Jeffrey M. Leis

Are larvae of demersal fishes plankton or nekton

A pelagic larval stage is found in nearly all demersal marine teleost fishes, and it is during this pelagic stage that the geographic scale of dispersal is determined. Marine biologists have long made a simplifying assumption that behaviour of larvae--with the possible exception of vertical distribution--has negligible influence on larval dispersal. Because advection by currents can take place over huge scales during a pelagic larval stage that typically lasts for several days to several weeks, this simplifying assumption leads to the conclusion that populations of marine demersal fishes operate over, and are connected over, similar huge scales. This conclusion has major implications for our perception of how marine fish populations operate and for our management of them. Recent (and some older) behavioural research-reviewed here-reveals that for a substantial portion of the pelagic larval stage of perciform fishes, the simplifying assumption is invalid. Near settlement, and for a considerable portion of the pelagic stage prior to that, larvae of many fish species are capable of swimming at speeds faster than mean ambient currents over long periods, travelling tens of kilometres. Only the smallest larvae of perciform fishes swim in an energetically costly viscous hydrodynamic environment (i.e., low Reynolds number). Vertical distribution is under strong behavioural control from the time of hatching, if not before, and can have a decisive, if indirect, influence on dispersal trajectories. Larvae of some species avoid currents by occupying the epibenthic boundary layer. Larvae are able to swim directionally in the pelagic environment, with some species apparently orientating relative to the sun and others to settlement sites. These abilities develop relatively early, and ontogenetic changes in orientation are seemingly common. Larvae of some species can use sound to navigate, and others can use odour to find settlement habitat, at least over small scales. Other senses may also be important to orientation. Larvae are highly aware of their environment and of potential predators, and some school during the pelagic larval stage. Larvae are selective about where they settle at both meso and micro scales, and settlement is strongly influenced by interactions with resident fishes. Most of these behaviours are flexible; for example, swimming speeds and depth may vary among locations, and speed may vary with swimming direction. In direct tests, these behaviours result in dispersal different from that predicted by currents alone. Work with both tropical and temperate species shows that these behaviours begin to be significant relatively early in larval development, but much more needs to be learned about the ontogeny of behaviour and sensory abilities in larvae of marine fishes. As a preliminary rule of thumb, behaviour must be taken into account in considerations of dispersal after the preflexion stage, and vertical distribution behaviour can influence dispersal from hatching. Larvae of perciform fishes are close to being planktonic at the start of the pelagic period and are clearly nektonic at its end, and for a substantial period prior to that. All these things differ among species. Larvae of clupeiform, gadiform and pleuronectiform fishes may be less capable behaviourally than perciform fishes, but this remains to be confirmed. Clearly, these behaviours, along with hydrography, must be included in modelling dispersal and retention and may provide explanations for recent demonstrations of self-recruitment in marine fish populations. Current work is directed at understanding the ontogeny of the gradual transition from planktonic to nektonic behaviour. Although it is clear that larvae of perciform fishes have the ability to strongly influence their dispersal trajectories, it is less clear whether or how these abilities are applied.

The biology, behavior, and ecology of the pelagic, larval stage of coral reef fishes

