Marine larval ecology

Marine larval ecology is the study of the factors influencing the dispersing larval stage which is exhibited by many marine invertebrates and fishes. Marine organisms with a larval stage usually release large numbers of larvae into the water column, where the larvae develop and grow for a certain period of time before metamorphosing into adults.

Many marine larvae are capable of dispersing long distances from their release site, although determining their actual dispersal distance is a significant challenge due to their microscopic size and the lack of an appropriate larval tracking method. Understanding dispersal distance, however, is important for a variety of reasons, including fisheries management, effective marine reserve design, and control of invasive species.

Theories on the evolution of a biphasic life history

Marine larval dispersal is one of the most important topics in marine ecology today. Most marine invertebrates and many fishes have evolved a life cycle involving a demersal adult and a pelagic larval stage or pelagic eggs that have the capacity to be transported long distances.[1] There are several theories behind why these organisms have evolved this biphasic life history:[2]

Pelagic larval dispersal, however, is not without its risks. For example, while larvae do avoid benthic predators, they are exposed to a whole new suite of predators in the water column.

Larval development strategies

Marine larval development can be broadly classified into three strategies: direct development, lecithotrophic, and planktotrophic.

Direct developers are characterized by a larval stage that has very low dispersal potential and usually looks like the adult form of the animal. These larvae are also known as “crawl-away larvae,” since numerous marine snails exhibit this type of development, and their larvae crawl away from the egg mass. Some species of frog also hatch this way.

Lecithotrophic larvae generally have greater dispersal potential than direct developers. Many fish species and some benthic invertebrates have lecithotrophic larvae, which are provided with a source of nutrition to use during their dispersal, usually a yolk sac. Though some lecithotrophic species are capable of feeding in the water column, many, such as tunicates, are not, and must settle before depleting their food source. Consequently, these species have short pelagic larval durations and do not disperse long distances.

Planktotrophic species, on the other hand, generally have fairly long pelagic larval durations and feed while in the water column. Consequentially, they have the potential to disperse long distances. This ability to disperse is one of the key adaptations of benthic marine invertebrates.[3] During their time in the water column, planktotrophic larvae feed on phytoplankton and small zooplankton, including other larvae. Planktotrophic development is the most common type of larval development, especially among benthic invertebrates.

The relatively long time most planktotrophic larvae spend in the water column and their apparently low probability of successful recruitment led some early researchers to develop a “lottery hypothesis” that states animals release huge numbers of larvae to increase the chances that at least one will survive, and that larvae cannot influence their probability of success.[4][5][6] This hypothesis, though, views larval survival and successful recruitment as chance events, and numerous studies on larval behavior and ecology have shown this to be false.[7] Though it has been generally disproved, the larval lottery hypothesis does represent an important understanding of the difficulties faced by larvae during their time in the water column, particularly because it recognizes the low probability of larval survival.

All three marine larval strategies face two major problems: avoiding predation and finding an appropriate site to settle.

Predator avoidance

One of the major difficulties faced by larvae is the threat of predation. Larvae are small and plentiful, so many animals take advantage of this food source. The situation is particularly dangerous for invertebrate larvae in estuaries; estuaries are nursery grounds for planktivorous fishes. Estuarine species’ larvae have evolved strategies to cope with this threat, including methods such as direct defense and avoidance. Direct defense is usually only evident in species in which larval development takes place entirely within the estuary. Studies have shown that larvae that do not leave estuaries are larger than larvae that develop in the open ocean. Additionally, many estuarine larvae have large spines and other protective structures. These defenses work because most planktivorous fishes are gape-limited predators—what they eat is determined by how wide they can open their mouths—so larger larvae are harder for them to ingest. Morgan showed that spines do indeed serve a protective function by cutting off spines of some estuarine crab larvae and monitoring differences in predation rates between despined and intact larvae.[8] Despined larvae suffered significantly higher predation rates than intact larvae, and were preferentially chosen during feeding trials with both types of larvae present. Additionally, Morgan showed that large-spined estuarine larvae usually keep their lateral spines relaxed, but raise them when approached by a predator. Therefore, predator deterrence in estuarine larvae is not only morphological but also behavioral.

