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Integrative and Comparative Biology Integrative and Comparative Biology, volume 52, number 4, pp. 447–457 doi:10.1093/icb/ics040 Society for Integrative and Comparative Biology SYMPOSIUM Dispersal in Marine Organisms without a Pelagic Larval Phase Judith E. Winston1 Research and Collections Division, Virginia Museum of Natural History, 21 Starling Avenue, Martinsville, VA 24112, USA From the symposium ‘‘Dispersal of Marine Organisms’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2012 at Charleston, South Carolina. 1 E-mail: [email protected] Synopsis In contrast to marine organisms whose offspring go through an extended planktonic stage, the young of others develop directly into benthic juveniles or into yolky nonfeeding larvae that spend only a few hours in the plankton before settling. Yet, paradoxically, many such species have geographic distributions that are comparable to those with a pelagic dispersal stage. This article reviews some of the ways in which these organisms can expand their distributions: drifting, rafting, hitchhiking, creeping, and hopping. Drifting applies to species in which larvae may be short-lived, but adults can detach or be detached from their benthic substratum and be passively carried to new areas, floating at the water’s surface or below it. Many encrusting species and mobile species can spread by rafting, settling on natural or artificial floating substrata which are propelled by wind and currents to new regions. Hitchhiking applies to those attaching to vessels or being carried in ballast water of ships to a distant region in which their offspring can survive. Other marine species extend their distributions by hopping from one island of hard substratum or favorable sedimentary microhabitat to another, while creeping species extend their distributions along shores or shelves where habitats remain similar for long distances. Introduction This review considers organisms that are either aplanic, having no planktonic life stage, or anchiplanic, spending only a few hours to a few days in the plankton (according to the classification of Levin and Bridges [1995]). The site of their development may be planktonic, demersal, or benthic. They may be internally or externally brooded by parents or they may develop apart from the parent in either a free or encapsulated form. For all of them long-distance dispersal is very much a sweepstakes event, but given enough propagules and enough time, there will be some lucky winners of the dispersal sweepstakes. These organisms include members of almost every major taxonomic group, but this review is limited to plants and invertebrates. The most complete list of taxa recorded from sweepstakes routes is found in the review by Thiel and Gutow (2005b). They recorded 1205 species: cyanobacteria, protists, unicellular algae, macroalgae, invertebrates from most marine phyla. All feeding types were represented and for most species, distribution by means of floating substrata was facultative rather than obligate. The most common groups of organisms encountered were hydrozoans, bryozoans, crustaceans, and gastropods. Modes of dispersal Autonomous drifting In this mode of dispersal benthic propagules, spores, or larvae may be short-lived, but the much longerlived benthic adults can detach (or be detached) from the bottom and drift or be moved by wind and waves at the water’s surface or by currents along the sea floor, to a new area. Plants, algae, and benthic clonal or colonial invertebrates are best equipped to take advantage of this method, as they produce new individuals by both sexual and asexual reproduction. Fragmentation of large genets may result in many smaller fragments capable of drifting to new areas and attaching there. We have learned something about fragmentation in algae and macrophytes because of studies on both undesirable invasive species such as the alga Caulerpa taxifolia and desirable native species such as eelgrass, Zostera marina. Advanced Access publication April 13, 2012 ß The Author 2012. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. 448 Smith and Walters (1999) found C. taxifolia was much better at regenerating from apical fragments (down to 10 mm in length) than were the two other species of Caulerpa found in Hawaii. A management plan that involved breaking the alga into fragments would be doomed to increase the species abundance and range, instead of controlling it. C. taxifolia has all the characteristics of a good invader, including the ability to survive fragmentation, disperse widely, and reattach successfully in a short amount of time (Smith and Walters 1999). Its congener, Caulerpa racemosa, has also spread by fragmentation, drift, and re-attachment from its original introduction into the Mediterranean (Ceccherelli and Piazzi 2001). Both species have had a great effect on the native