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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) and the cyprinodontid Cyprinodon variegatus (1.2–1.4 mm diameter). The recently hatched larvae of these two species are also relatively robust and large (4.8–5.5 mm and 4.2–5.2 mm, respectively) (Sakowicz 2003). A newly hatched F. heteroclitus is capable of entering the water column and even swimming at the surface, at least in the laboratory, while C. variegatus is incapable of these behaviours. The difference in these behaviours accounts for their different distributions in nature. For F. heteroclitus, its larvae are found in shallow depressions on the marsh surface and in the shallow waters of marsh pools and adjacent creeks (Able & Fahay 2010). For C. variegatus, larvae are only found in marsh pools. At the other extreme, eggs of salmonids that hatch in the gravel substrate where the eggs have been deposited (i.e. in a redd) may be resident there for months (Quinn 2018).

Figure 3.4 Eye migration during metamorphosis of settlement‐stage Paralichthys dentatus

(from Keefe & Able 1993).

The distribution of other species that spawn in the estuary varies in ways that may affect their transport into and out of estuaries. In one example, the moronid Morone americana spawns demersal eggs in estuaries on the east coast of North America that hatch into small (~3 mm) pelagic larvae with weak swimming ability. Larvae are passively transported to the estuarine salt front and estuarine turbidity maximum region where they are retained during early development (North & Houde 2001, Shoji et al. 2005b). In another example, the clupeid Gilchristella aestuaria spawns in the upper reaches of South African estuaries where the probability of estuarine retention for their pelagic eggs and weak‐swimming larvae is greatest (Talbot 1982).

Dispersal during the larval stage of estuary‐associated fishes was once considered to be largely via passive drift (Roberts 1997, Hare et al. 2002), but recent authors have noted that behaviours, including vertical and horizontal swimming, especially during late larval stages, have a strong influence on transport (Cowen et al. 1993, Leis et al. 1996, Stobutzki & Bellwood 1997, Hare et al. 2005a, 2005b). Dispersal during the recruitment process has been the emphasis of research on numerous species in many estuarine systems during recent decades. Recent evaluations of larval fish transport and navigation from offshore to the coast or estuaries have demonstrated that it is enabled by a suite of probable sensory cues (e.g. odour, sound, visual and geomagnetic cues) that become effective during ontogeny (Faillettaz et al. 2015, Teodosio et al. 2016, Rossi et al. 2019a), especially during and after the postflexion stage (Morais et al. 2017, Baptista et al. 2019, 2020) (Figure 3.5). It has been demonstrated that larvae and pelagic juveniles can use auditory cues (Montgomery et al. 2006), olfaction (James et al. 2008a) and other senses (Teodosio et al. 2016, Morais et al. 2017, Rossi et al. 2019a) for orientation towards estuary mouths using innate behaviours and infotaxis, an algorithm developed for turbulent odour plumes where searching movements by larvae are based on sporadic cues and partial information (Vergassola et al. 2007). Longshore currents may transport drifting larvae far from a natal or proximate estuary and directional swimming by postflexion larvae may be essential to ensure ingress to an estuary. Larvae unable to ingress to a proximate estuary may still ingress, but to an estuary downstream. Many examples documenting these transitions, and associated environmental conditions, are described for temperate estuaries (Boehlert & Mundy 1987, Allen & Barker 1990, Bruno et al. 2014, Ramos et al. 2017, Baptista et al. 2020). It is notable that larvae of many species enter estuaries at postflexion/metamorphic stages in North America (e.g. Figure in Able & Fahay 2010), South Africa (Strydom 2015), Europe (Bos et al. 1995, Jager 1999) and Australia (Miskiewicz 1986) when their sensory systems and swimming capabilities are still developing.

The swimming abilities of marine fish larvae, especially postflexion stages, may contribute importantly to dispersal (Fisher et al. 2000). In fact, in recent reviews (Leis 2006, Wuenschel & Able 2008), there is an indication that the larvae of many fishes are capable of swimming for long periods for much of the larval stage at speeds greater than ambient currents (see Section 3.3.1.2). The swimming capabilities of some larvae that use estuaries are impressive, as noted for postflexion and settlement stages of the sparids Diplodus capensis and Sarpa salpa (Pattrick & Strydom 2009) and Diplodus sargus (Baptista et al. 2019). In another example, the leptocephali of the congrid Conger oceanicus (69–117 mm Tl) and glass eels of the anguillid Anguilla rostrata (49–68 mm TL) were capable of performance in a laboratory flume that would allow them to swim the long distance from the Gulf Stream edge off the east coast of North America to the Little Egg Inlet (Wuenschel & Able 2008). This transit could be possible in ≈ 30 or 40 days from the edge of the continental shelf or the Gulf Stream edge for A. rostrata and ≈ 20 or 45 days from the shelf edge or Gulf Stream edge for C. oceanicus. Larvae of C. oceanicus entering this same inlet may arrive in even fewer days under conditions of faster growth (Correia et al. 2004).

Figure 3.5 Processes and cues supporting larval ingress into estuaries. (a) Estuarine (auditory, visual, odour) and navigational (geomagnetic, solar, stellar, coastal features) cues used by offshore fish larvae to detect estuaries and to navigate towards them prior to adopting active swimming for ingress

(modified from Teodosio et al. 2016, their figure 2).

