Download Dispersion and ecological impact of the invasive freshwater bivalve

Ó Springer 2006
Biological Invasions (2006) 8: 947–963
DOI 10.1007/s10530-005-5107-z
Dispersion and ecological impact of the invasive freshwater bivalve Limnoperna
fortunei in the Rı́o de la Plata watershed and beyond
Demetrio Boltovskoy1,2,3,*, Nancy Correa4, Daniel Cataldo1,2,3 & Francisco Sylvester1,3
1
Departamento de Ecologı´a, Gene´tica y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de
Buenos Aires, 1428, Buenos Aires, Argentina; 2Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas,
Argentina; 3Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Argentina; 4Servicio de
Hidrografı´a Naval, Argentina; *Author for correspondence (e-mail: [email protected])
Received 29 June 2004; accepted in revised form 14 November 2005
Key words: bivalvia, colonization, ecological impact, freshwater molluscs, invasive species
Abstract
Limnoperna fortunei is a freshwater bivalve that invaded South America through Rı́o de la Plata estuary in
1989 and has since become a major macrofouling pest. Along the Paraná-Paraguay waterway, which hosts
intense boat traffic, L. fortunei has moved upstream at an average rate of of 250 km per year. In contrast,
along the Uruguay river, where boat traffic is restricted to the lowermost 200 km section, upstream colonization is almost 10-times slower. This suggests that attachment to vessels is by far the most important
dispersion mechanism. It is suggested that the Amazon, Orinoco and Magdalena basins are under high risk
of invasion by this mussel, especially through their estuarine gateways. All South American basins host
innumerable water bodies with favorable conditions for L. fortunei’s colonization. Known ecological tolerance limits of the mussel also suggest that it may colonize much of the area from Central America to
Canada, including waters that due to their low calcium contents, high temperature and pollution levels, and
low oxygen are inadequate for the survival of Dreissena polymorpha. Despite it’s remarkable geographic
expansion and its extremely high population densities, L. fortunei’s ecological effects have received very
little attention so far. It is suggested that the 2.4-fold increase in Argentine landings of freshwater fish
between 1992–1993 and 2000–2001 may be associated with the introduction of this prey species.
Introduction
Limnoperna fortunei (Dunker 1857) is a freshwater bivalve mollusc native to the rivers and estuaries of Southeast Asia (China, Thailand, Korea,
Laos, Cambodia, Vietnam, Indonesia) (Ricciardi
1998). Between 1965 and 1990 it was unintentionally introduced in Hong Kong, Taiwan, and
Japan (Ricciardi 1998), and around 1989 it invaded Argentina, most probably via ships’ ballast water. In South America it was first
dicovered on the right hand margin of the Rı́o
de la Plata estuary, ca. 70 km southeast of the
city of Buenos Aires (Pastorino et al. 1993).
In 2003, thirteen years after entry, L. fortunei
has colonized practically all the Rı́o de la Plata
basin extending its range north as far as the
Pantanal (along the Paraguay river), and the
States of São Paulo and Minas Gerais (both in
Brazil). Beds of L. fortunei with up to 150,000
ind. m)2 dominate hard substrates from the
Rı́o de la Plata estuary to at least Asunción
(Paraguay) and Itaipú reservoir (Darrigran 2002;
Avelar et al., 2004; Figure 1).
L. fortunei shares several salient biological and
ecological features with the North American
invasive pest mollusc, the Zebra Mussel,
Dreissena polymorpha, which entered the US
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through the Great Lakes area around 1986 and
is now present as far south as the Gulf of Mexico. Both are dioecious and have similar sizes,
grow rapidly, attach to hard substrata by means
of a strong byssus, and are rapidly dispersed by
their planktonic larvae (Morton 1979; Ricciardi
1998). These similarities suggest that assessment
of the ecological impact of L. fortunei in South
America may benefit from comparisons with that
of D. polymorpha in Europe and North America.
Extensive research has demonstrated that Zebra
Mussels are very effective ecosystem engineers,
altering both structure and function of the ecosystems invaded. They change existing and provide new habitat for other organisms. They affect
trophic interactions and the availability of food
for both pelagic and benthic species, and they
influence the rates of other processes including
mineralization of nutrients, oxygen availability,
sedimentation rates, and dynamics of pollutants
(Karatayev et al. 1997). It is therefore highly
probable that ecological shifts as important as
those that occurred in the European and North
American areas colonized by the Zebra Mussel
Figure 1. Range expansion of Limnoperna fortunei in South America, locales and years when the mollusc was first detetected. Inset
map: Salto Grande reservoir and results of a survey carried out in September 2003.
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are underway in Rı́o de la Plata basin rivers,
lakes and reservoirs.
As opposed to research on the ecological
impacts of L. fortunei, which so far is practically
null, information on its harmful effects on
human activities is abundant. Shortly after invasion, L. fortunei has become a major nuisance for
industrial and power plants, most of which have
had to undertake additional maintenance tasks in
order to cope with the problem. Clogging of
water intake sieves and filters, pipes, heat
exchangers, condensers, etc., became a common
difficulty in industrial and power plants that use
raw water, chiefly for cooling purposes (Cataldo
et al. 2003). In Argentina, Uruguay, Bolivia,
Paraguay, and Brazil many plants (including two
nuclear and several hydroelectric power stations,
water treatment facilities, distilleries, and refineries, etc.) located along the Rı́o de la Plata estuary and the Paraná-Paraguay and Uruguay rivers
and their tributaries started experiencing clogging
and pressure loss problems associated with fouling by L. fortunei (Figure 2).