communities in the Mediterranean, particularly on beds of the native sea grass, Posidonia marina, already stressed by other factors, such as pollution (OcchipintiAmbrogi 2007). Grazers are limited. One ascoglossan molluscan grazer of a related species, Caulerpa prolifera, has been observed in Croatia to adapt to feeding on C. taxifolia (Žuljevic et al. 2001). However, instead of destroying the fronds, the sea slug Lobigera serradifalci fragments them into small pieces, each of which can then grow into a new plant. On the other hand, detached fragments of plants may be important in restoring a community. Harwell and Orth (2002) found detached, floating reproductive shoots of eelgrass could remain positively buoyant for up to 2 weeks. They recovered reproductive fragments with viable seeds up to 34 km from the nearest natural beds. In the Chesapeake Bay one of these fragments could be moved up to 23 km in a 6-h tidal window, indicating that this species has the capability to recolonize all suitable unvegetated habitat. Some colonial invertebrates also have the capability of dispersing via fragmentation. Large diskshaped colonies of the Brazilian cupuladriid bryozoan Discoporella umbellata form subcolonies that project from the edges of the parent colony in a very regular fashion (Marcus and Marcus 1962). These subcolonies eventually detach or are broken off, and grow into separate, but genetically alike colonies. Although the colonies use synchronized movements of vibracula (zooid polymorphs with opercula modified into bristles) to extricate themselves from sand or to raise themselves up to feed, they are powerless against major storm-induced or current-induced movements of the subtidal J. E. Winston sediments on which they live. Subcolonies can end up some distance from the parental location. In Antarctic waters, a colonial ascidian, Distaplia cylindrica, begins life on the bottom. In early development, colonies are encrusting. As they grow they develop into long narrow cylinders that frequently break off the substratum and float at the sea surface (McClintock et al. 2004). Since mature colonies contain male and female zooids and larvae (Tatián et al. 2005), even if the floating parental colonies eventually die, the larvae may settle in a new area. An Antarctic bryozoan, Alcyonidium pelagosphaera, has small (2 cm) hollow, brown spherical colonies that have been found floating on the surface of the sea. The species was first collected in 1992 (Peck et al. 1995), but was described as a new species even more recently (Porter and Hayward 2004) on the basis of molecular and morphological study. The few times colonies have been sighted, floating in the current past the RRS Bransfield while it was moored in the Weddell Sea (Peck et al. 1995), and noted by Sir Alister Hardy in the 1920s (Ryland 1996), large numbers of colonies were seen, but so far nothing more of the species life history is known. Some hydroids also possess the ability to disperse by fragmentation and subsequent survival of nonmedusan propagules of different sizes and types. Clytia viridicans can produce photosynthetic planulae that develop into floating colonies that later settle on the bottom (Pagliara et al. 2000). Other asexual means of dispersal found in hydroids include accidentally fragmented colonies, asexually produced planula-like buds, frustules, free hydranths, medusae, and by fission, frustules, stolonization, autotomized hydranths, and scissiparous medusae. For example, small Indian Ocean thecate hydroid Zelounies estrambordi hydranths autotomize and become planktonic, then settle and develop into a new benthic colony (Gravier-Bonnet 1992). Rafting Many groups of marine organisms can complete their life cycles on floating substrata during which time the currents may have carried them thousands of kilometers. The rafts that support them may be biotic (floating macroalgae, sea grass, wood, mangrove propagules, and sea beans) or abiotic (pumice, or floating anthropogenic debris, especially plastic). Thorough reviews of rafting organisms and their substrata were recently produced by Thiel and Gutow (2005a, b) and Thiel and Haye (2006). The authors 449 Nonpelagic dispersal modes listed 1205 species of marine and terrestrial organisms that have been recorded from floating substrata. The groups listed included most marine invertebrate phyla, as well as members of some terrestrial phyla, and even a few terrestrial vertebrates. They also included cyanobacteria, algae, macrophytes, and protists. A few rafters, e.g. some members of the pelagic sargasso fauna, are obligate, and for those in particular, cryptic coloration is important. However, most rafters are facultative—normally benthic or terrestrial organisms. Those for whom rafting is potentially important for dispersal usually share several features: small size, ability to attach to the raft and to establish and compete successfully