[Extract] Reef fish biologists are keenly aware that nearly all bony fishes on coral reefs have a pelagic larval phase that is potentially dispersive, and that this has major implications for reef fish populations not only at evolutionary (or biogeographic) scales, but also at ecological (or demographic, including management) scales. The literature is full of statements of how important this type of life history is for reef fishes, and for study and management of them. However, this realization has not been accompanied by a major shift in research effort to studying this pelagic phase, what one might refer to as “prerecruitment” studies. Neither has it led to a widespread view of the pelagic phase as much more than a “black box” that results in open populations and large fluctuations in recruitment. Even attempts to assess the population connectivity that presumably results from larval dispersal typically make simplifying assumptions, either explicitly or implicitly, that portray the larvae as little more than passive tracers of water movement that “go with the flow”, doing nothing much until they bump into a reef by chance and settle at once. Are larvae really as simple and as uninteresting as the assumptions made by this “black box” view of larval biology? We think not. The work reviewed here reveals larvae of coral reef fishes to have remarkably good swimming abilities, good sensory systems that develop early in ontogeny, and sophisticated behavior that is very flexible. Little of this would have been predicted from the much better known larval biology of temperate, non-reef species such as herring, cod, and plaice. We explore some of the reasons for this. The interaction of larval distributions with oceanography is the subject of Chapter 7 in the present volume, and we do not address that subject area. This chapter is not a revision of former work by Leis (1991a), nor does it cover ground already dealt with in reviews of coral reef fish larval biology by Boehlert (1996) and Cowen and Sponaugle (1997). Instead, here the focus is on recent research that examines reef fish larvae as animals interacting with their environment. The emphasis is on a perspective from the pelagic environment toward the demersal reef environment. The larvae have a similar perspective. Other studies take the opposite view, and indirectly examine the pelagic stage from the reef. These utilize information gleaned from otoliths of recruits or from abundance patterns either of settlement stage larvae captured by reef-edge light traps and reef-based nets, or of recruits on the reef (e.g., Dufour and Galzin, 1993; Milicich, 1994; Sponaugle and Cowen, 1994; Thorrold et al., 1994b,c; Robertson et al., 1999). Studies of this sort provide valuable insight, but they are largely beyond the scope of the present review. We review here new information on the pelagic stage, from spawning to settlement, including metamorphosis, but not postsettlement issues.

Climate change and coral reef connectivity

This review assesses and predicts the impacts that rapid climate change will have on population connectivity in coral reef ecosystems, using fishes as a model group. Increased ocean temperatures are expected to accelerate larval development, potentially leading to reduced pelagic durations and earlier reef-seeking behaviour. Depending on the spatial arrangement of reefs, the expectation would be a reduction in dispersal distances and the spatial scale of connectivity. Small increase in temperature might enhance the number of larvae surviving the pelagic phase, but larger increases are likely to reduce reproductive output and increase larval mortality. Changes to ocean currents could alter the dynamics of larval supply and changes to planktonic productivity could affect how many larvae survive the pelagic stage and their condition at settlement; however, these patterns are likely to vary greatly from place-to-place and projections of how oceanographic features will change in the future lack sufficient certainty and resolution to make robust predictions. Connectivity could also be compromised by the increased fragmentation of reef habitat due to the effects of coral bleaching and ocean acidification. Changes to the spatial and temporal scales of connectivity have implications for the management of coral reef ecosystems, especially the design and placement of marine-protected areas. The size and spacing of protected areas may need to be strategically adjusted if reserve networks are to retain their efficacy in the future.

How Nemo Finds Home: The Neuroecology of Dispersal and of Population Connectivity in Larvae of Marine Fishes

Nearly all demersal teleost marine fishes have pelagic larval stages lasting from several days to several weeks, during which time they are subject to dispersal. Fish larvae have considerable swimming abilities, and swim in an oriented manner in the sea. Thus, they can influence their dispersal and thereby, the connectivity of their populations. However, the sensory cues marine fish larvae use for orientation in the pelagic environment remain unclear. We review current understanding of these cues and how sensory abilities of larvae develop and are used to achieve orientation with particular emphasis on coral-reef fishes. The use of sound is best understood; it travels well underwater with little attenuation, and is current-independent but location-dependent, so species that primarily utilize sound for orientation will have location-dependent orientation. Larvae of many species and families can hear over a range of ~100-1000 Hz, and can distinguish among sounds. They can localize sources of sounds, but the means by which they do so is unclear. Larvae can hear during much of their pelagic larval phase, and ontogenetically, hearing sensitivity, and frequency range improve dramatically. Species differ in sensitivity to sound and in the rate of improvement in hearing during ontogeny. Due to large differences among-species within families, no significant differences in hearing sensitivity among families have been identified. Thus, distances over which larvae can detect a given sound vary among species and greatly increase ontogenetically. Olfactory cues are current-dependent and location-dependent, so species that primarily utilize olfactory cues will have location-dependent orientation, but must be able to swim upstream to locate sources of odor. Larvae can detect odors (e.g., predators, conspecifics), during most of their pelagic phase, and at least on small scales, can localize sources of odors in shallow water, although whether they can do this in pelagic environments is unknown. Little is known of the ontogeny of olfactory ability or the range over which larvae can localize sources of odors. Imprinting on an odor has been shown in one species of reef-fish. Celestial cues are current- and location-independent, so species that primarily utilize them will have location-independent orientation that can apply over broad scales. Use of sun compass or polarized light for orientation by fish larvae is implied by some behaviors, but has not been proven. Use of neither magnetic fields nor direction of waves for orientation has been shown in marine fish larvae. We highlight research priorities in this area.