This paper offers an analysis of the northward
range expansion of this bivalve in South America
emphasizing some salient features of interest for
interpreting the mechanims involved and for
anticipating its future spread in South America
and beyond. Prospective northward range extensions of L. fortunei are validated comparing its
Figure 2. Steel grate protecting the raw water intake at the
nuclear power plant Atucha I, clean (left), and heavily fouled
by L. fortunei approximately 9 months later (right).
known and inferred biological traits with those
of D. polymorpha. Potential impacts of the mussel on South American freshwater communities
are discussed.
L. fortunei dispersion rates: Paraná vs.
Uruguay rivers
In the 12 years elapsed since its first sighting in
the Rı́o de la Plata estuary (Pastorino et al.
1993), L. fortunei steadily expanded northwards
upstream the Paraná-Paraguay and Uruguay rivers. Along the Paraná-Paraguay, the mollusc
appeared in Atucha (ca. 130 km from Buenos
Aires) in 1996, and almost simultaneously
1240 km farther north, in Corrientes (Figure 1).
In 2000 it had already reached the Pantanal
along the Paraguay river (ca. 2000 km upstream,
Figure 1). Along the upper Paraná and its tributaries adult mussels were recorded in São Paulo
state (Brazil) in 2002 (Avelar et al. 2004), and
larvae at the San Simão dam on the Paranaı́ba
river, a tributary of the Paraná, in 2003 (ca.
3000 km upstream from the Rı́o de la Plata estuary). This represents an average upstream movement of ca. 250 km per year.
In contrast to the above pattern, along the
Uruguay river, which also feeds into the Rı́o de
la Plata, recent data indicate that upstream colonization is almost 10 times slower. In the Negro
and Yı́ rivers the mollusc was first recorded only
in 1999 (Clemente and Brugnoli 2000), and in
Salto Grande dam in August 2001 (A. Otaegui,
pers. communication; see Figure 1). The size of
the animals recorded in Salto Grande indicates
that the species reached the area about an year
earlier (Boltovskoy and Cataldo 1999). Salto
Grande is located 350 km north of the Rı́o de la
Plata; thus, the mollusc’s upstream movement
along the Uruguay river averaged only 30 km
per year.
Two basic modes of geographic expansion of
invasive species have been described: a gradual
dispersion from a localized epicenter (the ‘reaction-diffusion’ model), and a wave-like dispersion
punctuated by long distance transport events or
‘jump dispersal’ (the ‘stratified diffusion’ model)
(MacIsaac et al. 2001). Gradual expansion is
characterized by initial establishment and local
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population growth, followed by progressive
spreading to adjacent areas; in this case dispersion speed is assumed to be proportional to population growth rates, as well as to time since
initial colonization. Jump dispersal, on the other
hand, is more dependent on the availability
of long-distance dispersal agents, both natural
(storms and strong winds, flooding events)
and man-mediated (shipping, fishing, tourism,
boating, etc.).
Contrasting dispersion patterns in the Paraná
and the Uruguay rivers seem to respond to these
two different modes of invasion. The Paraná
river hosts intense commercial boat traffic all
year round. The yearly volume of cargo (chiefly
grain) transported between the Atlantic Ocean
and Santa Fé (lowermost 580 km of the waterway; Figure 1) by ocean-going vessels is around
70 million metric tons. Between Santa Fé and the
Brazilian port of Corumbá (Figure 1), in the
Pantanal (total distance: 2200 km), where cargo
(chiefly iron ore) is transported by tug-pushed
barges, the yearly volume is around 7 million
metric tons. In addition, both major rivers and
tributaries are regularly used by smaller commercial, tourist, fishing and leisure boats, especially
during the summer. Thus, L. fortunei’s upstream
colonization along this waterway was most
probably characterized by jump dispersal mediated by human activities (Figure 3). This type
of range extension depends less on distance
between source and recipient site and allows very
long-range invasions over short time intervals
(MacIsaac et al. 2001). It is quite probable that
adult animals adhering to ships’ hulls are transported upstream, spawn, and their larvae drift
with the current (usually around 3–4 km h)1) settling a few hundred kilometers downstream. The
distance covered between the area of spawning
and settlement depends on larval development
rates, which vary between 10 and 20 days,
depending on water temperature (Cataldo et al.
2005). Most of the area is therefore colonized by
downstream larval dispersal, rather than upstream. The fact that L. fortunei was recorded
the same year (1996) in Atucha and in Corrientes, which are over 1100 km apart (Figure 1),
supports the above conclusions.
As opposed to the Paraná, along the Uruguay
commercial ocean-going vessels have access only
to the port of Nueva Palmira, located about
5 km upstream from the confluence of the latter
with the Rı́o de la Plata. Between Nueva Palmira
and Concepción del Uruguay (200 km) commercial and fishing boat traffic is very limited,
whereas in the following 150 km stretch, between
Concepción del Uruguay and Salto Grande
dam (Figure 1, inset), navigation is essentially
restricted to coastal fishing activities on small
(<10 m) craft and some short-range leisure sail
and motor boating.
In September 2003 we thoroughly surveyed
both margins of Salto Grande reservoir in order
to pinpoint the northernmost records of L. fortunei
along the Uruguay river (Figure 1, inset map).
L. fortunei was present at very high densities (over
50,000 individuals m)2) from the dam to the local-
Figure 3. Schematic representation of the ‘‘jump dispersal’’
mechanism used by L. fortunei in the Paraná system. Numbers
indicate potential chronological sequence of records of the
species along the waterway (see text for detailed explanation).