A second strategy to deal with estuarine predators is to avoid them on small or large spatial scales. Some larvae do this at a small scale by simply sinking when approached by a predator. However, a more common avoidance strategy is to become active at night and remain hidden during the day, since most fishes are visual predators and need light to hunt. This strategy is not only evident in estuaries, but is also the main predator-avoidance strategy in the open ocean, since the water column lacks topography and thus hiding places. Most pelagic larvae and other planktonic species undertake diel vertical migrations between deeper waters with less light and fewer predators during the day and shallow waters in the photic zone at night, where their microalgal food source lives. By retreating to areas of low light during the day, marine larvae (and other zooplankton) can significantly decrease their risk of predation.[9] On a larger scale, most estuarine invertebrate larvae avoid predators by leaving the estuary and developing in the open ocean, which has fewer planktivorous fishes. The most common strategy for leaving an estuary is reverse tidal vertical migrations. In this strategy, larvae use the tidal cycle and estuarine flow regimes to aid their departure to the ocean, a process that is well-studied in many estuarine crab species.[10][11][12][13]

The process of reverse tidal vertical migrations begins when female crabs release larvae on a nocturnal spring high tide in an attempt to limit predation by planktivorous fishes. As the tide begins to ebb, larvae swim to the surface waters and are carried away from their site of hatching towards the ocean. When the tide reaches its low and begins to flood, larvae swim towards the bottom of the estuary, where water moves more slowly due to the boundary layer. This prevents them from being sloshed back and forth within the estuary in the surface waters. When the tide again changes back to ebb, the larvae swim to the surface waters and resume their journey to the ocean. Depending on the length of the estuary and the speed of the currents, this process can take anywhere from one tidal cycle to several days.[14]

Dispersal and settlement

Probably the most widely accepted theory explaining the evolution of a larval stage is the need for long-distance dispersal ability. Sessile organisms such as barnacles and tunicates, as well as sedentary species like mussels and crabs, need some mechanism to move their young into new territory, since they cannot move long distances as adults. Many species have relatively long pelagic larval durations—the amount of time a larva is in the water column before it is competent to settle—on the order of weeks or months.[15][16] During this time in the water, larvae feed and grow, and many species move through several stages of development. For example, most barnacles molt through six naupliar stages before molting to a cyprid, the stage at which they seek an appropriate settlement substrate. This allows the larvae to use different food resources than the adults and gives them time to disperse.

This strategy, however, involves a certain degree of risk. While some larvae have been shown to be able to delay their final metamorphosis for a few days or weeks, few if any species are able to delay metamorphosis indefinitely, and most species cannot delay it at all.[17][18] If these larvae metamorphose too far from a suitable settlement site, they perish. Due to the imperative of finding a suitable settlement site within a certain timeframe, many invertebrate larvae have evolved complex behaviors and endogenous rhythms to ensure their successful and timely settlement, which will be explained below.

Many estuarine species exhibit swimming rhythms of reverse tidal vertical migration to aid in their transport away from their hatching site, however, the same species can exhibit tidal vertical migrations to reenter the estuary when they metamorphose and are competent to settle.[19] This process is similar to the reverse tidal vertical migrations described in the section discussing predator avoidance above, but instead of swimming down on flood tide, settlers remain in the surface waters, allowing themselves to be transported into the estuary.

Another change that many larvae undergo after they reach their final pelagic stage is to become much more tactile, clinging to anything larger than themselves. For example, Shanks observed crab postlarvae in the lab and found that they would swim vigorously until they encountered a floating object.[20] Postlarvae would then cling to the object for the duration of the experiment. Shanks hypothesized that by clinging to floating debris, crabs can be transported towards shore due to the oceanographic forces of internal waves, which carry floating debris shoreward regardless of the prevailing currents.