Vertical and horizontal distribution of fish larvae near coral reefs at Lizard Island, Great Barrier Reef

Consistent patterns of horizontal distribution of fish larvae from plankton tows were found in shallow waters around Lizard Island, Great Barrier Reef during 1979 and 1980. Few types of larvae were most abundant in Lizard Lagoon, and none of these were old larvae. Forty percent of the 57 types of larvae studied differed in abundance between windward and downwind sides of the island. More types of old larvae were found in greatest abundance off the windward side of the island than the downwind side. Most types of larvae preferred deeper water (>3 m) during the day and moved upward at night, although a few types preferred upper (<3 m) or middle portions of the water column. These latter were more likely to descend at night or to maintain their day-time distribution than to move upward. Windward larvae [those more abundant off the windward (SE) side of the island] were more shallow-living than were downwind larvae, and were more likely to maintain their day-time distribution at night. The current patterns around Lizard Island were favourable for retention of larvae in both Lizard Lagoon and off the windward side of the island, if combined with certain vertical distributions of the larvae. However, while there was evidence for retention on the windward side of the island, there was no evidence for retention in Lizard Lagoon. Currents on the downwind side of the island were not favourable for retention of larvae and there was little evidence that larvae were retained there. Retention may be an accidental result of interaction between currents and larval behaviour, or the result of a strategy of retention by the larvae. These could not be distinguished in the present study.

Vertical distribution of fish larvae in the Great Barrier Reef Lagoon, Australia

The vertical distribution of shorefish — primarily reef fish — larvae in the upper 20 m in relatively shallow (<30 m) waters of the Great Barrier Reef Lagoon near Lizard Island was investigated from 27 February to 7 March 1983 during both day and night. Four strata were sampled by neuston net and opening/closing bongo net: neuston (0 to 0.1 m), upper (0 to 6 m), middle (6 to 13 m), and deep (13 to 20 m). Taxon-specific patterns of vertical distribution which changed little ontogenetically, were found for the 50 taxa (in 24 families) analysed. Vertical distribution was highly structured during the day, and with few exceptions was nearly unstructured at night. Most taxa had highest concentrations deep in the water column during the day, but in any given stratum some taxa had highest concentrations. Day/night changes in pattern apparently were due to randomization or spread, rather than active migration. Related taxa had similar patterns. Similarity analysis including 211 taxa produced three groupings of samples: day neuston; day upper/middle; and day deep plus all night samples. The sampling strategy of using drogues to tag water parcels for subsequent resampling was compared with one of sampling at a fixed point. The drogue strategy was not superior to the fixed-point strategy as measured by dissimilarity indices, but this may differ among strata.

Pacific coral-reef fishes: the implications of behaviour and ecology of larvae for biodiversity and conservation, and a reassessment of the open population paradigm

The two-phase life history of most marine fishes and invertebrates has enormous implications for dispersal, population connectivity, and resource management. Pelagic dispersal larvae of marine animals traditionally thought to ensure that populations are widespread, that chances of local extinction are low, and that marine protected areas (MPA) can easily function to replenish both their own populations and those of unprotected areas. Traditionally, dispersal is considered to depend primarily on two variables: pelagic larva duration and far-field currents. These conclusions arise from the ‘open population’ paradigm and are usually accompanied by a ‘simplifying assumption’: larvae are distributed passively by far-field currents. Unfortunately, they ignore the complex reality of circulation and hydrological connectivity of reefs, and do not consider newly-demonstrated behavioural capabilities of coral-reef fish larvae. Far-field circulation varies with depth and often excludes water bodies where propagules are released, and this has important implications for predicting trajectories of even passive larvae. However, larvae are not passive: late-stage larvae of coral-reef fishes can swim faster than currents for long periods, can probably detect reefs at some distance, and can actively find them. This behaviour is flexible, which greatly complicates modelling of larval fish trajectories. Populations at ecological (as opposed to evolutionary) scales are probably less open and more subdivided than previously assumed. All this means that dispersal predictions based solely on far-field water circulation are probably wrong. An emerging view of larval-fish dispersal is articulated that takes these new data and perspectives into account. This emerging view shows that re-evaluation of traditional views in several areas is required, including the contribution of larval-fish biology and dispersal to biodiversity patterns, the way reef fishes are managed, and the way in which MPA are thought to operate. At evolutionary and zoogeographic scales, reef-fish populations are best considered to be open.

