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Abstract

We report the migration of Manayunkia speciosa from its distribution in North America into the Neotropical Region (Argentina). We collected specimens from November 2007 to March 2009 in the lower Uruguay River-at 33° 5.01′S 58° 12′W, 33° 5.9′S 58°25.2′W from sediments reaching densities of 2,890 ind. m−2, at a mean abundance of 350 ind. m−2. Introductions of nonindigenous species, resulting intentionally or accidentally from anthropic activities, cause significant changes in ecosystems. In aquatic environments, polychaetes are a key invasive group that increases the geographical range of several species through human activities. M. speciosa may have reached the Río de la Plata Basin through a shipping vector and thereafter the Uruguay River by self-navigation. Keywords Manayunkia speciosa –Polychaeta–First record–Uruguay river–Neotropical Region
INVASION NOTE
Manayunkia speciosa Leidy (Polychaeta: Sabellidae):
introduction of this nonindigenous species in the Neotropical
Region (Uruguay river, South America)
Laura C. Armenda
´riz Analı
´a Paola
Alberto Rodrigues Capı
´tulo
Received: 15 June 2010 / Accepted: 5 July 2010 / Published online: 15 July 2010
ÓSpringer Science+Business Media B.V. 2010
Abstract We report the migration of Manayunkia
speciosa from its distribution in North America into the
Neotropical Region (Argentina). We collected speci-
mens from November 2007 to March 2009 in the lower
Uruguay River-at 33°5.010S58°120W, 33°5.90S
58°25.20W from sediments reaching densities of 2,890
ind. m
-2
, at a mean abundance of 350 ind. m
-2
.
Introductions of nonindigenous species, resulting inten-
tionally or accidentally from anthropic activities, cause
significant changes in ecosystems. In aquatic environ-
ments, polychaetes are a key invasive group that
increases the geographical range of several species
through human activities. M. speciosa may have reached
the Rı
´o de la Plata Basin through a shipping vector and
thereafter the Uruguay River by self-navigation.
Keywords Manayunkia speciosa
Polychaeta First record Uruguay river
Neotropical Region
Introduction
Manayunkia speciosa Leidy (Sabellidae, Fabricii-
nae) was first found in tubes of mud attached to
stones in the Schuylkill River (Pennsylvania) by
Leidy in 1858. At a new location, the Egg Harbor
River (New Jersey), the species was later described
in the first complete record of a strictly fresh-water
polychaete and one closely related to the marine
genus Fabricia (Leidy 1883). New specimens were
then collected from these sites by Potts (1884) and
Foulke (1884), and some 45 years later, by Meehean
(1929) in the Duluth, Wisconsin Harbor (Lake
Superior). A decade afterwards, Krecker (1939)
found specimens of Manayunkia in Lake Erie and
considered that this material belonged to the same
species as had been collected by Meehean (1929)
from Lake Superior, yet differed sufficiently to be
considered a separate species from M. speciosa.
This author then gave the name of M. eriensis for
the Great-Lakes specimens. Hartman (1951), in a
review of the subfamily Fabriciinae, indicated
that M. eriensis Krecker might be the same as
M. speciosa Leidy. Pettibone (1953) finally rede-
scribed the species and placed M. eriensis in
synonomy with M. speciosa.
In subsequent years, additional specimens of
M. speciosa were collected from a wider area
extending from Lake Superior (Michigan, Wisconsin)
to California and Oregon (Pettibone 1953). The
species was then recorded in new localities, such as
L. C. Armenda
´riz (&)A. R. Capı
´tulo
Instituto de Limnologı
´a Dr. Rau
´l A. Ringuelet
(ILPLA-CONICET La Plata-UNLP), CC 1888
La Plata, Argentina
e-mail: larmendariz@ilpla.edu.ar
L. C. Armenda
´riz A. Paola A. R. Capı
´tulo
Facultad de Ciencias Naturales y Museo,
UNLP, La Plata, Argentina
A. R. Capı
´tulo
Consejo Nacional de Investigaciones Cientı
´ficas
yTe
´cnicas (CONICET), Buenos Aires, Argentina
123
Biol Invasions (2011) 13:281–284
DOI 10.1007/s10530-010-9838-0
Lake St. Clair (Ontario, Michigan), St. Marys
River (Ontario, Michigan), the Sevenmile Canal
(Oregon), two lakes in northern Alaska, the Ottawa
River, Cayuga Lake (New York), Simmon’s Bayou
(Mississippi), besides being collected again in
Lake Erie (Hiltunen 1965; Britt 1965; Hazel 1966;
Holmquist 1967; Mackie and Qadri 1971; Spencer
1976; Croskery 1978; Brehm 1978). Its distribution
by that time covered the east- and west-coast river
systems of North America, the Great Lakes region,
and the coast of the Gulf of Mexico.