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ities of Santa Ana (right-hand margin, 40 km upstream from the dam) and Constitución (left-hand
margin, 30 km upstream). A few kilometers north
of Constitución, at Espinillar, densities dropped to
less than 1 mollusc m)2, and about 5 km north of
Santa Ana the animal was absent altogether (Figure 1, inset map).
Considering that adult L. fortunei were first
detected in installations of the Salto Grande
hydroelectric station in 2001 (which means that
larvae or juveniles arrived there about an year
earlier), and that in September 2003 the farthest
point with L. fortunei was located 40 km
upstream from the dam, colonization of the reservoir has occurred at an average rate of about
10–20 km per year. Very high-population densities in the areas so far colonized (Figure 4), as
well as the fact that hard substrata adequate for
the mollusc’s settlement (pebbles, boulders
and rock outcrops) are much more abundant in
the Uruguay river than along the Paraná-Paraguay, indicate that constraints associated with
upstream transport, rather than environmental
suitability, are responsible for such dissimilar
colonization rates. These evidences suggest that,
of the over 20 dispersal mechanisms described
for freshwater, invasive, byssate molluscs (Carlton 1993), for L. fortunei attachment to and
upstream transport by commercial vessels is by
far the most important. Transport by birds,
fishes and aquatic mammals cannot be ruled out,
but is improbable because molluscs are normally
destroyed and/or digested before egestion, at
least by fishes (Penchaszadeh et al. 2000; Cataldo
et al. 2002). Strong and persistent southern
winds, especially during periods of low discharge,
could temporarily reverse the normally southward water flow in the reservoir, thus advecting
entrained larvae northwards. Human-aided dispersion cannot be ruled out either: a few dozen
sailing boats stationed at marinas located in the
vicinity of the dam use regularly the lower third
of the reservoir for leisure and sports actvities,
and Coast Guard vessels are ocassionally deployed as well. Fishing activities are probably of
minor importance because the very small and
few boats involved are mostly kept on land when
not in use (which keeps their hulls free from
fouling by L. fortunei), and their north–south
displacements are minimal.
Figure 4. Limnoperna fortunei in Salto Grande reservoir. Top:
living organisms in a shallow costal area at Santa Ana (inset
shows detail of shells). Middle: same area, mussels attached
to wood debris. Bottom: empty shells along the waterline in
Federación after a prolongued low water period (see Figure 1,
inset). All photographs taken on 16 September 1993.
The density–occurrence pattern recorded in the
Uruguay river, where over an ecologically homogeneous area sites inhabited by L. fortunei in
extremely high densities are only a few kilometers
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away from locales where the animal is not present
at all, indicate that once established L. fortunei
reaches extremely high densities rapidly.
In addition to these records along the two
major Rı́o de la Plata basin waterways (ParanáParaguay and Uruguay rivers), L. fortunei is also
present in Rı́o Tercero, and in the Guaiba river
basin (Figure 1). Rı́o Tercero is a medium-sized
(54 km2) reservoir whose waters are used by a
nuclear power plant for cooling purposes.
L. fortunei was first discovered in this plant in
1998. The reservoir drains into the Paraná
through the Tercero-Carcarañá rivers (Figure 1),
neither of which is navigable. Rı́o Tercero is a
popular tourist destination, with boating and
fishing on the reservoir being its main attractions. It therefore is conceivable that L. fortunei
was introduced inadvertently, attached to the
hull of a boat trailered overland from some location on the Paraná or Uruguay rivers.
In the Guaiba lake L. fortunei was first
recorded in 1998 (Mansur et al. 1999). This basin
is separated from the Rı́o de la Plata watershed,
which suggests the possibility of L. fortunei having been introduced here via ballast water as well
(the ports of Rio Grande and Porto Alegre,
located in this basin, serve oceanic-going ships).
Prospective expansion of L. fortunei
in South America and beyond
Because of its major impacts on human activities
and on the environment, prediction of the future
behavior of L. fortunei in and beyond South
America is of much interest. We are not yet in
the position to attempt the use of numerical
modeling techniques like, for example, those used
in North America in the early stages of the invasion of the Zebra Mussel (e.g., Ramcharan et al.
1992; Padilla et al. 1996). Constraints due to the
virtual absence of information on the ecological
preferences of L. fortunei, associated with a generally modest to poor knowledge of the limnologic and biologic traits of the enormous and
very complex South American river system, only
allow outlining a series of general observations.
These considerations, however, may serve to
identify promising investigation avenues thus
contributing towards our understanding of the
mechanisms that govern the spread of aquatic
invasive species in general, and of L. fortunei in
particular.
The vulnerability of new areas to biological
invasions are basically dependent on two aspects:
(1) likelihood of introduction (naturally or
human-mediated, such as by shipping and boating activities), and (2) environmental suitability.
We will first assess the potential exposure of
South American waterways to biological invasions from outside and within the subcontinent,
and then comment on the suitability of these
waters for the establishment of L. fortunei.
Likelihood of introduction
The South American river system is characterized by five major drainage basins and several
minor ones; the major rivers are (from north to
south): Magdalena, Orinoco, Amazon, São Francisco, and Rı́o de la Plata (Paraná-Uruguay)
(Figure 5). As outlined above, the Rı́o de la
Plata basin has already been almost totally
colonized (Figure 1). Due to their size and proximity with the infested area, the Amazon and the
Orinoco rivers are the most likely candidates to
receive the bivalve in the future.
