Читать книгу Fish and Fisheries in Estuaries - Группа авторов - Страница 39

Estuaries can be diverse and complex habitats, offering a broad range of salinity, water quality, hydrographic characteristics and habitat types (Whitfield et al. 2022a). As such, it is not surprising that numerous reproductive modes have evolved and are represented by taxa using the estuary for reproduction. Species reproducing in estuaries and using them as nurseries range in size from small (e.g. fundulids, gobiids, clupeids, and engraulids) to the largest (some sharks, acipenserids) fishes (e.g. Blaber 2000, Elliott & Hemingway 2002, Able & Fahay 2010, Whitfield 2019). Habitat diversity in part explains the broad range of reproductive behaviours and habitat utilisation exhibited by adult spawners and early‐life stages (Able et al. 2022).

The modes of reproduction by fishes in estuaries have changed markedly since the Late Devonian when estuaries were dominated by live‐bearing taxa (Gess & Whitfield 2020). However, following a mass extinction event at the end of the Devonian, virtually all these estuary‐associated species were extirpated, and estuaries then became fully colonised by actinopterygians, a feature that has persisted into the Holocene. Therefore, modern estuaries are dominated by oviparous taxa, which contrasts to the earlier prevalence of viviparous and ovoviviparous species during the Late Devonian (Gess & Whitfield 2020).

Most marine bony fishes spawn pelagic eggs, but in estuaries there is increased incidence of taxa that spawn demersal eggs, presumably as an adaptation for retention in the spawning area (Pearcy and Richards 1962, Able 1978, Potts 1984, Elliott & Hemingway 2002, Able & Fahay 2010). Gobiids are classic examples of such fishes. The demersal‐spawning strategy apparently also applies to tidal and non‐tidal freshwaters as for Osmerus spp., Salmo salar and other salmonids. Many freshwater taxa with demersal eggs inhabit and reproduce in brackish waters of the northern Baltic Sea, for example percids, cyprinids and esocids. Fishes with demersal eggs include species that do not guard their eggs, those that do and those that bear live young (Balon 1990, Blaxter 1969). Estuarine fishes are represented in all these groups.

Species with pelagic eggs dominate the component of the estuarine fauna that originates from spawning in the ocean (Able and Fahay 2010, Whitfield 2019) and in some cases in estuaries (Schultz et al. 2000, Ribeiro et al. 2015). Some estuarine spawners have eggs that are slightly denser than water but can be suspended at modest current velocities, e.g. the moronid Morone saxatilis (Mansueti 1958) or at higher salinities as for the soleid Trinectes maculatus (Fahay 2007). Some variation can occur within the same or similar species. For example, the pleuronectid Platichthys flesus trachurus spawns pelagic eggs in deep waters of the Baltic Sea; however, in shallow coastal areas of the northern Baltic, and in the gulfs of Finland and Riga, there is a closely related, demersal‐spawning species Platichthys solemdali that produces smaller and heavier eggs, which sink in low salinities (5–7) and develop at the bottom of shallow banks (Solemdal 1967, Nissling et al. 2002, Florin & Höglund 2008, Momigliano et al. 2018). As in other marine teleosts in the Baltic Sea, reproductive success of the two Platichthys species depends on the ability of developing embryos or newly hatched larvae to float in the brackish, low‐saline water (Nissling et al. 2002).

Other estuarine species undergo embryonic development internally, as in viviparous and ovoviviparous species that are born live at relatively advanced stages of development (e.g. syngnathids, hippocampids, chondrichthyans). In the viviparous Zoarces viviparus (Zoarcidae) in the Baltic Sea and estuaries around the central and northern North Sea, females carry developing young for four to five months (Kristofferson & Pekkarinen 1975, Elliott & Griffiths 1986). In viviparous species, the development of embryos depends mainly on embryonic yolk reserves, with only a small maternal contribution to embryonic growth. In an upper‐estuarine gobiid from South Africa, Glossogobius callidus, precocial embryonic development results in the emergence of larvae that have already undergone flexion in the egg (Strydom & Neira 2006). This adaptation is thought to provide newly hatched larvae with stronger swimming abilities to prevent being lost by ebb‐tide flushing to the lower estuary or marine environment.