on it, ability to develop persistent populations as the raft travels, and ability to colonize the destination reached by the raft In general, small organisms are better candidates for dispersal by rafting, as are substratum generalists and food generalists. Successful rafting organisms are often clonal, growing by asexual budding, but also reproducing sexually. Typically, the sexual reproduction of rafters features internal fertilization, brooding or laying of egg masses, and settlement close to the parent (Thiel and Gutow 2005a, b). Biotic substrata Rafters can be divided into those taxa that are more successful on biotic (chiefly macroalgal) rafts and those that are best at colonizing abiotic floating substrata. Mobile organisms are more often found on macroalgal rafts than on abiotic rafts. Algal rafts often start their journey with their original inhabitants from their subtidal attached period; some of which later become lost. Additional species may colonize over time. Macroalgal rafts are also populated by a larger number of species with direct development and by species that feed on their substratum (Thiel and Gutow 2005a, b). Gutow and Franke (2003) studied the neustonic amphipod Idotea metallica, a species that inhabits floating patches of debris or algae. The authors sampled in the Mediterranean, Atlantic Ocean, and North Sea, as well as carrying out experiments in the laboratory. They found that rafting populations persisted when the rafts were in open water, but were extirpated in coastal regions because of competition from other isopods and more rapid destruction of patches. Once away from shore, populations on such algal patches are capable of travelling in the currents to colonize new areas (Gutow 2003). This ability was recently demonstrated in New Zealand where the barnacle fauna of encrusted bull-kelp rafts and the kelp itself both were determined by molecular genetics methods to have come from subantarctic islands many kilometers distant and which would have required between 20 and 65 days of drift to travel that far (Fraser et al. 2011). Abiotic substrata In contrast to the situation on biotic substrata, abiotic substrata are not fed upon by their rafters. They may be broken down eventually by the action of sun and waves, but they have a longer life span in general (Thiel and Gutow 2005b, Bravo et al. 2011). Some abiotic substrata have potentially multi-year life spans: these substrata include volcanic pumice clasts, plastic objects, tar lumps, and sea beans (which although they are biotic, do not provide food, or provide very little). Suspension feeders, particularly sessile and/or colonial species, are the most successful organisms on abiotic substrata. Rafting of organisms on pumice has been reported from several areas. In the Caribbean, Donovan (1999) documented the rafting of lepadomorph barnacles on pumice produced by a volcano in Montserrat to the south coast of Jamaica. The pumice clast had mature barnacles on its surface as well as young individuals attached in its crevices. In the Indo-Pacific, Jokiel (1990) pointed out that corals could be transported to the Great Barrier Reef from areas further east on pumice from eruptions in the Tonga-Kermadec area. He speculated that present-day areas of high species diversity might be areas of species accumulation rather than of species origin. A large amount of sea-rafted pumice from a submarine volcanic explosion in Tonga was stranded on eastern Australian shores a year later, carrying algae, serpulids, bryozoans, coral, oysters, and gastropods (Bryan et al. 2004). From this Australian study, the following conclusions are most significant for the dispersal of marine organisms by rafting: (1) even a small submarine volcanic event can produce billions of rafts, (2) rafts can travel thousands of kilometers and last more than a year at sea, and (3) once beached, evidence of the event disappears very rapidly as the pumice clasts are buried or abraded. Plastic debris and tar balls are anthropogenic rafts. Biologists may deplore the ever-increasing presence of plastic in the oceans (the eastern and western Pacific trash gyres [90% plastic] comprise the biggest 450 ‘‘landfill’’ site in the world), but for sessile, calcified invertebrates in particular, floating plastic debris offers progressively increasing habitat (Winston et al. 1997; Gregory 2009; Hoeksema et al. 2012). On plastic rafts, sessile organisms are the most abundant inhabitants. Their lifestyle has some disadvantages; they cannot change their position if the raft tips over (Bravo et al. 2011) or leave it if it either starts to sink or grounds on a new shore, but there are advantages as well. Solitary organisms with hard shells, especially serpulid polychaetes, gastropod mollusks, and both acorn and stalked barnacles do well on abiotic rafts, but 20% of the rafting taxa reported in Thiel and Gutow’s (2005b) review