The Amazon river is the largest in the world
in terms of watershed area, number of tributaries, and volume of water discharged (mean:
212,000 m3 s)1). It measures 6400 km from
source to mouth, has hundreds of tributaries,
and drains a territory of over 5.7 million km2
(about half of them in Brazil, the rest in Peru,
Ecuador, Bolivia, and Venezuela). The Amazon
enters the Atlantic through a broad estuary,
roughly estimated at 240 km in width; the mouth
of the main stream, the Pará, is 80 km wide. The
Amazon is navigable to ocean liners of virtually
any tonnage for two-thirds of its course. Transoceanic ships call regularly at Manaus, nearly
1600 km upstream; and smaller ships can reach
Iquitos, Peru, 3700 km from the river’s mouth
(the farthest point from sea of any port serving
ocean traffic). Due to the scarcity of roads, river
navigation has an essential role in this area
and is naturally facilitated by the generally
favorable hydrographic conditions; in total, the
system is estimated to host over 19,000 km of
navigable waterways. Small and medium-sized
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river steamers can navigate on more than 100 of
the larger tributaries (Solimões, Negro, Branco,
Madeira, Purus, Juruá, Trombetas, Jari, Tapajós,
Xingu, Guama, Capim, etc.).
The Orinoco river is the third largest river in
the world in terms of water discharged to the
ocean (mean discharge: 36,000 m3 s)1), draining
an area of 870,000 km2 in Venezuela, Colombia
and Brazil. Large river steamers travel upriver
for about 700 miles from the delta to the Atures
rapids. Dredging has allowed large ocean going
vessels to navigate the Orinoco from its mouth
Figure 5. Main watersheds of South America.
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to its confluence with the Caronı́ river, a distance
of about 400 km.
The São Francisco river has a mean discharge of 2800 m3 s)1, and a drainage area
of 665,000 km2 (entirely in Brazil). Its main
navigable tract of 1300 km is a middle section
that flows between the towns of Pirapora and
Juazeiro, which is regularly used by commercial
traffic (tourist ships, tugboats, freight barges, etc.).
Navigation in the lowermost section is restricted
by the Paulo Afonso falls (with a drop of 80 meters), located 200 km from the river mouth, and
by the low bottom depths in the estuary; this section does not have regular commercial traffic.
The Magdalena river (mean discharge:
7500 m3 s)1; drainage area: 257,000 km2) has a
length of 1550 km, of which 1092 are permanently navigable, and 887 are navigable by
large ocean-going steamers (the access channel
has an authorized depth of 10 m). The city of
Barranquilla, located on the river mouth, connects maritime with fluvial transport.
Thus, of the four major South American
hydrographic basins (excluding the Rı́o de la
Plata), three are readily accesible through their
mouths by ocean-going vessels, which makes
them highly vulnerable to invasions via ships
ballast water.
Invasion of the basins through their estuaries
via ballast water, as assumed for the original colonization of L. fortunei in the Rı́o de la Plata
(Pastorino et al. 1993), is but one of the potential
routes of entrance. Freshwater molluscs can also
be dispersed by a number of other mechanisms,
both natural and human-mediated (e.g. Carlton
1993; Padilla et al. 1996), some of which
have most probably been of importance for the
colonization of remote areas of the Rı́o de la
Plata watershed, away from the Paraná-Paraguay
mainstream (e.g., Rı́o Tercero, see above).
Although most of the mayor South American
watersheds involved are effectively separated,
some are not. For example, the Orinoco and the
Amazon basins are permanently connected by
the rivers Casiquiare-Negro, which greatly facilitates interchange of fauna and flora. South
American tropics and subtropics are characterized by a sharp alternation of a dry period
with a rainy season (July to September for the
Orinoco basin, December to April for the central
Amazon basin); during the latter phase enormous areas around the river and creek channels
are flooded increasing the total water-covered
surface by up to 900% (Junk 1997). Although
these periodically flooded wetlands would not be
able to offer permanent refuge to L. fortunei,
because they dry out during the dry season, they
can greatly facilitate connection between and
invasion of neighboring waterways.
In addition to these natural means of dispersion, several human-mediated ones can also be
envisioned. As seen above, all five major South
American watersheds have significant commercial
shipping activity; in addition, in all cases projects
are underway to improve navigation conditions
through the construction of locks, dredging, signalization, etc., which will further enhance river
traffic. Moreover, for several decades politicians,
administrators and engineers have contemplated
the possibility of linking the river systems of
South America to open up navigation across the
entire continent. The Hidrovia project, a megaundertaking designed to expand commercial shipping along the Paraná-Paraguay waterway
(3400 km) by deep dredging and excavation,
removal of rock outcrops and river curves,
realignment of channels and other heavy engineering works, which has recently completed its
first phase, is very probably largely responsible
for the fast upstream dispersal of L. fortunei in
this system (see above).
The likelihood of transport and re-seeding of
adults and larvae due to fishing activities is more
difficult to assess because quantitative data on
fishing-related displacements are unavailable.
Much of the area of influence of the Amazon and
the Orinoco has very low population densities
(<10 inhabitants km)2), but many of these depend on fishing for survival. FAO statistics indicate that the summed freshwater fish landings of
Brazil, Paraguay, Venezuela and Colombia for
2001 was 275,000 tonnes (60% more than, for
example, all of North and Central America
for the same period), which suggests intense activity and, concomitantly, at least some risk level.
It should be noticed that colonization of any
one of these northern basins significantly
increases the chances of infestation of the others.
