Download Dispersal in Marine Organisms without a Pelagic Larval Phase

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.
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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
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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
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‘‘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,
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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
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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
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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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