belong to colonial groups. Colonial organisms can grow to sexual maturity and brood embryos during their raft’s voyage. Each colony that reaches a new region represents a potential founder population. Those colonial species with hard skeletons, some foraminiferans, and invertebrates, including bryozoans and scleractinian corals as well as some hydrozoan corals, may have an even greater advantage because of their ability to resist abrasion, predation, and grazing during the voyage. In Caribbean and Floridian waters, the calcareous multi-chambered foraminiferan Planorbulina acervalis is one of the first species to settle on plastic drift items. Settlement by foraminferans is usually followed by settlement by encrusting bryozoans. Other common encrusters are hydroids, tubeworms, filamentous algae, barnacles, and mollusks. Bryozoans are the champions in terms of species diversity. As would be expected, the two species with pelagic cyphonautes larvae, Electra tenella, and Jellyella tuberculata, were most abundant, but 23 brooding species with yolky nonfeeding embryos were also found (Winston et al. 1997). On the east coast of Florida much of the debris washed ashore has a Caribbean origin, but the amount of material of domestic versus Caribbean sources varies with season, even though storms strong enough to carry drift from the Gulf Stream onto Floridian beaches can occur at any season. Rapid transport occurs in autumn when beached drift items are a mixture of domestic and Caribbean objects, many of them still unencrusted or encrusted only by foraminiferans and filamentous algae. At other times of year, colonial forms dominate and objects are encrusted more densely and by a greater variety of organisms, suggesting a longer period of drift. J. E. Winston Some brooding bryozoans, like the Brazilian species, Thalamoporella evelinae, have so far been found in Florida only on drift plastic and have not been seen invading the shoreline (Winston et al. 1997). Another common Caribbean and South Floridian bryozoan, Schizoporella pungens, was not known from the Indian River area when the above drift-plastic studies were carried out. It was first found on plastic drift on a local beach in 2002. The next year it appeared on fouling panels in the Fort Pierce inlet, and since the summer of 2003 has been found on other natural and artificial substrata in the inlet and adjacent Indian River Lagoon (J. E. Winston, unpublished data). Its range expansion may be the result of warming water, but the rapid northward spread of the species may have been expedited by rafting. The fate of transatlantic rafters is less certain. Drift objects that become entrained in Gulf Stream currents can reach the eastern Atlantic in a few months time, but whether any attached organisms can survive and become introduced is unknown, although the recent report of trans-Atlantic rafting by the brooding reef coral Favia fragum (Hoeksema et al. 2012) indicates this type of dispersal may occur more often as ocean waters warm. Hitchhiking Hitchhikers are organisms that attach to a mobile vehicle, such as a sailboat or ship and are carried to a new region along a coast or through an ocean. They can also be carried to new regions in the ballast water of ships. Both of these are human-caused introductions. One less common kind of vessel for hitchhikers is a living nektonic or mobile benthic organism. Both invertebrates like Nautilus and vertebrates, including whales, dolphins, sea turtles, and sea snakes, may all have organisms encrusting them. Whales and dolphins are fouled by certain barnacles (e.g., Spivey 1980). On other organisms, the epifauna may include a wide variety of encrusting taxa. For example, nesting loggerhead turtles in Georgia were found to have 11 major groups of organisms ranging from algae and sponges to tunicates, attached to their shells (Frick et al. 1998). During the nesting season their shells show a successional pattern of colonization, beginning with barnacles, followed by bryozoans and hydrozoans, and ending with colonial ascidians (Frick et al. 2002). Bryozoans are successful at encrusting swimming organisms ranging from sea Nonpelagic dispersal modes snakes and sea turtles (Kropach and Soule 1973; Frazier et al. 1992; Key et al. 1995; Pfaller et al. 2012), to living Nautilus species (Landman et al. 1987). These shelled Indo-Pacific cephalopods host a great variety of taxa including sponges, foraminiferans, tube-building polychaetes, barnacles, bivalve mollusks, and diatoms, as well as bryozoans. Distances spanned range from a few kilometers (for sluggish sea snakes) to a few thousand kilometers (for sea turtles). One sea snake, Pelamis platurus, from the Pacific coast of Costa Rica was recently found to host eleven epibionts, including the first six decapod epibionts ever reported from a sea snake (Pfaller et al. 2012). Loggerhead sea turtles have even been