On one hand, geographic spread of the species
carries it closer to areas free of the mussel, thus
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making overland transport more likely. On the
other, geographic expansion involves a growing
number of estuarine ports whose waters are contaminated, and therefore greater chances of further disseminating the invader through ballast
water. This is particularly important because
many of the freighters and passenger liners leaving the port of Buenos Aires stop at Brazilian
and Venezuelan ports on their way north. As a
matter of fact, it is very likely that the source of
the 1998 invasion in the Guaı́ba basin (Figure 1)
was the Rı́o de la Plata area, rather than Asia.
As opposed to much of the early spread of
D. polymorpha in the Great Lakes area, most of
which may have occurred by passive downstream
larval dispersal (Griffiths et al. 1991), from the
very start in the Rı́o de la Plata L. fortunei could
only disperse upstream, since downstream expansion was precluded by the nearby brackish
waters of the Rı́o de la Plata estuary. In spite of
this difference, the average upstream dispersal
rate of L. fortunei (ca. 250 km per year,
see above) is very closely comparable to that
of D. polymorpha downstream (Claudi and
Mackie 1994). Downstream dispersal, for which
L. fortunei’s planktonic larvae are particularly
well adapted, would therefore occur much faster.
Thus, if the headwaters, rather than the estuaries, of any one of the tropical South American
watersheds are invaded, complete basin colonization is expected to take significantly less time
than in the case of the Rı́o de la Plata.
The fact that many freshwater ports serving
ocean-going ships are located in estuarine areas,
in the vicinity of and upstream from brackish
and saline waters, is probably one of the reasons
that keeps species like L. fortunei from invading
alien regions worldwide more often. It is conceivable that the succesful 1989 colonization of the
Rı́o de la Plata was but one of many previous
attempts when juveniles were seeded in the
area, and even grew to reproductive size, but
whose offspring was entirely swept into the
ocean. L. fortunei’s larvae take 10–20 days to
reach the settling stage (Cataldo et al. 2005),
which is comparable to the time it takes a cargo
ship to steam across the ocean; thus, most of the
seeding individuals are very early juveniles ready
for attachment, rather than free-drifting larvae.
This enhances the invader’s chances of survival.
Environmental suitability
Amazon and Orinoco waters have been classified
into two main categories according to their
loadings of silt-sand and organic matter: ‘white
waters’ are turbid from a high content of
suspended mineral solids (fine silt-sand and
loam), with high conductivity values (60–80
s cm)1), nearly neutral pH and high content of
major cations, including calcium. ‘Black waters’
on the other hand, are transparent red-brown
from high loadings of humic substances, their
condunctance (typically 9–10 s cm)1) and pH
(ca. 5) are lower, and major cations, including
calcium, are scarce (e.g. Furch and Junk 1997).
The Paraná-Paraguay and Uruguay systems,
where L. fortunei dwells, are dominated by
white-water rivers. Dispersion of the mussel into
Amazon and Orinoco white waters would most
probably not involve major ecological challenges,
but black-water floodplain lentic habitats may
prove harder to colonize due to their acidity,
low levels of dissolved oxygen and scarce
calcium. As a matter of fact, the absence of
bivalves in black-water lakes of the central
Amazon floodplain has been noticed as one of
the major faunal differences between these and
the white-waters associated with this river (Junk
and Robertson 1997). Many of the benthic
invertebrates found in these areas avoid the
critical low-water period when oxygen depletion
is at its peak by migrating elsewhere; thus,
L. fortunei’s sessile, attached habit would further
hamper its chances of spreading through
black-water environments. Nevertheless, some
of the most critical conditions, like dissolved
oxygen, do not undergo such drastic fluctuations
in the turbulent conditions of the permanent
river channels. Furthermore, river waters may
seasonally shift from black to white, thus reducing the overall amount of time when colonization
by L. fortunei is particularly challenging.
Calcium loadings have often been found to
restrict the distribution of freshwater molluscs
(e.g., Sprung 1987; Ramcharan et al. 1992). Concentrations of this ion are generally low in Amazon (7–10 mg l)1; Furch and Junk 1997) and
Orinoco (2–5 mg l)1) (Hamilton and Lewis 1990)
white waters, but not significantly different from
those in the Rı́o de la Plata-Paraná-Paraguay
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system, where L. fortunei dwells (3–9 mg l)1;
Maglianesi 1973; Bonetto et al. 1998).
We therefore conclude that the Amazon,
Orinoco, and Magdalena watersheds are under
high risk of biological invasion through their
estuarine gateways (by means of ballast water or
other mechanisms), while for the São Francisco
basin this risk is lower. All four basins are also
likely to receive the invader through either natural or human-mediated mechanisms overland,
and host innumerable water bodies with adequate conditions for L. fortunei’s colonization.
Beyond South America
Even before it was discovered far beyond its
native range, researchers were concerned about
the possibilities of L. fortunei spreading into
other countries (Morton 1979), and after its discovery in Japan and Argentina Canadian and US
researchers forecasted its potential expansion to
North America (Ricciardi 1998; McNeill 2001).
While this has not yet happened, the more
L. fortunei expands its range in South America
and elsewhere, the higher are its chances of
reaching the fresh waters of North America as a
ballast water hitchhiker, either from South American ports to ports along the Gulf of Mexico, or
from Asia to ports on the West Coast.
Known ecological tolerance limits of L. fortunei
suggest that it may colonize much of the area
from Canada to Central America, including
waters inadequate for the survival of D. polymorpha. L. fortunei tolerates higher temperatures,
lower pH values and lower oxygen levels than the
zebra mussel (Ricciardi 1998; Karatayev et al.
