Is Developmental Mode an Important Determinant of Dispersal Distance?

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Is developmental mode an important determinant of dispersal distance?

Marine benthic organisms dispersal ability is widely thought to influence species geographic range (Emlet, 1995), and species with greater potential for dispersal are expected to establish and maintain larger ranges than comparable species with more restricted dispersal capabilities (Lester and Ruttenberg, 2005). This potential has been viewed as the multifaceted consequences of variations in developmental mode, dispersing particle size and fecundity (Foggo et al., 2007), and is termed ‘propagule pressure’. Dispersal can also contribute to population rates of growth, gene flow and species persistence (Lowe and Allendorf, 2010). Therefore assessing the effects of dispersal is critical to our understanding of population biology and evolution in natural systems (Hanski et al., 1997, Wright, 1949). It should be noted here to avoid confusion between the concepts of dispersal and dispersion, that dispersal is a process, the movement of individuals from one place to another, whereas dispersion is the state, or pattern created by the dispersal of said individuals (Armstrong, 1977). Marine communities are comprised of taxa with hugely varied reproductive mechanisms (Grantham et al., 2003), and many marine invertebrates have biphasic life histories, meaning they often disperse as mobile planktonic larvae and then mature to a sedentary benthic existence as they progress into adulthood (Lester and Ruttenberg, 2005).

There are generally three main types of developmental strategy (or developmental mode) described in relation to the types of mechanism specific taxa employ whilst in the planktonic stage of development, they can be: (a) planktotrophic – larvae derive nutrition from outside (exogenic) sources, normally from predation of other planktonic taxa; (b) lecithotrophic – larvae feed off yolk from maternal provisioning for a least some of their time in the plankton (endogenic sources); (c) non-planktonic development – larvae either develop demersally, eggs are brooded maternally, or the species is viviparous – the young have developed inside the body of a parent (Rundle et al., 2007) (e.g. Nucella sp., Cerithideopsis sp.) . This simple grounds of division represents an over-generalization however (Poulin et al., 2001), for example, some planktotrophs develop feeding structures during their planktonic phase, commencing development from maternal provisioning (Miner et al., 2005) whilst others, in the case of some Echinoderms, are primarily lecithotrophic but become facultatively planktotrophic (Strathmann, 1987). These developmental modes can differ immensely in the duration of developmental period and/or time in the plankton itself.

Feeding larvae generally spend weeks to months in the plankton; nonfeeding, pelagic larvae spend hours to days; and nonpelagic larvae spend little or no time in the water column at all (Emlet, 1995, Grantham et al., 2003). These differing lengths of time spent in the water column therefore have the ability to influence geographic range. This may not be the case for all species though, and it does seem to depend on the species being focussed on. For example, free swimming invertebrate taxa with long planktonic durations are thought to have large geographic ranges. However for fishes, studies on several species showed a negative relationship between larval duration and geographic range when compared to other zooplankton, possibly due to self-recruitment (Lester and Ruttenberg, 2005).

The length of time spent in the plankton – the planktonic larval duration (PLD) has been put forward as a possible predictor of dispersal distance (Grantham et al., 2003). The longer an organisms PLD, the further the species should technically be able to disperse before requiring to settle. This dispersal potential in marine macroinvertebrates is primarily determined by the potential for passive movement as either adults or larvae (Bradbury and Snelgrove, 2001, Emlet, 1995). Planktotrophs tend to be the smallest in size, are produced in the highest numbers and tend to have the longest PLD – as such they should have the potential for the longest geographic range (Bradbury and Snelgrove, 2001, Emlet, 1995, Jeffery and Emlet, 2003, Paulay and Meyer, 2006). Lecithotrophs, however, tend to be smaller in adulthood, and have faster developing eggs that are larger, with an intermediate dispersal potential (Emlet, 1995, Strathmann, 1987). Non-planktonic larvae tend to be the smallest in adulthood and have the largest effective dispersing particle sizes. Planktonic larvae could buffer oscillations in populations, which may be a useful process to minimise extinctions on a local scale (Eckert, 2003, Emlet, 1995).

As a general rule, it appears that the dispersal range potential for marine invertebrates is planktotrophs > lecithotrophs > non-planktonic developers (Foggo et al., 2007). PLD is, however, taxon specific and as such can be influenced by temperature among other environmental factors, also, dispersal distance can be season, species and location specific as well (Cowen and Sponaugle, 2009). Actually quantifying this dispersal and connectivity is no mean feat however, due to the small size of larvae and huge and complex environment that is the world’s oceans (Cowen and Sponaugle, 2009). A recent study estimated dispersal distance across a large variety of organisms, this showed some larvae disperse only meters, with others dispersing more than 1000 km,  some fish species dispersed less  than 100 km, and less distance still for some coastal invertebrates and plants (Kinlan and Gaines, 2003). Available nutrients and water temperature play a pivotal role in dictating the PLD of some species (Houde, 1989, Pepin, 1991, Rombough, 1997). Production of offspring requires adults to be sufficiently healthy, and seasonal changes in water temperature and therefore productivity more often than not kick-start the production of young (Cowen and Sponaugle, 2009). These environmental conditions influence egg and therefore larval quality – and in turn larval survival (Berkeley et al., 2004, McCormick, 2006).