If they are able to successfully return to shore, settlers encounter a new suite of problems concerning their actual settlement and successful recruitment into the population. Space is a limiting factor for sessile invertebrates on rocky shores, and larvae might not find any open habitat. Additionally, settlers must be wary of adult filter feeders, which usually cover the rocks at settlement sites and eat particles the size of larvae. Settlers must also avoid becoming stranded out of water by waves, and must select a settlement site at the proper tidal height to prevent desiccation and avoid competition and predation. To overcome many of these difficulties, some species rely on chemical cues to assist them in selecting an appropriate settlement site. These cues are usually emitted by adult conspecifics, but some species cue on specific bacterial mats or other qualities of the substrate.[21][22][23]

Much of current research is focused on how larvae, especially larval fish, navigate in the pelagic zone and ultimately find a place to settle. While larvae are very tiny and have limited complexity, they actually have very active and useful sensory systems. Fish can hear a range from about 100 to 1000 Hz and the ear is developed within the first two days of larval life. Sound is a useful tool for larvae because the ocean is not a quiet place. Coral reefs, for example, are quite noisy and likely provide a large stimulus for larvae looking to settle there. Olfaction, or the sense of smell, is also used by larvae, but on a smaller scale. Chemical signals that are detected through olfaciton have a limited lifetime in the ocean and do not travel long distances. Vision is used by larvae in two ways. The first is what is commonly thought of as vision, observing the immediate surroundings. This is useful for larvae in predator avoidance and prey detection but the limited visibility in some oceans and the small scale do not make this a useful tool for finding a settlement site. Studies have found that fish can detect polarized light and this is used to orient themselves in the water and can direct larval to settlement regions as a solar compass.[24] It is likely that larvae use a combination of all these sensory systems when locating settlement sites. Although these sensory systems exist in larvae, they are highly reduced. Upon settlement or metamorphosis, there is large development in the sensitivity and proliferation of these systems. Understanding how larvae navigate the ocean has very useful implications for managing fisheries and marine protected areas.

Self-recruitment

One of the most important unanswered questions in larval ecology concerns the degree of self-recruitment in populations. For most of the short history of the field of larval ecology, larvae were considered to be passive particles that were carried by ocean currents to locations far from their site of hatching. This led to the belief that all marine populations were demographically open, connected by long distance larval transport. Recent work, however, is starting to show that many populations may be self-recruiting, and that larvae and juveniles are capable of purposefully returning to their natal sites.

Researchers take a variety of approaches to estimating population connectivity and self-recruitment, and several studies have demonstrated their feasibility. Jones et al.[25] and Swearer et al.,[26] for example, both investigated the proportion of [reef fish] larvae returning to their natal reef after their time in the water column. Each study found higher than expected (possibly as high as 60%) self-recruitment in these populations, using variations of a typical mark, release, recapture sampling design. These studies were the first to provide conclusive evidence of self-recruitment in a species with the potential to disperse far from its natal site, and laid the groundwork for numerous future studies.[27]

Conservation

Ichthyoplankton, or fish larvae, have a 99% mortality rate as they transition from their yolk sac to zooplankton as their food source. This was first described by Johan Hjort in 1914 as a “critical period” a few days after first-feeding. While the cause of this is still under debate, it has been proposed that this mortality rate is related both to inadequate zooplankton (food source) density as well as an inability to move through the water effectively at this early stage in development. Compounded together, these factors lead to starvation for the mass majority of first-feeding fish who have avoided predation. Ichthyoplankton use suction to feed and the turgidity of their water environment impairs the organisms’ ability to feed even when there is a high density of prey. Reducing these hydrodynamic constraints on cultivated populations could lead to higher yields for repopulation efforts and has been proposed as a means of conserving fish populations by acting at the larval level.[28]

A network of marine reserves (see marine protected area) has been initiated for the conservation of the world’s marine larval populations. These areas restrict fishing and therefore increase the number of otherwise fished species. This leads to a healthier ecosystem and affects the number of overall species within the reserve as compared to nearby fished areas; however, the full effect of an increase in larger predator fish on larval populations is not currently known. Also, the potential for utilizing the motility of fish larvae to repopulate the water surrounding the reserve is not fully understood. Marine reserves are a part of a growing conservation effort to combat overfishing; however, reserves still only comprise about 1% of the world’s oceans. These reserves are also not protected from other human-derived threats, such as chemical pollutants, so they cannot be the only method of conservation without certain levels of protection for the water around them as well.[29]