Submitted). As opposed to the North American
subspecies of Dreissena polymorpha, which can
withstand salinities <6& (Karatayev et al. 1998),
L. fortunei has been recorded in the Rı́o de la
Plata estuary at salinities around 14& (D Giberto,
pers. comm.). It also is very resistant to high pollutant loadings: very dense L. fortunei beds
are present along the Luján river, in the lower
delta of the Paraná, in the vicinity of urbanized
and industrialized areas which discharge high
volumes of untreated domiciliary and industrial
wastes. The waters and sediments of this river
contain many pollutants at levels several times
above those considered hazardous for aquatic
life (e.g. Zn, Cr, Cu, benzo (a) pyrene, PCBs, etc.)
(Cataldo et al. 2001a). Bioassays with juveniles of
Corbicula fluminea indicate that waters, porewaters and sediments of this area are unfit for
the survival of this bivalve (up to over 75%
mortalities in 144 h exposures; Cataldo et al.
2001a, b).
Of particular significance may be the fact that,
as opposed to D. polymorpha, L. fortunei does
not require high calcium concentrations for larval and adult survival. Sprung (1987) found in
laboratory experiments that survival of D. polymorpha larvae required at least 12 mg Ca l)1 and
pH values above 7.4 for survival; critical calcium
concentrations were defined at 12–20 mg l)1,
whereas fertilization success and survivorship
were strongly enhanced by concentrations above
47 mg l)1. Vinogradov et al. (1993) concluded
that D. polymorpha’s requirements of calcium are
considerably higher that those of most other
freshwater bivalves: in order to maintain a metabolic balance between calcium loss and uptake,
concentrations of this element in the water must
not drop below 12–14 mg l)1. These results were
confirmed by a survey of 278 European lakes,
where occurrence and density of the Zebra
Mussel were found to be highly correlated with
water chemistry: D. polymorpha is absent in lakes
with average pH values below 7.3 and concentrations of calcium below 28.3 mg l)1 (Ramcharan
et al. 1992). South American inland waters are
characterized by rather low concentrations of
calcium, usually around 7 mg l)1 (Wetzel 1975),
and values as low as 3–4 mg l)1 are not uncommon in areas densely populated by L. fortunei
(e.g. the middle Paraná river, cf. Maglianesi
1973). In contrast, many North American and
most European freshwaters have calcium loadings in excess of 20–30 mg l)1 (Wetzel 1975;
Payne 1986). Thus, L. fortunei may colonize
areas unfit for D. polymorpha due to their low
calcium contents, like New England, the Canadian Shield, and much of the Pacific Northwest
(Strayer 1991). Conversely, South American low
calcium concentrations (in addition to the high
water temperatures) may represent a major
obstacle for invasion by D. polymorpha.
The fact that L. fortunei has continuous reproduction for 8–9 months of the year (Boltovskoy
and Cataldo 1999; Cataldo and Boltovskoy 2000),
957
while D. polymorpha spawns over a period of
1–3 months (Garton and Haag 1993), may also
constitute a competitive advantage for the former.
As anticipated above, our predictive considerations are based on but a fraction of the conditions that are thought to govern biological
invasions in freshwater systems. Selection of the
ones reviewed was based as much on their perceived importance, as on the body of knowledge
behind them. There are many other causal mechanisms that may be involved (e.g. the degrees of
pre-invasion ecosystem disturbance, overall biological diversity, synergistic and antagonistic
effects between invaders, etc.; Elton 1958; Stachowicz et al. 1999) and have not been taken in to
consideration, primarily because of gaps in our
understanding of their relevance (e.g. MacIsaac
et al. 2001).
Impacts
There is no doubt at this point that L. fortunei
has negatively affected practically all installations that use raw ‘contaminated’ water. Industry
and utility plants have experienced clogged or
blocked intakes and distribution piping, fouled
pumps, forbays, holding tanks, trashracks, and
condenser units, an increase in the corrosion of
iron and steel piping and riveting, etc. We have
had personal first hand experience and/or discussions with personnel involved with fouling
problems in nuclear and thermal power plants,
distilleries and refineries, steel mills, food plants,
commercial and leisure boats, drinking water
treatment facilities, etc. (e.g. Cataldo et al. 2003).
No estimates of the economic losses involved
have been made in South America.
Impacts on the ecosystem, on the other hand,
have not been investigated yet beyond a couple
of marginal observations (see below). Freshwaters of the Rı́o de la Plata basin have few filtering organisms, of which only Corbicula fluminea
can occasionally be abundant; thus, L. fortunei
has occupied a previously vacant niche, which
would partially explain its outstanding success.
The Rı́o de la Plata estuary flushes between
1,000,000 and 2,000,000 tn of particulated
organic carbon per year into the sea (Depetris
and Kempe 1993; Guerrero et al. 1997). With the
invasion of L. fortunei part of this organic matter
is intercepted and modified into a form available
to organisms that cannot feed on small particles,
like fishes. In order to assess how much of
this drifting carbon is now channelled through
L. fortunei we are still missing some key pieces of
the puzzle involved, in particular a reasonable
estimate of the densities of the mollusc in the water bodies colonized.