The effect of dispersal ability on geographic range has been hypothesized to either originate from an evolutionary perspective; where gene flow arising from dispersal affects rates of adaptation, speciation and extinction locally, or from an ecological perspective; where it is viewed as a life-history trait that influences demography and colonization (Lester et al., 2007). Although commonly suggested to play an important part in the influencing of species geographical ranges (Brown et al., 1996, Gaston, 1996), dispersal has not really been explained or evaluated (Lester et al., 2007). Lester et al., 2007 penned three main mechanistic hypotheses that could predict a positive dispersal ability range – size relationship. First the site colonisation hypothesis: where species with a dispersal ability that is limited may struggle to colonize or supply individuals to distant sites, regardless of the suitability of said sites (Wellington and Victor, 1989). Likewise, the dynamics of metapopulations (Hanski and Parmesan, 1999) could lead to limited dispersers having smaller ranges when they have lower rates of recolonization – and therefore a smaller number of equilibrium sites at the range margin (Lester et al., 2007). Whereas the metapopulation ‘rescue effect’ (Brown and Kodric-Brown, 1977), where immigration from ‘source’ populations maintain ‘sink’ populations that could go extinct. This could perhaps affect how far sink populations at ranges edges extend the overall range size (Lester et al., 2007). Secondarily the speciation rate hypothesis: where species with low dispersal abilities could suffer greater isolation and therefore lower gene flow among populations. This decreased gene flow could potentially increase the likelihood of adaptation locally, and therefore the probability of speciation (Hansen, 1980, Jablonski, 1986, Lester et al., 2007, Shuto, 1974). Therefore, higher rates of speciation could lead to smaller geographical ranges if the speciation process leads to a small starting range as the new species will not have had enough time to expand their geographic range (Hansen, 1980, Lester and Ruttenberg, 2005, Lester et al., 2007). Finally, the selection hypothesis: Species that have small geographical ranges could experience selection for decreasing dispersal, if there is no benefit to larger dispersal ranges, or if the cost outweighs the benefits at least (Gaston, 2003, Lester et al., 2007). Lester et al., 2007 analysed two data sets and revealed that in most cases the ability of an organism to disperse is of very little value when trying to predict range size. However, when interrogated at smaller scales (Lester and Ruttenberg, 2005), some tropical reef fishes dispersal ability is a driver of range size in the Indo-Pacific. Interestingly, they found that the species that have to disperse over significant barriers to dispersal have longer PLD’s than species who have ranges that do not (Lester and Ruttenberg, 2005, Lester et al., 2007).

So what factors other than developmental mode can influence dispersal and therefore geographic range in marine larvae? Many evolutionary and ecologically based explanations have been suggested, including niche breadth and environmental tolerance, latitude, body size, population abundance, environmental variability, colonization-extinction dynamics and dispersal ability to name a few (Brown et al., 1996, Gaston, 1996, Gaston, 2003, Stevens, 1989, Rundle et al., 2007). It certainly appears than a number of these factors have an influence on dispersal and geographic range at any one time (Berkeley et al., 2004, Brown et al., 1996, Byrne et al., 1999, Cowen and Sponaugle, 2009, Eckert, 2003, Emlet, 1995, Gaston, 1996, Rombough, 1997, Rundle et al., 2007, Shanks, 2009).

There is another interesting hypothesis that could certainly influence dispersal distance and therefore geographic range of marine larvae, known as the ‘Desperate Larvae Hypothesis’ (Elkin and Marshall, 2007). This hypothesis proposes that marine larvae are generally found in discrete patches that vary in quality, and taking into account that the larval stage in most invertebrate marine organisms disperses to find new habitat, they will generally try to settle in areas favourable to post-metamorphic performance (Walters et al., 1999). It also suggests that some marine organisms are found in habitat other than optimal for their post settlement success, possibly due to what they are sometimes willing, or are forced to accept (Elkin and Marshall, 2007, Raimondi and Keough, 1990). This could potentially be due to age, known as ‘decreasing selectivity’ (Elkin and Marshall, 2007, Gibson, 1995, Knight-Jones, 1951, Knight-Jones, 1953, Rumrill, 1989). The hypothesis further proposes that once the larvae has passed through the obligate phase of development and is competent to metamorphose (Elkin and Marshall, 2007), and moves into the facultative phase where it begins to encounter habitat and is competent to settle, that feeding larvae in the presence of local food availability could remain in the plankton longer until suitable cues for settlement are received, whereas non-feeding larvae that are larger (and therefore have more resources) have the ability to stay in the plankton longer before settling than their smaller counterparts.

Despite all the work that has been invested into understanding developmental mode in marine taxa thus far, it appears overall that habitat choice for individuals is complex, and that many factors both biotic and abiotic have an influence on geographic range when considering marine taxa with planktonic life histories. Accounting for developmental mode and its connection to demographic, ecological and macroevolutionary consequences has proved difficult for some time, and unpicking these factors to give a steady, consistent model for dispersal range in the future particularly with the ugly face of climate change looming, is an ongoing process and will probably (and unfortunately) continue well into the future.

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