Near the estuary mouth, larvae may adopt a suite of strategies to ingress (infotaxis). (b) Longshore currents (u) in coastal waters may transport drifting larvae far from a ‘natal’ or proximate estuary such that they are unable to utilise STST (Selective Tidal Stream Transport) to ingress at the postflexion stage. (c) Directional swimming by larvae may be essential to ensure ingress to some estuaries. Larvae unable to ingress to a ‘natal’ or proximate estuary may still ingress and recruit, but to another estuary.

In demersal species, settlement for many estuarine fishes often signals the end of highly dispersive egg (for some) and larval stages and initiation of a more localised juvenile stage. In flatfishes, dramatic eye migration occurs (Figure 3.4), along with the ability to bury in the sediment, as seen in the paralichthyid Paralichthys dentatus (Keefe & Able 1993). Development during settlement warrants understanding because these important morphological, physiological and behavioural transitions occur while fishes are undergoing habitat transitions (Moser 1981, Balon 1984, Chambers et al. 1988, Youson 1988, Levin 1991, Kaufman et al. 1992), and the transition is potentially associated with an increased risk of mortality (Able & Fahay 2010). This transition, often coupled with metamorphosis to a juvenile morphology, is not unique for estuarine fishes but is a common mode of ontogeny in many demersal species (Espinel‐Velasco et al. 2018). Metamorphosing and settling juveniles of estuary‐dependent fishes may also face osmoregulation challenges upon entering lower‐salinity waters in estuaries (Whitfield 2019).

In pelagic species that do not settle and in demersal settlers, ontogenetic shifts experienced by transforming individuals may be accompanied by changing food habits. This is evident, for example, based on ontogeny of the feeding apparatus in post‐settlement individuals from three foraging guilds (pelagic, generalist and benthic) of sciaenid fishes (Figure 3.6) in Chesapeake Bay (Deary et al. 2017). This research demonstrated that ontogenetic, developmental changes in the jaw and sensory capabilities were accompanied by shifts in feeding in which larvae adopted very different feeding habits and foods at settlement (Deary et al. 2017). The ontogeny of head and jaw development in larvae of the closely related South African sciaenids Argyrosomus japonicus and A. inodorus differed in small ways, but resulted in species‐specific differences in feeding ability (Deary et al. 2015). Ontogenetic shifts in habitats occupied that represented areas with differing prey types and abundances were documented for postflexion larvae and juveniles of the pleuronectid Platichthys flesus in the Lima Estuary, Portugal (Amorim et al. 2016).

Figure 3.6 Illustration of ontogenetic diet shifts in early‐life‐history stages of sciaenid taxa from Chesapeake Bay, USA. Shifts are illustrated with respect to development of the feeding and sensory systems and with respect to transition from pelagic, pre‐settlement habitats to post‐settlement, early‐juvenile habitats. The larval lengths (SL) of the observed dietary shift for each foraging guild are noted over the arrows. Dominant prey types are represented but are not drawn to scale. The line drawings of the oral jaw structures are drawn to scale except for the generalist sciaenid larva illustration. Blue represents the water column and brown represents the benthos

(from Deary et al. 2017, their figure 7).

The coincidence between morphological and physiological transformation and settlement is evident in many temperate estuarine fishes, as well as estuarine species in the South Atlantic Bight of the USA (Hoss & Thayer 1993), the Gulf of Mexico (Yáñez‐Arancibia 1985), Spain (Arias & Drake 1990), South Africa (Day 1981, Beckley 1984, 1986) and Australia (West & King 1996). The typical ontogeny and associated behaviours, however, do not apply to all demersal species. For example, all Urophycis spp. (Phycidae) in the Middle Atlantic Bight of the Western Atlantic have a pelagic juvenile stage and they do not settle until they are older and larger (>23–80 mm) than most other species (Able & Fahay 1998). Others, such as the anadromous salmonids which spawn in freshwater, may use estuaries in their transition from freshwater to the ocean for days, weeks, months or years as parr or smolts, e.g. Oncorhynchus spp. and Salmo salar (Healey 1985, Thorpe 1994, Weitkamp et al. 2014, Levings 2016). Furthermore, the patterns of estuarine use by juvenile salmonids can vary within species and include variation amongst rivers and estuaries (Thorpe 1994, Levings 2016, Quinn 2018).

The culmination of the above developmental patterns influences the degree of estuary dependence in fishes, and thus potentially their survival. For example, in the western North Atlantic, estuary dependence is variable across a variety of scales for a large sample of estuarine fishes (Figure 3.7). Many of these species are obligate users, but the spectrum is broad and not all fishes ingressing into estuaries are dependent on these ecosystems for their growth and survival. In contrast to the above situation, most fish species ingressing into Australian and southern African estuaries use these systems ‘opportunistically’ (Potter et al. 1990). For those species that are dependent on estuaries as nursery areas, the supply of larvae, and sometimes juveniles, that enter estuaries can have a great influence on the numbers of individuals that survive to be reproducing adults.

Figure 3.7 Characterisation of degree of estuary dependence for representative estuarine fishes from the northeastern USA

(based on Able 2005).