suggested as a dispersal vector for one invasive species, the Asian Veined Rapa whelk, Rapana venosa, along the eastern coast of the United States, as living individuals have been found on their shells (Harding et al. 2011). Mobile benthic animals, as well as those such as crabs and horseshoe crabs who swim part of the time, also may become fouled by epifauna (e.g., Key 1996; Patil and Anil 2000; McGaw 2006). In some cases the fouling load builds up until the animals molt. Others, such as decorator crabs, purposely place epifaunal organisms on their shells or even have a close relationship with a particular epibiont (e.g., hermit crabs and Hydractinia hydroids; Triticella bryozoans with crabs and shrimp). The movements of the crustaceans and horseshoe crabs may facilitate regional dispersal of the epibionts without a serious negative effect on their hosts thanks to the host’s periodic molts. Much more research effort was put into the study of invasive marine species once marine ecologists started to realize it was such a widespread phenomenon. Estuaries and harbors, especially those with large ports, have been the recipients of the largest number of invaders. The problem has grown rapidly in recent years due to transport of ballast water and the globalization of ship-carried trade (Ruiz et al. 1997; Floerl et al. 2005; Williams and Smith 2007; Williams and Grosholz 2008). Fouling on ships’ hulls was the earliest form of anthropogenic transport of nonindigenous species (NIS). Carlton and Hodder (1995) studied the organisms carried on the hull of the Golden Hinde, the replica of a famous 16th-century sailing vessel when it visited the west coast of the United States. The ship sailed along an 800-km stretch of coast from Yakima Bay, Oregon, to San Francisco Bay, 451 California, staying for a month in each of four bays. The common fouling species survived the entire voyage without significant changes in abundance or diversity. Even some benthic species captured when the hull settled on the floor of a harbor were transported 390 km to the next bay. Modern shipping with its faster speeds, antifouling coatings and shorter residence times in ports has made the role of hull-fouling less significant. However, hullfouling is still a factor in dispersing organisms along coastlines and in spreading introduced species from their port of entry along the coasts of new regions. Ecologically, NIS can all be thought of as potential colonizers regardless of their mode of introduction and as colonizers if they establish new populations. Noninvasive colonizers have little impact on their new environment. Invasive colonizers can cause great changes, either temporary or permanent, in their new habitats (Davis and Thompson 2000). Sphaeroma walkeri, a warm-water isopod believed to be native to the Indian Ocean, is a prime example of a hull-fouling invasive species that has not been found to have any negative impact on invaded communities. The isopods prefer crevices such as polychaete tubes or empty barnacle shells on ship hulls, and may themselves be fouled by others such as encrusting bryozoans (Carlton and Iverson 1981; Galil 2008). They have a rather wide tolerance of salinities and temperatures. The female isopods brood their eggs. The species is known as a port-fouling and ship-fouling organism in places ranging from the Mediterranean (from Spain to Israel) to Asia, Australia, South Africa, Brazil, Florida, and the Caribbean. It colonized the Mediterranean early in the century, but appears to have spread to the Western Atlantic about the time of World War II or later. It was introduced into western United States at San Diego Bay in 1973 but seems to have had no detectable effect on other organisms there, either native or established Carlton and Iverson 1981). Ascidians are also good examples of organisms that are likely to have invaded new areas by hull-fouling, sometimes to negative effect. They are sessile filter feeders. Many species are colonial or social, hermaphroditic, and capable of selffertilization, with short-lived larvae unlikely to survive transit in ballast water. Many species are also eurytopic, with rapid growth to sexual maturity and a long breeding season. Lambert and Lambert (1998) documented 14 nonindigenous species 452 invading southern Californian harbors during the 20th century. Their survey in 1997 found species believed to be native to Japan, Peru, Europe, eastern United States, and the Sea of Okhotsk, Japan. All but one species persisted, and nonnative species now dominate the ascidian fauna of those harbors, while native species have declined. In addition to ships’ hulls, other locations within a vessel may attract fouling organisms. This is the case for sea chests, grated seawater-filled inlet boxes designed to increase the pumping efficiency of seawater used in engine cooling. Because of their more protected environment they may