetic field. For  Open water lifestyles: marine nekton 251 air-breathing marine reptiles and mammals, there is the opportunity to use astronomi- cal clues. It is highly likely that most migrations, especially precise ones such as salmon returning to their natal river to spawn (Box 5.4), are accomplished using several differ- ent mechanisms, including geomagnetic, celestial, olfactory and learning. Highly migratory species present particular difficulties when it comes to conser- vation and fisheries management (see Section 9.3.4) and this certainly applies to anadromous and catadromous fish species such as salmon. These two terms apply to species that migrate between freshwater and ocean habitats as part of their life cycle and this is described in Section 8.1.3. Species that make regular migrations within the ocean are sometimes termed oceanodromous. Migration is a fascinating and important part of marine ecology, and is widely researched, but only a few aspects and examples can be described here. Some further reading on the topic is included at the end of this chapter. 5.6.1 Whale migrations Many species of baleen whale make long migrations between cold, food-rich feeding grounds in and near the Arctic and Antarctic and warm, but food-poor subtropical and tropical breeding areas. These immense animals need huge quantities of planktonic food and small fish to build up the thick layers of blubber that act both to keep them warm and as food reserves. Southern Ocean populations of Humpback Whales (Megaptera novaeangliae), spend the Antarctic spring and summer feeding on rich supplies of krill (E. superba). However in winter, as food supplies dwindle, they migrate north into the low- latitude waters around Hawaii. The planktonic food on which these baleen whales feed is scarce in these warm tropical waters and the adults must survive on their blubber reserves, but this is an ideal environment in which to give birth to their vul- nerable calves. The feeding grounds of the Grey (or Gray) Whale (Eschrichtius robustus) are in the cold northern parts of the North Pacific and adjacent Arctic waters, mainly around Alaska, where they spend the summer months. As the water begins to cool in autumn, the whales start their long migration south, following the west coast of North America towards the much warmer waters of Mexico and Baja California. Here they spend the winter and give birth to their calves. The annual migration is a 15,000 20,000 km round trip and the return journey for the calves is arduous, with deaths resulting from attacks by pods of Orca. Their summer grounds freeze over in winter so migration is the only way for them to access these rich feeding grounds. Winter ice cover in the Arctic has been reduced by climate change and it will be interesting to see if Grey Whales alter the timings or even extent of their migration. 252 Elements of Marine Ecology 5.6.2 Pinniped migrations All pinnipeds give birth and undergo an annual moult on land and many make predictable seasonal movements for these reasons. Northern Elephant Seals (Mirounga angustirostris), however, make exceptionally long migrations totalling as much as 21,000 km every year. They are the only mammal known to make a double migra- tion, from their normal feeding grounds, to more clement, southern areas once for breeding and once for moulting, hence the exceptional distances covered. Their breeding and moulting beaches (rookeries) are along the coasts of Mexico and California, whilst most forage much further north in the Gulf of Alaska and offshore out into the North Pacific where they feed mainly on squid. These northern waters provide a much greater abundance of prey, necessary for maintaining the energy requirements of these enormous animals. Their ability to store massive amounts of food in the form of fat reserves means that they can then fast for weeks whilst at their rookeries. This double migration is described by Stewart and DeLong (1995). 5.6.3 Fish migrations Sharks Large oceanic sharks are well-suited to long-distance travel and many undertake migrations. Some such as the Blue Shark have evolved regular seasonal migration routes but many migrate to take advantage of good feeding opportunities. Whale Sharks (Rhincodon typus) have a global distribution in tropical and warm temperate waters. Whilst they do not seem to follow any specific migration routes, they will travel long distances for seasonal food bonanzas. Numbers congregate each year on Ningaloo Reef off NW Australia, many arriving in late March, a time when mass coral spawning occurs 5 10 days after the March full moon. Whale Sharks feed on plankton and coral spawn provides a rich addition to their diet. Collection of data on the movements of individual Whale Sharks is now well-established through the ECOCEAN photo identification library (see Section 7.5.4). There is at least one recorded instance in which a Whale Shark crossed the entire North Atlantic Ocean. White Sharks have also been recorded making long, solitary migrations out and back again from specific locations, ranging long distances in search of prey. Regular migra- tions between Hawaii and Mexico also occur and some have been tracked making regular seasonal journeys. One satellite-tagged individual travelled from South Africa to Australia but the reason for this exceptionally long journey is unclear. In some shark species, males and females or mature and juveniles have different migration patterns. Scalloped Hammerhead Sharks (Sphyrna lewini) sometimes travel in large shoals (unusual for sharks) gathering around seamounts and other areas where prey is abun- dant. Nutrient-laden upwelling currents result in an abundance of plankton and there- fore an abundance of small fish and their larger predators. As adults these sharks are  Open water lifestyles: marine nekton 253 usually solitary and seamounts may act as known locations, marking travel corridors to pupping areas or they may have a role in mating. The transatlantic migration of female Blue Sharks has already been mentioned above in the introduction to Section 5.6. The long distances involved between mating and pupping grounds mean that the round trip takes more than