The modes of reproduction in estuarine fishes are strongly influenced by the spatial location of spawning sites. Some species, either residents or migrant spawners, spawn only in estuaries. Other species have population or stock components that spawn both coastally and within estuaries (Able & Fahay 2010). Adults of anadromous species have remarkable homing ability (philopatry) and return to their natal estuaries to spawn or undertake riverine spawning migrations (Secor 2015, Quinn 2018), which, for some taxa, is a singular event followed by death, i.e. semelparity, as in many salmonids (Figure 3.2), or for other taxa is characterised by potential for adults to return and undertake repeat spawning (i.e. iteroparity, as in acipenserids). This diversity in reproductive modes is mirrored in the variation in freshwater rearing duration (Figure 3.2).

Figure 3.2 Generalised life history of iteroparous and semelparous anadromous salmonids showing the central role of the estuary as a transition between the freshwater and ocean phases of the life cycle. a = sub‐yearling migrants, mid‐summer; b = sub‐yearling migrants, fall; c = yearling smolts; d = early spring migrants (recently hatched young or repeat migrants); e = kelts or returning veterans

(modified from Levings 2016).

In some instances, the location and timing of spawning vary amongst cohorts. Pomatomus saltatrix demonstrates cohort‐based differences of estuarine use and recruitment along the east coast of the USA (Wuenschel et al. 2012). Production of a spring‐spawned cohort occurred in both South Atlantic Bight and Middle Atlantic Bight habitats (south and north of Cape Hatteras, respectively), while a summer‐spawned cohort was limited to the Mid‐Atlantic Bight and south of Cape Hatteras. Estuarine habitat use by P. saltatrix varies between cohorts and time of year. Based on these characteristics, modelling indicates that the Mid‐Atlantic and South Atlantic bights provide similar numbers of recruiting young produced by the spring‐spawned cohort, but only the Mid‐Atlantic Bight produces recruits from the summer‐spawned cohort.

There is evidence of spatial partitioning of spawning by resident taxa and by spawning migrants within estuarine systems, e.g. selection of different salinity zones by some adults of Morone americana that ensures variability in hatching and nursery areas (Kerr & Secor 2012). Some species clearly have adapted to human alteration of estuary habitat and now spawn in areas that remain accessible after dams have blocked access to historical spawning sites, e.g. alosine species (see Limburg & Waldman 2009, Able et al. 2020). Although modes of reproduction are diverse, relatively few species reproduce within estuaries, possibly because of extreme and sometimes rapid changes in temperature and salinity, as well as microbial‐rich conditions that can prevail (Dando 1984). In addition, other water quality conditions such as hypoxia can be stressful to young fishes (Teichert et al. 2017).

There are numerous estuary‐associated species that spawn both in estuaries and the adjacent ocean (Able 2005). The diversity of spawning modes and early‐life ecology is also expressed in the fecundity, egg and larval size, morphology, embryonic duration and their pelagic, demersal or semi‐demersal habitats, all characteristics that influence dynamics associated with the recruitment processes of fishes (Forsgren et al. 2002, Cole 2010, Fogarty & O'Brien 2016, Houde 2016).

Many estuary‐dependent species have adults that spawn in the ocean and their larvae grow and survive there, either distantly or near the spawning sites. This is clearly apparent in catadromous species such as the eels Anguilla rostrata (in North America), A. anguilla (in Europe), A. japonica (in Japan) and Conger oceanicus (in North America) and C. conger (in Europe) (Able & Fahay 2010, Kettle et al. 2011, Tsukamoto et al. 2011). Their leptocephalus larvae transform to ‘glass eels’ before entering temperate estuaries in the western North Atlantic, such as those entering Little Egg Inlet in New Jersey (USA). These can result from spawning that occurred 100 s to >1000 km distant, e.g. spawning that occurred in the Sargasso Sea for Atlantic anguillids, southern Florida for elopomorphs or Georges Bank to the north for some gadids (Figure 3.3). Other larval taxa entering New Jersey estuaries originate from north and south of Cape Hatteras or elsewhere in the Mid‐Atlantic Bight.

Four species of anguillid eels utilise tropical, subtropical and warm‐temperate river catchments in southern Africa as nursery areas (Bruton et al. 1987). Like other anguillids, these species are obligate catadromous migrants that require estuaries for both the immigration of the ‘glass‐eel’ life stage and the emigration of adults to spawn in the marine environment. The four species Anguilla bicolor, A. mossambica, A. nebulosi and A. marmorata spawn in the open sea east of Madagascar and larvae are transported to the west by major ocean currents (Robinet et al. 2003, Pous et al. 2010). Evidence suggests that the most common of the eel species on the subcontinent, Anguilla mossambica, migrates from South Africa to marine waters off Madagascar where spawning occurs (Jubb 1961), a distance of at least 3000 km. Fertilised eggs and larvae are then swept southwards by the Agulhas Current, with the larval leptocephalus stages exiting the current and moving onshore along the coasts of Mozambique, east and south east South Africa to enter perennially flowing rivers via estuaries entering the Western Indian Ocean (McEwan & Hecht 1984). Additionally, spawning areas of six species of southwest Pacific anguillids (Anguilla bicolor pacifica, A. marmorata, A. australis, A. reinhardtii, A. megastoma and A. obscura) that ingress to estuaries and freshwaters of islands and continental land masses were delineated from small leptocephali larvae collected broadly within latitudes embraced by the South Equatorial Current (Kuroki et al. 2020), highlighting the extensive spawning migrations by adults and sometimes overlapping spawning periods of these species.