attract a different fouling fauna than would be found on the exposed hull of the ship. The organisms found on the walls of sea chests may include introduced species. For example, Carcinus maenus, Watersipora subtorquata, and Corbula gibba, all species introduced to Australia, were found living in the sea chest of a ferry travelling between Sydney and Tasmania (Coutts et al. 2003). In recent years marine ecologists have studied ballast water as the primary transporter of NIS. Initial studies chiefly considered transoceanic transport (e.g., Medcof 1975; Carlton 1985, 1987; Carlton and Geller 1993). Some organisms can even survive a trip from tropical to northern hemisphere cold waters; populations of one species, the harpacticoid copepod Tisbe graciloides, were even able to increase in abundance during travel from the Indian Ocean to the North Sea (Gollasch et al. 2000). The introduction of toxic dinoflagellates is of great concern for management of ballast water, as these organisms can survive transport as cysts that may germinate in their new habitat when the ship is de-ballasted (Hallegraeff 1998; Hamer et al. 2000). Intracoastal shipping may also significantly affect distributions both of NIS and native species (Lavoie et al.1999; Levings et al. 2004). Lavoie and colleagues (1999) looked at transfer of organisms in ballast water by shipping traffic between Narragansett Bay, Massachusetts, and Norfolk, Virginia. Few larvae of benthic invertebrates survived. Diatoms, dinoflagellates, and copepods dominated. Although the study found a decline in abundance of organisms between the beginning and end of the voyages, millions still survived each trip to be released into the harbor at the end point. Aquaculture and the aquarium trade have also played a role in distributing marine and estuarine organisms across vast distances. East-coast oysters were transferred to several locations on the west J. E. Winston coast of the United States in the hope of establishing new fisheries. The oysters did not persist, but many of the organisms associated with them, including taxa with nonfeeding larvae persisted. The same thing happened with Asian oysters, Crassostrea gigas. One associated invader, the Japanese False Cerith, Batillaria attramentaria, a mud-snail with direct development, was first noticed on the western coast of the United States in the 1930s in association with oysters and has recently been found spreading into areas without oyster aquaculture. It has caused a decline in the native Cerithidea californica (Byers 1999, 2000; Ruesink et al. 2005) and has introduced a new trematode parasite of both native and introduced fish (Torchin et al. 2005). It may also have had positive effects in some areas by providing homes for hermit crabs and increasing the cover of eel grass beds (Wonham and Carlton 2005). Hopping Hopping, or intergenerational stepping-stone dispersal, is the method we usually expect for organisms without feeding larvae to use in maintaining or extending their distributions. For epifauna, this means that larvae are making the jump from one island of hard substratum or microhabitat in stages. For infauna, the larvae must hop from one patch of suitable sediment to the next. There have been many studies, both theoretical and experimental, on the occurrence and importance of this kind of dispersal in marine systems. Conclusions vary from organism to organism, but in many of the cases studied so far this type of dispersal seems to work for coastal and shelf organisms, as well as those from coral reefs. For example, at geographical distances of 1–50 km genetic distances between patches of the solitary scleractinian coral Balanophyllia elegans met a linear stepping stone model (Hellberg 1995), although at greater distances, historical differences in gene flow, perhaps due to late Pleistocene climatic changes disrupted the pattern. In a study of reef coral recruitment on Helix Reef in Australia, Sammarco and Andrews (1988) found that recruitment declined rapidly with distance from the reef, indicating that coral reefs are primarily self-supplied with new coral recruits, although over a long time period the planktonic life of different reef corals (from 4 h to 3 months) makes hops to more distant reefs likely for some of them. Nonpelagic dispersal modes The biggest leaps may be taken in deep water, whale fall to whale fall, seamount to seamount, cold seep to cold seep, or hydrothermal vent to hydrothermal vent. These habitats may provide stepping-stones for transoceanic dispersal of some of the more than 1000 species of invertebrates and fishes occupying these habitats (Wilson and Kaufman 1987; Rouse et al. 2004). Global species diversity on whale falls is high, but on any particular fall the fauna goes through several successional stages: first a mobile scavenger stage, then an enrichment opportunist phase, followed by a sulphophilic stage, in