In more recent years, the studies on M. speciosa
have focussed on aspects of its population dynamics,
reproductive biology, and the role of the species as an
intermediate host for Myxozoan parasites of the
salmonids Ceratomyxa shasta and Parvicapsulum
minibicornis (Bartholomew et al. 1997,2006;
Stocking and Bartholomew 2007; Wilzbach and
Cummins 2007).
As stated above, to date this species has only been
recorded in freshwater habitats of the Nearctic
Region, from Alaska to the coast of the Gulf of
Mexico (Spencer 1976; Brehm 1978; Rouse 1996;
Stocking and Bartholomew 2007; Glasby and Timm
2008; Glasby et al. 2009). The purpose of this report
is to document the first record for M. speciosa in the
Neotropical Region, thus extending the limit of its
distribution from the United States to Argentina and
as such representing the southernmost localization of
this species within the Americas.
Material, methods and results
The Uruguay River, arising in Geral Mountain,
Brazil, is one of the longest South American rivers
and along with the Parana
´River and its tributaries
unite with the Rı
´o de la Plata river in the Del Plata
basin. The 1,770-km length of the Uruguay River
serves as the border between Argentina and Brazil,
and further downstream between Argentina and
Uruguay. The uses of its waters include navigation,
power generation, fishing, and recreation.
For the study we conducted 5 samplings seasonally
between November 2007 and March 2009 in the
lower Uruguay River. The area of study was located
at 33°5,0180S58°12,6470W; 33°5,2050S58°
22,4150S; 33°5,9400S58°25,2020W; 33°7,4410S
58°22,9680W, near a pulp factory and covered the
main channel, the bays, and the reed beds along the
banks of the river. The material was collected with
dredges and fixed in situ with 5% formalin, and
physicochemical variables were recorded during each
sampling date.
The sediments from the study area were mainly
plastic silty clay with small proportions of scarcely
sorted quartz sand (Iriondo and Kro
¨hling 2004). The
values for the physicochemical variables measured
were very similar between the different habitats
analyzed, with the turbidities and conductivities
exhibiting their widest range in these areas. The mean
physicochemical variables registered were: water
temperature, 20.0°C (with variation between 9.7 and
30.1); depth, 4.0 m (between 0.9 and 9.6 m); turbidity,
68.4 UTN (from 13 to 185.2 UTN); conductivity,
64.4 lScm
-1
(from 46.7 to 177 lScm
-1
); pH, 8.1
(between 7.3 and 9.3); and dissolved oxygen,
8.9 mg l
-1
(from 7.2 to 12.8 mg l
-1
).
In the laboratory the samples were washed on a
sieve of 0.5-mm mesh size. The material thus
obtained was stained with erythrosin, picked out of
the sediment under a stereoscopic microscope, and
identified by light microscopy. The specimens were
preserved in 70% aqueous alcohol. Some of the
individuals were measured (total length, maximum
width, thorax and abdomen length, and length of the
radioles) under an Olympus model CX31 compound
microscope.
A total of 360 individuals of M. speciosa were
collected during the study. These specimens are depos-
ited in the Coleccio
´n Argentina de Invertebrados,
Museo Argentino de Ciencias Naturales Bernardino
Rivadavia (MACN-In 37788), Argentina.
The general description of the specimens collected
from the Uruguay River coincided with that made by
Leidy (1858,1883) and Pettibone (1953). The lengths
of the thoracic segments, except for the first, were
regular and greater than the widths. The abdominal
segments were much shorter and narrower than the
thoracic. The mean total length and maximum width
coincided with those observed by Leidy (1883)and
were lower than those obtained by Pettibone (1953).
The anal segment, or pygidium, is short, rounded, and
without eyespots. Both males and females were present,
and two females were found with eggs (in March 2009).
Manayunkia speciosa was found in sediments at
densities reaching as high as 2,890 ind. m
-2
(in June
2008). The presence of egg-bearing females, although
282 L. C. Armenda
´riz et al.
123
in sparse numbers, indicates that the population is
capable of carrying out the initial phases of reproduc-
tion. The fauna accompanying M. speciosa in
this study was represented by the following taxa:
Nematoda; Oligochaeta; Bivalvia and Gastropoda
molluscs; Ostracoda; Caenida, Chironomidae, and
Elmidae insects.
Discussion
Introductions of nonindigenous species are widely
thought to be one of the most powerful direct drivers of
biodiversity loss and/or alteration in ecosystems,
together with habitat and climate change, overexploi-
tation of species, and pollution. Inland waters in
particular are highly susceptible to either inadvertent
or deliberate introductions of species and to the
subsequent spread of the new arrivals through inten-
sive human use, the natural linkages among streams
and lakes, and the dispersal capability of aquatic
organisms. Biological invasions are not a phenomenon
caused only by human activities, but the number of
species involved and the frequency of their relocation
have grown enormously as a direct result of the
expansion of trade and transport (Penchaszadeh 2005;
El Haddad et al. 2007; Ciutti and Cappelletti 2009).