The elopomorphs Megalops atlanticus and Elops spp., which also have leptocephalus larval stages, spawn offshore in the coastal seas of tropical and subtropical regions and, like the anguillids, spawn pelagic eggs in the open sea. Leptocephali of these elopiforms enter estuaries where they metamorphose and grow (Crabtree et al. 1997, McBride et al. 2001). In the case of M. atlanticus, the prolonged juvenile stage may encompass 7–10 years of estuarine habitation before maturation in Florida and Louisiana, USA (Kurth et al. 2019). A high percentage of individuals of another elopomorph, Albula vulpes, also may ingress to estuaries as advanced leptocephali and utilise estuaries as nurseries in Florida and Cuba (Santos et al. 2019).

Figure 3.3 Sources of larvae transported from several locations in the western North Atlantic to Little Egg Inlet in southern New Jersey, USA.

Migrations of other early‐life stages from ocean spawning sites to estuarine nurseries can extend to hundreds of kilometres or more, and migrations by adults to estuarine spawning habitats by anadromous fishes (e.g. some salmonids, the moronid Morone saxatilis) may approach or exceed 1000 km. However, the early‐life stages of these fishes, once within the estuary or estuarine tributaries, are often confined to small areas (1–10 km) with hydrographic features that promote retention and ensure growth, survival and successful recruitment. In the long‐lived acipenserids (sturgeons), adults may migrate hundreds of kilometres along the coast or within large estuaries, before ascending freshwater rivers where they spawn demersal eggs. Young‐of‐the‐year and juvenile acipenserids may remain in the rivers or migrate to estuaries and shallow coastal regions, sometimes undertaking extensive coastal migrations (100 s to 1000 s of km) during their years in a protracted juvenile stage (Van Eenennaam et al. 1996, Bemis & Kynard 1997, Birstein et al. 1997, Secor et al. 2002).

Patterns in spawning locations by estuary‐dependent fishes also vary. Some estuarine taxa spawn selectively in the vicinity of the salt front (e.g. moronids) while others may spawn widely in the estuary, or select spawning habitats on its fringing shoreline (Able & Fahay 2010, Whitfield 2019). The clupeid Brevoortia tyrannus typically spawns pelagic eggs in the coastal ocean, but substantial spawning can occur within larger estuaries (Able & Fahay 2010) such as Chesapeake Bay (Hildebrand & Schroeder 1928, Murdy et al. 1997, MDSG 2009). The engraulid Anchoa mitchilli also spawns both on the continental shelf and in estuaries along the Atlantic coast of North America (Able & Fahay 2010), with most spawning probably occurring within estuaries. In the Eastern Atlantic, the engraulid Engraulis encrasicolus spawns in continental shelf waters but also in coastal estuaries of Europe and the Mediterranean region (Morais et al. 2012). The tropical alosine Ethmalosa fimbriata spawns both in estuaries and at sea off West Africa, with spawning concentrated during cooler months in the estuaries and in warmer months at sea (Faye et al. 2014). Indo‐Pacific alosines in the genus Tenualosa are economically important fishes that spawn in coastal, estuarine and freshwaters (Blaber et al. 2003a, 2003b, Wahab et al. 2019) from the Arabian Gulf to the Philippines. Some, for example T. toli, are anadromous while others, e.g. T. ilisha, are estuarine spawners. Variability in spawning habits and modes are present in the Tenualosa species (Blaber et al. 2003a). Some species, for example T. macrura and T. toli, are protandrous hermaphrodites (Blaber et al. 2009).