which a large and in part chemotrophic group of organisms live off the skeleton (Smith and Baco 2003). Results of initial taxonomic and ecological studies of seamounts and vents suggested that they were areas of high endemism. However, later studies have shown faunal similarities between seamounts separated by a few thousand kilometers, indicating that some of the species may be able to disperse longer distances and raising the question of whether models of isolated islands (and ensuing endemism) or of oases (concentrations of widespread species) can best explain their diversity (Samadi et al. 2006). Creeping Creeping applies to organisms extending their distribution incrementally along continental shelves where habitat and environmental conditions are sufficiently similar for long distances. Short-lived larvae do not present a problem for animals dispersing in a rather homogenous habitat. Genetic studies show that young of many marine organisms do settle near their parents (e.g., Havenhand and Svane 1989; Callaway 2003; Harii and Kayanne 2003; Hadfield 2011). Little by little their populations spread along a coastline or continental shelf until the species reaches the limits of its tolerance of physical factors like water temperature and salinity, or reaches ecological limits imposed by competitors or predators. Much less is known about what continuity of habitat means to different kinds of marine organisms. What might be a homogeneous sand bottom to a burrowing organism might offer just a few scattered islands of habitat to an epifaunal organism. Yet, divisions that seem logical to scientists may be perceived differently by the organisms under study. Encrusting bryozoans require a hard surface for attachment. Subtidal sand bottom would seem to 453 offer only the occasional dead shell, sunken piece of wood, can, or bottle for hospitable habitat. Here and there currents might have swept larger shell fragments and shells, or in places rock or reef might project from the sand, but it appears to be a very patchy and fragmented habitat for a colonial encrusting animal. That is what a Danish colleague and I thought, too, until we undertook a study of the ecology of two species of free-living cupuladriid bryozoans on a shoal on the eastern coast of Florida off Fort Pierce, in the early 1980s. We sampled four times per year using a small epibenthic sledge. The mixed calcareous and terrigenous sand samples we collected were transported to the laboratory and spread out in big shallow trays of seawater. Within a few hours to a few days, the larger juvenile and mature cupuladriid colonies would dig their way up to the sediment’s surface, using coordinated movements of their bristle-like vibracula. To find the juvenile, sexually produced colonies that had settled on a single grain of sand and had not yet grown around and over it to become free living, we had to sort many spoons of sand under a stereomicroscope. We soon noticed that there were other bryozoans encrusting the shell and mineral grains. One group consisted of species with very small colonies, able to grow and reproduce on the grain on which the larva had settled. We also realized that a whole community of attached organisms including serpulids, entoprocts, encrusting foraminiferans, and hydroids also lived on the sand grains. We found the mean number of living encrusting bryozoan colonies was 0.75 colonies per cubic centimeter, or an estimated 7500 colonies in an area a square meter in size and a centimeter in depth. We realized that the sandbottom areas, rather than being free of encrusting taxa, actually supported large populations. In addition to the new species of single-grain encrusters, we found colonies of encrusting bryozoans that normally were attached to larger rock or dead mollusk-shell substrata also living on sand-size to gravel-size shell fragments (Winston and Håkansson 1986). Later studies in Brazil resulted in the discovery of very similar subtidal encrusting sand fauna on the coast of São Paulo state. Some of the Brazilian species were identical morphologically to those from Florida (although we do not yet know anything about their genetics), others are very similar sister taxa, suggestive of a greater-than-expected degree of connectivity between the two regions. The presence 454 of representatives of species more commonly encountered on larger patches of hard substratum, like rocks and unbroken shells, suggested that sand bottoms might actually serve as a refuge and a dispersal corridor for encrusting taxa in a way that had not been appreciated previously (Winston and Migotto 2005). The paradox of dispersal The modes discussed above show ways in which marine organisms without planktonic larvae that feed might extend their distributions regionally and even from one ocean to another, but we still have little evidence as to how much a particular species distribution is