Assessment of average densities of the mussel
over large areas is complicated by the fact that
beds of L. fortunei have an extremely patchy distribution. This seems to be associated not only
with the uneven distribution of available substrate, but also with some other traits whose
influence we do not understand yet. For example,
concrete revetments along the Luján river (lower
delta of the Paraná) located a few hundred
meters apart host very different population densities (Figure 6). Nevertheless, overall abundances
are most probably very high in the areas colonized. On hard substrates, the mollusc has been
recorded at densities of up to 150,000 ind. m)2
(Darrigran 2002). Colonization is not restricted
to man-made structures, such as revetments,
piers, rock armors, gabions, boat hulls, etc.,
as the animal settles on debris, driftwood
(Figure 4), reed roots, etc. While rivers in this region are typically soft bottom, large areas, especially along the coasts of Uruguay, are
dominated by rock outcrops and hardpan formations (Figure 4) where the mollusc thrives.
Furthermore, clusters are common even on soft
bottom, especially when the mud is covered by a
thin hardened crust (Figure 7). Widespread
occurrence of L. fortunei in the gut contents of
fish (see below) also points at its abundance in
the area.
Observations of the negative impacts of
L. fortunei include reports from southern Brazil
and Japan. In the area of Guaı́ba lake (southern
Brazil), Mansur et al. (2003) reported that the
mussel attaches to at least 6 species of molluscs,
including 2 unionids, in numbers of up to ca. 300
L. fortunei per host. In several cases this overgrowth may hinder the host’s normal displacement and valve mobility. The same authors also
suggested that L. fortunei’s settlements on the
roots of the reed Scirpus californicus, an emergent helophyte, may be ‘suffocating’ the plants
958
and be responsible for the thinning of reed populations. Howewer, this effect is unlikely because
the roots of Scirpus must be adapted to the very
low oxygen environment characteristic of shallow
areas with very abundant organic debris. Furthermore, filtering bivalves are known to enhance
water oxygenation, rather than the opposite (e.g.
Karatayev et al. 1997).
Another potential threat posed by this invader
was reported by Ogawa et al. (2004). The
authors identified widespread parasitic infections
by bucephalid trematodes in several cyprinid
fishes from the Uji river, suggesting that the
infections started with the accidental introduction
of infested first intermediate hosts – Limnoperna
fortunei.
Among the potentially positive impacts,
enhancement of the diversity and abundance of
most other benthic organisms (Darrigran et al.
1998), and consumption by fish have been mentioned. Trophic interactions with fish are of
Figure 6. Concrete revetments along the Luján river, in the
lower delta of the Paraná, with different degrees of fouling by
L. fortunei; general view and detail (insets). The two sites
illustrated are approximately 500 m apart.
particular interest because the mussel represents
a novel resource available at an unprecedented
scale. At least 16 species have been recorded in
the Paraná and Rı́o de la Plata rivers that
actively consume L. fortunei (Montalto et al.
1999; Ferriz et al. 2000; Penchaszadeh et al.
2000; Cataldo et al. 2002). Some of the commercially most valuable species, like Pterodoras granulosus and Leporinus obtusidens, have been
observed to feed preferentially on L. fortunei:
up to 100% of the specimens retrieved in the
summer have their guts filled predominantly or
exclusively with remains of this mollusc (Ferriz et
al. 2000; Penchaszadeh et al. 2000; Cataldo et al.
2002). In situ experiments with L. fortunei-colonized panels with and without a protective screen
against fish predation showed that exposed colonies are swiftly eliminated by predators (Cataldo
et al. 2002). Sylvester et al. (submitted) carried
out a 1 year in situ experiment in order to assess
the colonization of PVC panels protected against
predation by screens of different pore-size (0.5,
1.5 and 4 cm). Densities of the resulting settlements of L. fortunei were inversely proportional
to the pore-size used, indicating that different fish
sizes, including animals as small as 1.5 cm in
thickness, feed on the mollusc. Predators were
estimated to harvest ca. 6 kg of whole mussel
mass per square meter of substrate per year, eliminating over 80% of Limnoperna’s production.
The positive effects of L. fortunei on these
fish communities are not restricted to species
that consume the mollusc directly, in particular
Figure 7. Cluster of L. fortunei on soft sediment in the Luján
river (lower delta of the Paraná).
959
those that can detach and crush the shells with
their frontal teeth, like Leporinus obtusidens
(Penchaszadeh et al. 2000), but also extends to
species that may benefit from this new food
resource indirectly, including many of the
larger (and commercially most valuable)
species that feed on other fishes (e.g. Pseudoplatystoma fasciatum, Pseudoplatystoma coruscans,
Salminus
maxillosus,
Hoplias
malabaricus,
Paulicea luetkeni, Luciopimelodus pati, etc.). Furthermore, L. fortunei’s functional similarities with
D. polymorpha strongly suggest that it may actively transfer large amounts of organic matter
from the pelagic to the benthic domains, through
filtration and the formation of feces and pseudofeces (Karatayev et al. 1997), which in turn
boosts invertebrate densities (Botts et al. 1996).
This may be of particular importance in the
Rı́o de la Plata basin where over 60% of the
overall fish biomass is represented by a single
deposit feeding detritivorous species: the sábalo,
Prochilodus lineatus (Sverlij et al. 1993). Enrichment of the sediments with organic matter would
therefore enhance the densities of sábalo in the
system (as observed with other fish species in the
presence of D. polymorpha, e.g. Thayer et al.
1997), which in turn represents the main food
item of most ichtyophagous species (Sverlij et al.
1993; Iwaskiw 2001).
The positive impact of L. fortunei on fish populations is not restricted to enhanced food availability, but also to better food quality. With the
invasion of Corbicula fluminea (around 1976),
and L. fortunei, dietary changes have been noted
in omnivorous fishes, which switched from a
lower quality predominantly plant-based diet, to
an energetically richer one dominated by these
molluscs (Ferriz et al. 2000).