Complex behaviour by coral-reef fish larvae in open-water and near-reef pelagic environments

We present the first in situ observations of the pelagic larvae of coral-reef fishes feeding, schooling and being preyed upon. In addition, we report on their behavioural interactions with adult and juvenile fishes. Observations on over 500 larvae of over 50 species (mostly from four families) near the end of their pelagic interval were made in both open water (> 1 km offshore) and near-reef environments. Nearly 10% of larvae were seen to feed in open water, but < 1% fed near the reef. Presettlement schooling was observed in five species of four families. We observed no predation upon larvae in open water except near the bottom. Near the reef, 8.5% of larvae were eaten. The main predators near and on the reef were a species of wrasse and lizardfishes. Rates of predation seem to differ among genera of pomacentrids, perhaps related to differences in behaviour when settling. When confronted with adult fishes, which happened largely near the reef, larvae reacted with a limited range of behaviours, including sheltering near the observer, swimming to the surface, slowing or stopping, or swimming offshore. The frequency of these behaviours differed among larvae of three pomacentrid genera. Interactions with reef residents, particularly pomacentrids, were common, and usually involved aggression by the resident toward settling larvae. This may act to discourage settlement during the day when such residents are active. These data show that behaviour of late larvae of coral-reef fishes is complex and can greatly influence survival and recruitment. Further, behaviour differs among taxa, showing that not only are larvae not passive, but also that a ‘generalised behaviour’ of larvae does not exist.

Currents in the Lizard Island region of the Great Barrier Reef Lagoon and their relevance to potential movements of larvae

Current data were collected at 3 stations in the Great Barrier Reef Lagoon of Australia between Lizard Island and Carter Reef, an outer ribbon reef, (approximately 14°S) over a 2 year period. During the southeast Trade wind season (March–September), net circulation at all stations was to the northwest, parallel to the coast and reefs, with little cross-shelf movement. This motion was periodic at about 20 days and highly coherent with the wind. During the non-Trade wind season (October–February) the net circulation depended on the variable wind regime and exhibited frequent current reversals and cross-shelf motion. Tidal currents were superimposed on the net circulation and were mainly cross-shelf but with a tidal excursion of only about 5 km on a flood tide. Tidal currents close to Carter Reef were not cross-shelf but remained parallel to the reef, suggesting that the major tidal flux is through the reef passages. Net circulation close to Carter Reef was not coherent with net circulation at the stations in more open waters, during both Trade and non-Trade seasons. Current speeds were typically 10–30 cm s-1. Passive plankters entering the water from Carter Reef are therefore likely to remain close to the outer ribbon reefs and be moved parallel to them. Based on the above, we predict that in the Trade wind season, passive plankters would be advected further from their point of origin than during the non-Trade wind season, but there would be more cross-shelf advection during the latter.

A preliminary distributional study of fish larvae near a ribbon coral reef in the Great Barrier Reef

Fish larvae from horizontal plankton tows along a single transect near outer ribbon reefs of the Great Barrier Reef in spring 1979 and summer 1980 had persistent distributional patterns. Larvae were identified to family and divided into young (preflexion) and old (postflexion) larvae, thus giving 28 taxa abundant enough for analysis. Non-uniform larval distributions were found for 81% of the 16 reef fish taxa with non-pelagic eggs, but for only 17% of the six reef fish taxa with pelagic eggs. Most differences in larval concentration were between the lagoonal and seaward sides of the reef. Only tripterygiid larvae had highest concentration just seaward of the reef, while larvae of 12 reef and three oceanic fish taxa occurred in highest concentrations on the lagoonal side of the reef. In five taxa of reef fishes, higher larval concentrations were found in the lagoonal backreef compared with the mid-lagoon habitat; but the reverse was not found in any taxon. Eleven taxa had indeterminate distributions, (i.e. no difference in concentration between stations). Mechanisms responsible for the distribution remain unknown, but we suggest that the view which considers fish larvae to be passively-drifting particles is unjustified without more information on larval behaviour.