In order to effectively conserve the number of fish species, it is important to understand the larval dispersal patterns of the fish that are in danger, as well as the dispersal of invasive species which could impact the numbers of those species which are desirable for humans. Dispersal patterns can range from a few meters in one species to thousands of kilometers in another species. Understanding these patterns is an important factor when setting up protocol for governing fishing and creating reserves, but the data on threatened, over-fished, and invasive species is limited. Additionally, a single species may have multiple dispersal patterns. The spacing and size of marine reserves must reflect this variability in order to maximize their beneficial effect. The species with shorter dispersal patterns are more likely to be affected by local changes such as habitat disruption and global warming effects. These species would require higher levels of conservational priority because they are separated from other subpopulations and chance of extinction is higher in their situation.[30]

Implications

The principles of marine larval ecology can be applied to a number of fields both inside and outside the marine realm. Successful fisheries management relies heavily on understanding population connectivity and dispersal distances, and these processes are driven by larvae. Dispersal and connectivity must also be considered when designing natural reserves, both on land and in the water; if populations are not self-recruiting, then solitary reserves may lose their species assemblages. Additionally, many invasive species are able to disperse long distances during an early life stage, such as seeds in land plants or larvae in marine invasives. Understanding the factors influencing their dispersal is key to controlling their spread and managing already established populations. Through the continued study of the ecology of these microscopic creatures, scientists can better understand and more effectively manage myriad populations of both land and sea.