actually affected. Between the 1980s and today, we have made progress in understanding larval dispersal in groups of marine organisms with larval life histories varying from nonplanktonic to extended pelagic. Benchmark topics range from studies leading to better understanding of clonal and colonial invertebrate ecology (e.g., Jackson 1986), studies of the extent and impact of invasive species (Carlton 1985, 1987; Ruiz et al. 1997), to studies of rafting (Thiel and Gutow 2005a, b; Thiel and Haye 2006), dispersal of larvae in the field, and the genetics of populations and metapopulations of marine species. Many studies have upheld the expected finding that short-lived larvae settle close to their parents, often with gregarious settlement patterns that may depend on chemical cues (e.g., Havenhand and Svane 1989), in which recruitment declines rapidly with distance, and the genetic relatedness of populations aligns neatly with their geographical distance from each other. For example, in the Japanese blue octocoral Heliopora coerulea recruitment of the short-lived larvae was observed only within 350 m of the adult colonies, and often larvae settled between adults (Harii and Kayanne 2003). The Mediterranean sponge Crambe crambe showed the same pattern, slightly complicated by its ability to reproduce asexually as well as sexually (Calderón et al. 2007). Yet there are many paradoxes. That of the snails of Rockall (Johannesson 1988) in which a species with direct development has a broader distribution than one with planktonic larvae is perhaps most well known. Some species with a long planktonic life and thought to be widespread turn out, on morphological (e.g., Bhaud and Fernandez-Alamo 2000) or J. E. Winston molecular bases (e.g., Hellberg 2009), to have relatively restricted distributions. In other cases, two species with the same type of larvae have turned out to have very different distributions, e.g. the northeastern Pacific gastropods Nucella ostrina, and N. lamellosa and Littorina scutulata and L. plena species-pairs in which ecological or historical demographic differences outweigh larval dispersal potential (Kyle and Boulding 2000; Marko 2004). Other research results show patterns of genetic variation that do not correlate with geographical distances; in those, some past disaster or climatic change may account for the pattern (e.g., Magalon et al. 2005; Borerro-Pérez et al. 2011). Larvae cheat, too. Some nonfeeding lecithotropic larvae, such as those of the abalone Haliotis rufescens, can take up amino acids from seawater (Jaeckle and Manahan 1989). Other species may produce more than one type of larva, as needed (poecilogony: e.g., Clemens-Seely and Phillips 2011). We are still seeking better methods to help us understand the meaning of different distributions of marine species and different kinds of life histories among their offspring. The most recent trend is the study of connectivity in marine systems, including the role of larvae. Occurring or predicted global climatic changes make it essential to understand the role of connectivity in order to design adequate marine reserves. Larvae, their dispersal pathways, recruitment, and survival are keys to this effort (Cowen and Sponagle 2009). Reviewing the past 25 years of publications on larval dispersal has also revealed a large amount of speculation supported by a quite limited amount of data. The size of larvae versus the size of the oceans make it a daunting task to understand even the distribution of one marine species within one ocean or one small region of an ocean. Empirical studies like those of Thiel and associates on rafting dispersal are labor-intensive and time-consuming, but we need more of them. We must apply the models of connectivity, not just among subpopulations of marine organisms, but also among specialists in the different disciplines involved. We need combined results from oceanographic and biophysical modeling, microchemical analyses, and molecular genetic studies, as well as additional thorough ecological study in both field and laboratory, to understand marine dispersal now and for the future. Nonpelagic dispersal modes Acknowledgments The author thanks the organizers of the symposium for all their hard work in putting together a unique multidisciplinary array of speakers. Thanks to Dr Mary E. Rice for the guidance and enthusiasm that encouraged so many of us to pursue life-history studies. Thanks, too, to Dr Valerie Paul and the staff of the Smithsonian Marine Station for their support over the years. This is contribution no. 876 from the Smithsonian Marine Station, Fort Pierce, Florida. Funding This work was supported by the American Microscopical Society, SICB Divisions of Evolutionary and Developmental Biology, Ecology & Evolution, and Invertebrate Zoology, and by NSF Grant (IOS-1148884 to Sara M. Lindsay). 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