a year to complete. Consequently, the females in the populations that undertake this journey cannot pro- duce pups every year. Blue Sharks are one of the most heavily fished sharks in the world and are declining and much more data on migration are needed if Atlantic populations are to be managed effectively. Tuna and billfish Along with oceanic sharks, tuna and billfish rank as the fastest and most powerful groups of nektonic fish and many are capable of making extensive, ocean-wide migra- tions. Tunas belong to a large family (Scombridae) of fishes, but most migratory tunas belong to the genus Thunnus. Billfishes include marlins (six species of Tetrapturus and two species of Makaira), sailfishes (Istiophorus platypterus and I. albicans) and Swordfish (Xiphias gladius). Pacific Bluefin Tuna (Thunnus orientalis) are known to make extensive migrations, par- ticularly between major spawning areas in and around the Sea of Japan and distant feeding areas. Archival tagging has demonstrated that young fish can and do cross the Pacific to the Californian coast, a distance of around 8000 km and that mature fish return from there and other locations to the spawning grounds. Such long migrations, through water of varying and sometimes very cold temperatures, are facilitated by this species being partially endothermic. This means the fish can maintain their core swimming muscles and organs, including the brain and eyes, well above ambient temperature. This is attained by a specia- lised network of blood vessels, the ‘rete mirabile’, which acts as a heat exchange mecha- nism preventing loss of muscle-generated heat when blood passes close to the exterior through the gills. Other large migratory tuna species, swordfishes, some marlin species and sailfishes also have this adaptation, as do some of the fastest swimming and migratory sharks such as the White Shark. A similar mechanism located near the base of the flippers allows the Leatherback turtle (Dermochelys coriacea) to extend its feeding range well away from the tropical waters where it breeds. 5.6.4 Sea turtle migrations As adults, all seven species of sea turtles lead solitary lives and during the years before they mature, they may disperse many thousands of miles away from their natal bea- ches. Females mature late, at ages ranging from about 10 to 30 years, giving them plenty of time to wander large distances. Once ready to lay eggs, the female turtles return to the area where they were born and come ashore on the same or a nearby beach to the one where they hatched. The Olive Ridley (Lepidochelys olivacea) and the 254 Elements of Marine Ecology Kemp’s Ridley (Lepidochelys kempii) turtles have mass synchronised nesting events (called ‘arribadas’) in some areas. Whilst much still remains to be learnt about turtle breeding migrations, the females appear to continue to use the same beaches for egg laying throughout their adult lives but do not lay every year. Clusa et al. (2018) have shown that in the Mediterranean populations of Loggerhead Turtles (Caretta caretta), males also return to the area and beaches where they were hatched. 5.6.5 Benthic species migrations Whilst long-distance migrations are, for obvious reasons, restricted to nektonic species, benthic, mobile animals can also migrate seasonally, but on a much more limited dis- tance scale. Many of these migrations are onshore, offshore and connected with find- ing refugia in response to seasonal changes in water temperature. Caribbean Spiny Lobsters (Panulirus argus) migrate in large numbers moving in a single file, ‘nose-to- tail’ fashion called ‘queuing’. This may save energy by reducing drag as well as provid- ing protection from predators. During the summer they feed in shallow, warm water, but autumn storms disturb this habitat making feeding more difficult and cooling the water. By migrating into deeper water for the winter they avoid rough waters churned up during the hurricane season and find more equitable and stable water temperatures. A few species of crabs have evolved to live a terrestrial existence, to the extent that they drown if permanently submerged. However, they retain a connection with the ocean through their planktonic larval stages. The necessity to return to the water to release their developing eggs initiates arduous seasonal reproductive migrations down to the coast. Christmas Island Red Crabs (Gecarcoidea natalis) live in burrows inland in forested areas of the island, but the first rains of the rainy season set them off on a mass migration down to the coast. Millions of crabs on the move make for a dramatic spec- tacle. Once at the shore, they mate in temporary burrows above the tide level where the females remain for about 2 weeks until their eggs are nearly ready to hatch. They then release the larvae into the water, always before dawn as the tide starts to recede. The actual timing is always on the final quarter of the moon when tides are highest. Some species of benthic fish also undertake seasonal migrations between feeding and spawning grounds. Most flatfish are not especially strong swimmers as their normal lifestyle involves lying on the seabed. However, Metcalfe et al. (2002) have shown that Atlantic Plaice (Pleuronectes platessa) in the North Sea can adapt their behaviour and use tidal currents to help them move relatively long distances to their spawning grounds (see Section 8.1.2). By swimming up into the water when the tide is running the way they want to go, they can use the current to help them along and save energy. When the tide turns, they remain on the seabed until the next tidal cycle. Telemetric devices attached to the fish were used to measure the depth at which they were swimming. Some aspects of fish tagging are described in Section 8.4.2.  Open water lifestyles: marine nekton 255 Further reading Boyd, I.L., 2004. Migration of marine mammals. In: Werner, D. (Ed.), Biological Resources and Migration. Springer. Available from https://doi.org/10.1007/978-3-662-06083-4_20. Priede, I.G., 2017. Biology, Diversity, Ecology and Fisheries. Cambridge University Press, 500pp. Secor, H.D., 2015. Migration Ecology of Marine Fishes. John Hopkins University Press, 292pp.