See also

References

  1. ↑ Grosberg, R.K. and D.R. Levitan. 1992. For adults only? Supply-side ecology and the history of larval biology. Trends Ecol. Evol. 7: 130-133.
  2. ↑ Swearer, S. E., J. S. Shima, M. E. Hellberg, S. R. Thorrold, G. P. Jones, D. R. Robertson, S. G. Morgan, K. A. Selkoe, G. M. Ruiz, and R. R. Warner. 2002. Evidence of self-recruitment in demersal marine populations. Bull. Mar. Sci. 70(1) Suppl.: 251-271.
  3. ↑ Strathmann, R. R., T. P. Hughes, A. M. Kuris, K. C. Lindeman, S. G. Morgan, J. M. Pandolfi, and R. R. Warner. 2002. Evolution of local recruitment and its consequences for marine populations. Bull. Mar. Sci. 70(1) Suppl.: 377-396.
  4. ↑ Thorson, G. 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev. Cambridge Philos. Soc. 25: 1-45.
  5. ↑ Roughgarden, J., Y. Iwasa, and C. Blaxter. 1985. Demographic theory for an open population with space-limited recruitment. Ecology 66: 54-67.
  6. ↑ Caley, M.J., M.H. Carr, M.A. Hixon, T.P. Hughes, G.P. Jones, and B. Menge. 1996. Recruitment and the local dynamics of open marine populations. Evolution 35: 1192-1205.
  7. ↑ Kingsford, M. J., J. M. Leis, A. Shanks, K. C. Lindeman, S. G. Morgan, and J. Pineda. 2002. Sensory environments, larval abilities, and local self-recruitment. Bull. Mar. Sci. 70(1) Suppl.: 309-340.
  8. ↑ Morgan, S. G. 1989. Adaptive significance of spination in estuarine crab zoeae. Ecology 70: 462-482.
  9. ↑ Zaret, T.M. and J.S. Suffern. 1976. Vertical migration in zooplankton as a predator avoidance. Limnol. Oceanogr. 21: 804-813.
  10. ↑ Cronin, T.W. and R.B. Forward, Jr. 1979. Tidal vertical migration: An endogenous rhythm in estuarine crab larvae. Science 205: 1020-1022.
  11. ↑ Tankersley, R.A. and R.B. Forward, Jr. 1994. Endogenous swimming rhythms in estuarine crab megalopae: implications for flood-tide transport. Mar. Biol. 118: 415-423.
  12. ↑ Zeng, C. and E. Naylor. 1996. Endogenous tidal rhythms of vertical migration in field collected zoea-1 larvae of the shore crab Carcinus maenas: implications for ebb-tide offshore dispersal. Mar. Ecol. Prog. Ser. 132: 71-82.
  13. ↑ DiBacco, C., D. Sutton, and L. McConnico. 2001. Vertical migration behavior and horizontal distribution of brachyuran larvae in a low-inflow estuary: implications for bay-ocean exchange. Mar. Ecol. Prog. Ser. 217: 191-206.
  14. ↑ Forward, R.B. Jr, and R.A. Tankersley. 2001. Selective tidal-stream transport of marine animals. Oceanogr. Mar. Biol. Annu. Rev. 39: 305-353.
  15. ↑ Brothers, E.B., D.M. Williams, and P.F. Sale. 1983. Length of larval life in twelve families of fishes at “One Tree Lagoon,” Great Barrier Reef, Australia. Mar. Biol. 76: 319-324.
  16. ↑ Scheltema, R.S. 1986. On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. Bull. Mar. Sci. 39: 290-322.
  17. ↑ Gebauer, P., K. Paschke, and K. Anger. 2004. Stimulation of metamorphosis in an estuarine crab, Chasmagnathus granulata (Dana, 1851): temporal window of cue receptivity. J. Exp. Mar. Biol. Ecol. 311: 25-36.
  18. ↑ Goldstein, J.S., M.J. Butler IV, and H. Matsuda. 2006. Investigations into some early-life history strategies for Caribbean spiny lobster and implications for pan-carib connectivity. J. Shellfish Res. 25: 731.
  19. ↑ Christy, J.H. and S.G. Morgan. 1998. Estuarine immigration by crab postlarvae: mechanisms, reliability and adaptive significance. Mar. Ecol. Prog. Ser. 174: 51-65.
  20. ↑ Shanks, Alan L. 1985. Behavioral basis of internal-wave-induced shoreward transport of megalopae of the crab Pachygrapsus crassipes. Marine Ecol. Prog. Series 24: 289-295.
  21. ↑ Crisp, D.J. and P.S. Meadows. 1962. The chemical basis of gregariousness in cirripedes. Proc. Roy. Soc. Lond. B158: 364-387.
  22. ↑ Pawlik, J.R. 1986. Chemical induction of larval settlement and metamorphosis in the reef building tube worm; Phragmatopoma californica (Sabellidae: Polychaeta). Mar. Biol. 91: 51-68.
  23. ↑ Elliott, J.K., J.M. Elliott, and R.N. Mariscal. 1995. Host selection, location, and association behaviors of anemonefishes in field settlement experiments. Mar. Biol. 122: 377-390.
  24. ↑ Leis, J., Siebeck, U., and Dixson, Q. 2011. How Nemo Finds Home: The Neuroecology of Dispersal and of Population Connectivity in Larvae of Marine Fishes. Integr Comp Biol. 51: 826-843.
  25. ↑ Jones, G. P., M. J. Milicich, M. J. Emslie and C. Lunow. 1999. Self-recruitment in a coral reef fish population. Nature 402: 802-804.
  26. ↑ Swearer, S. E., J. E. Caselle, D. W. Lea, and R. R. Warner. 1999. Larval rentention and recruitment in an island population of a coral-reef fish. Nature 402: 799-802.
  27. ↑ Levin, L. 2006. Recent progress in understanding larval dispersal: new directions and digressions. Int. Comp. Biol. 46: 282-297.
  28. ↑ China, V., and R. Holzman. 2014. Hydrodynamic starvation in first-feeding larval fishes. PNAS doi:10.1073/pnas.1323205111.
  29. ↑ Bohnsack, J. A. 1992. Reef resource habitat protection: the forgotten factor. Marine Recreational Fisheries 14: 117-129.
  30. ↑ Jones, G. P., M. Srinivasan, and G. R. Almany. 2007. Conservation of marine biodiversity. Oceanography 20: 100-111.
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