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.
3.2.1.2 Early‐life stages and nurseries
Ontogeny of estuarine fishes begins at fertilisation and continues after hatching, usually involving dramatic changes in morphology, biomass, sensory systems and behaviour, including swimming performance up to the juvenile stage, and thus colonisation of estuarine nurseries (Webb 1999, Fuiman & Werner 2002, Miller & Kendall 2009, Pavlov & Emel’yanova 2016). These early‐life history transitions occur during the stages of smallest size, fastest growth and highest mortality (Houde 1989a, 2016, Pepin 1991, 2016). The complex ontogenetic transitions in early life contribute to factors generating recruitment variability (see Section 3.3) in marine and estuarine fishes (Houde 2016).
Egg size can influence size at hatching, aspects of the morphology at hatching, nutritional status of newly hatched larvae and subsequent swimming and feeding behaviours. Bony fishes that hatch from large eggs may effectively hatch at an advanced developmental stage, i.e. with fins partially formed and able to feed (Balon 1984). Examples include Fundulus spp. and Cyprinodon variegatus (Able & Fahay 2010). Others from large eggs hatch and remain on the spawning site until they complete juvenile development, skipping the pelagic phase and settlement stage completely (e.g. batrachoidids, Opsanus tau) (Dovel 1960). Salmonids that reproduce in freshwater tributaries that feed into estuaries bury their large eggs in gravel substrates of freshwaters, often far from the sea, where a prolonged development (weeks to months) transpires before hatching (Levings 2016, Quinn 2018).
Larval size may influence reproductive success and dynamics leading to recruitment. For example, in western North Atlantic temperate estuaries, lengths of newly hatched fish larvae range from ~2 to 14 mm BL, with most individuals <6 mm and many in the 2–4 mm range (Able & Fahay 2010). Larval‐stage duration for species where information is available ranges from 11 to 82 days. In a meta‐analysis on fish ontogeny and related dynamics, the mean larval‐stage duration for estuary‐dependent species was 48 days (Houde & Zastrow 1993). Size for most species that settle in western North Atlantic estuaries ranges from 17 to 100 mm (Able & Fahay 2010), the larger lengths in part because some species (for example, Anguilla rostrata, Conger oceanicus) have pelagic juveniles (e.g. leptocephali, glass eels) that precede the settlement stage. Other species (e.g. the achirid Achirus lineatus) metamorphose and settle at only 6 mm (Houde et al. 1970). Between hatching and the juvenile stage, body shape and morphometrics may change dramatically, with eyes becoming functional, fin rays and internal organs developing, and sensory systems forming in both pelagic and demersal species (Fuiman & Werner 2002, Miller & Kendall 2009). Amongst the most dramatic examples of ontogenetic shifts and metamorphoses are those seen in pleuronectiform fishes (Figure 3.4) in which eye migration and restructuring of the body plan occur.
The behaviour of recently hatched larvae can dramatically influence their distribution, transport and recruitment. At one extreme, larvae that hatch from pelagic eggs are themselves pelagic, but their swimming ability varies, with many species having newly hatched larvae that are incapable of influencing their distribution, either vertically or horizontally, or weakly capable of vertical swimming (Leis 2006). Thus, many are essentially passive particles in the water column. At the other extreme, numerous species of resident, shallow‐water fishes hatch from relatively large demersal eggs, e.g. the fundulid Fundulus heteroclitus (1.7–2.0 mm diameter)