Ancillary data on Argentine freshwater fish
yields support the above conclusions suggesting
that L. fortunei may have had a positive effect
on fish biomass in the Rı́o de la Plata system.
Figure 8 illustrates the trend in fish landings in
Argentina and other South American countries
during the last 50 years. The upper panel shows
freshwater fish catches as reported by FAO for
the six major South American producers (these
countries account for 97% of the overall total
for the entire subcontinent). The only country
where catches increased consistently after 1990 is
Argentina, whose figures grew from 11,277 tn in
1992, to 30,416 tn in 2000 (dropping to 23,860 tn
in 2001). When comparing the periods 1992–1993
vs. 2000–2001, Argentina’s catches show a net
2.4-fold increase; Paraguay and Brazil had slight
gains (35% and 8%, respectively), whereas Perú,
Venezuela and Colombia produced 1–20% less in
2000–2001 than in 1992–1993. It should be
emphasized that for Argentina these numbers
reflect almost exclusively catches in the area colonized by L. fortunei: over 90% of the freshwater
fish production is originated from the Rı́o de la
Plata basin, including the Paraná, Paraguay,
Uruguay and their tributaries (Iwaskiw 2001).
The numbers for Argentina are generally supported by other sources of information, such as
data from the INDEC (Instituto Nacional de
Estadı́sticas y Censos, Argentina, http://www.
indec.mecon.ar/), as well as various regional and
provincial agencies (e.g. Iwaskiw 2001). For
example, in the province of Santa Fé, whose
freshwater fish catches originate almost exclusively from the Paraná river and its tributaries, in
the 1995–2001 period landings increased almost
ten fold (from ca. 500–5376 tn), whereas fishing
effort, as measured by the number of commercial
fishing licences issued, only doubled (from 660 to
1214 licences; probably as a result of the better
fishing yields in the 3–4 preceding years) (Iwaskiw 2001). Export statistics confirm these trends
as well: Argentine exports of sábalo (Prochilodus
lineatus) to Bolivia and Brazil increased from
1467 tn in 1990 to 19,699 tn in 2000 (INDEC).
On the other hand, Argentine marine fisheries
increased steadily during the last five decades,
dropping sharply after 1996 (chiefly as a result of
the collapse of the Argentine hake – Merluccius
hubbsi – fishery due to overfishing; e.g. Renzi
2002) (Figure 8). Thus, the trend in freshwater
fisheries is most probably not a nation-wide phenomenon governed solely by social or economic
factors, but seems to reflect regional differences
in the availability of fish resources. A similar
effect has been observed in European fresh
waters where the invasion of D. polymorpha has
been associated with strong changes in fish populations (Poddubny 1966).
It may be argued that these positive effects
could be offset by L. fortunei’s impact on filterfeeding organisms, including fishes. However,
960
Figure 8. Freshwater and marine fish catches by selected South American countries between 1950 and 2001. Landings of the countries included in the graphs account for over 95% of the overall catches of South America. Based on FAO statistics (http://
www.fao.org/).
because the highly turbid waters of the Rı́o de
la Plata system are poor in plankton (Secchi
disk depths around 20 cm, phytoplankton densities usually below 500 cells ml)1; zooplankton,
including Rotifera, Cladocera and Copepoda,
usually below 30 ind. l)1; O’Farrell 1994;
Boltovskoy et al. 1995), filtering organisms are
relatively scarce in this system. As mentioned
above, the only occasionally abundant filterer is
the invasive Asian clam Corbicula fluminea
(Boltovskoy et al. 1995; Cataldo and Boltovskoy
1998), whereas representatives of the ca. 60
native clam species (20 of them unionids of the
genera Diplodon and Castalia) are recorded only
ocassionally and in very low densities (Bonetto
and Di Persia, 1975). Planktophagous fishes are
restricted to a few species, some of which prey
on plankton during their juvenile phases only
(e.g. Odontesthes bonariensis; Iwaskiw 2001).
Concluding remarks
The introduction of non-indigenous species is
widely recognized as a serious problem involving
major economic losses and one of the leading
961
global threats to native biodiversity and ecosystem function (Pimentel et al. 2000). The long history of negative unexpected results of the
intentional introduction of plants and animals,
as well as the impacts of accidental invasions,
clearly show that such range expansions involve
much more losses than benefits. However, despite
growing concern and interest in this problem,
biological invasions are likely to continue as
international trade increases and as climate and
land use continue to change (Byers et al. 2002).
Because economic resources are always a major
limiting factor, managers must decide which populations and species to control immediately,
which to control if time and money permit, and
which to leave alone. Such decisions are based
on the known or expected effects of the organisms in question, which in turn must balance
their detrimental impacts and their beneficial
influences. However, once an invasion has
occurred, research efforts are usually oriented
towards the assessment of damage, whereas positive effects, which are sometimes significant, often receive little attention.
Just as not all non indigenous species have
large effects (Byers et al. 2002), very similar
invaders can have different net effects in different
areas. In the case of L. fortunei, data on the
ecologically very similar D. polymorpha have
proven very useful for defining potential relationships with other components of the ecosystem and identifying fruitful lines of research.
However, these similarities may be misleading
when attempting to extrapolate D. polymorpha’s
known impacts on European and North American waterbodies to L. fortunei in South America.
Both from the physical and biological viewpoints, and from the socio-economic perspective,
South America is very different from Europe and
North America. Thus, one should not take it for
granted that the adverse effects of the zebra mussel in the northern hemisphere are a solid basis
for forecasting the impacts of L. fortunei
elsewhere.
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