Another pattern is for anadromous species to grow and mature in the ocean and then return to spawning grounds in freshwater, e.g. salmonids and some alosine clupeids (Able & Fahay 2010, Levings 2016, Quinn 2018). For many of the noted taxa, there is a strong temporal component to estuarine use that is especially prominent in temperate estuaries with strong seasonal changes in temperature as in the Baltic Sea (Arula et al. 2019) and the western North Atlantic (Able & Fahay 2010) and in the southeastern Atlantic and southwestern Indian Ocean off South Africa (Whitfield 2019), but less so in tropical estuaries (Blaber 2000). In South Africa, the ubiquitous estuarine clupeid Gilchristella aestuaria, a serial spawner, spawns in response to riverine input into an estuary (Strydom & Whitfield 2000), suggesting a range of triggers for spawning in estuarine species.

Fecundity (defined here as egg production) in fishes, including those that use estuaries, is variable and can range from fewer than 10 in chrondrichthyans, to <200 in livebearers of small species, to millions in other species. Modes in fishes associated with estuaries are often related to fecundity, with viviparous (e.g. Clinus spatulatus, Whitfield 1990; Zoarces viviparus, Muus & Nielsen 1999) and ovoviviparous (Syngnathus fuscus, Campbell & Able 1998; Nerophis ophidion, Dawson 1986) taxa producing low numbers of eggs (Whitfield 2019). However, oviparous fishes (e.g. Mugil cephalus) produce many more eggs (Dando 1984, Whitfield 1990), with numbers ranging from thousands (e.g. Anchoa mitchilli, Zastrow et al. 1991) to millions (Morone saxatilis, Gervasi et al. 2019). Fecundities can represent the annual egg production from a single spawning event (capital spawning) for some species (e.g. Clupea harengus, Morone saxatilis) or the result of serial egg spawning (i.e. income, or repeat or batch spawning) practised by many species (e.g. engraulids and many clupeids) (Dando 1984, McBride et al. 2015, Arula et al. 2019) during extended spawning seasons (Zastrow et al. 1991, Peebles et al. 1996).

A recent synthesis focused on reproductive strategies and mechanisms, emphasising energy acquisition and allocation to spawning (McBride et al. 2015). Some species, especially large taxa such as Acipenseridae, that spawn in estuaries or their tributaries essentially are capital spawners, but individuals may not spawn every year, a strategy to maintain reproductive fitness (McBride et al. 2015). Differences in spawning strategies and processes of estuarine and estuary‐associated fishes span the known spawning alternatives in fishes. Adults may maintain flexible processes for energy acquisition and allocation to reproduction, sometimes prioritising their own nutritional condition over that of egg production to maximise reproductive value (McBride et al. 2015). The batch‐spawning engraulid Anchoa mitchilli presents an example of this strategy in Florida estuaries (Peebles et al. 1996).

Fecundity also varies with female size. As for most bony fishes, fecundities of estuarine fishes increase rapidly with female weight. For example, fecundity increases >18‐fold from 170 000 to 3 100 000 in the moronid Morone saxatilis of 2.8–36.8 kg, respectively (Mansueti 1961, Goodyear 1985) and tenfold (12 000 to 108 000) for the autumn‐spawning Baltic clupeid Clupea harengus membras of body mass 25–70 g, respectively. Individuals of similar age may have different fecundities. For example, in three‐year‐old C. h. membras, fecundity varied from 11 100 to 73 300 eggs (Arula et al. 2012b). For the serial‐spawning engraulid Anchoa mitchilli, batch fecundities range from 500 to 2000, and total fecundity can reach 50 000 eggs in an 80‐day spawning season for an adult of average mass 1.5 g wet weight (Zastrow et al. 1991).

Anadromy is unusual for an engraulid, for example Coilia nasus, which migrates from coastal bays, e.g. from Ariake Bay (Japan) into the Chikugo River estuary where it spawns (Suzuki et al. 2014). Small resident fish species with low fecundity often have parental care, for example gobiids, fundulids, atherinids and blennioids (Hastings & Petersen 2010, Able & Fahay 2010). In many regions, numerous estuaries, including large and complex systems (e.g. Baltic Sea, Chesapeake Bay, San Francisco Bay Estuary, Puget Sound) afford opportunity for variability in individual behaviours (portfolio effect) of spawning stock components (contingents) and variability in spawning patterns that promote sustainability of populations. Salmonids and moronids may best represent this strategy amongst estuary‐dependent species (Secor 2015, Levings 2016). There is value in maintaining a population structure that conserves old females (see Section 3.4.1.2) in many marine and estuarine fishes (e.g. Berkeley et al. 2004). Older and larger females including estuarine species such as the moronid Morone saxatilis have greatly elevated fecundities (Gervasi et al. 2019). Conserving their egg production is a tool that managers can utilise to sustain high spawning levels and high probabilities of recruitment success.