The transfer of alien species in aquatic environ-
ments may occur by different mechanisms, including
transport by maritime vessels through hull fouling or
in the ballast tanks. Accordingly, the scattered
distribution of M. speciosa in the Nearctic region
has in the past attracted the attention of certain
authors (Meehean 1929; Brehm 1978) who suggested
that the species may have been introduced to some of
its new locations in the ballast tanks of ships.
Polychaetes are a significant group within the list of
invasive organisms, the geographical range of several
of whose species has been increased through human
activities (Penchaszadeh 2005; El Haddad et al. 2007;
Glasby and Timm 2008).
We therefore suppose that M. speciosa arrived at the
Del Plata Basin through shipping as a vector and thus
reached the Uruguay River as part of the usual
navigation route. We still have no criteria for estab-
lishing whether this introduction of the polychaete is
recent or not; nor, given the current state of knowl-
edge, can we predict whether or not M. speciosa,asa
new invasive species, would be especially aggressive
in South American ecosystems.
In South America, the system of the Rı
´odela
Plata and its adjacent sea area is hardly immune to
the problem of biological invasions. Among the
exotic species recorded in these areas can be cited
Ficopomatus enigmaticus (Fauvel, 1923); Balanus
glandula Darwin, 1854; B. amphitrite Darwin, 1854;
Crassostrea gigas (Thumberg, 1793), Corbicula
fluminea (Mu
¨ller, 1774), Limnoperna fortunei (Dun-
ker, 1857) and Rapana venosa (Valenciennes, 1846),
several having been more recently introduced during
the decades of the 80 s and 90 s (Penchaszadeh
2005).
In agreement with several authors (Pettibone 1953;
Hazel 1966; Spencer 1976; Brehm 1978; Stocking
and Bartholomew 2007), we further believe that
M. speciosa may have a geographical distribution
beyond the Nearctic Region, but might have never-
theless escaped notice either because of the poly-
chaete’s small size, its semitransparent body, its
tendency to gather and coat its body with fine
material; or simply because of inadequate collection
methods. We would also speculate that this species
could pass unnoticed because of its low population
densities (Pettibone 1953; Brehm 1978). Most of the
existing records have been based on only a few
individuals, with the exception of Hiltunen (1965),
who reported more than 45,000 ind. m
-2
in the
mouth of the Detroit River. The mean abundance
recorded by us in the present study, however, was
intermediate at about 350 ind. m
-2
. The extent of this
polychaete’s further dispersion within this portion of
the Neotropical region remains to be investigated.
Acknowledgments We would like to thank Dr. Donald
Haggerty for the English translation of the manuscript.
Scientific contribution No 888 from the Instituto de
Limnologı
´a ‘‘Dr. Rau
´l Ringuelet’’.
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... At first these specimens were determined as Manayunkia speciosa Leidy, 1858. It was assumed that this species could have been introduced into the Uruguay River from North America by human activities (Armendáriz et al. 2011(Armendáriz et al. , 2012. Later, the morphology of this species was described in detail (Paola et al. 2013). ...
... The specimens were fixed in 5 % formalin and preserved in 70% EtOH. For more details see Armendáriz et al. (2011) and Paola et al. (2013). For SEM studies, specimens were dehydrated in a critical point drier (K850 EMITECH), attached to a stub and sputtercoated with gold palladium. ...
... The main companion taxa were the mollusks Limnoperna fortunei, Corbicula fluminea (both are invasive species in America), Heleobia sp., Potamolithus sp., and also oligochaetes, ostracods and insects (Chironomidae, Elmidae and Caenis sp.). For more details see Armendáriz et al. (2011Armendáriz et al. ( , 2012. ...
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Freshwater polychaetes are relatively rare and little-studied members of the benthos of lakes and rivers. We studied one polychaete species (Manayunkia speciosa) in Lake Erie near the mouth of the Detroit River. Abundances at one site were determined between 1961 and 2013 and life‐history characteristics at two sites were determined seasonally (March–November) in 2009–2010 and 2012–2013. Life‐history characteristics included abundances, length‐frequency distributions, presence/absence of constructed tubes, sexual maturity, and number and maturation of young of year (YOY) in tubes. Long-term abundances decreased in successive time periods between 1961 and 2003 (mean range = 57,570 to 2583/m²) but few changes occurred between 2003 and 2013 (mean = 5007/m²; range/y = 2355–8216/m²). Seasonal abundances varied substantially between sites and years, but overall, abundances were low in March–April, high in May–August, and low in September–November. Although reproduction was continuous throughout warmer months, en masse recruitment, as revealed by length–frequency distributions, occurred in a brief period late‐June to mid-July, and possibly in early-September. All life history characteristics, including tube construction, were dependent on water temperatures (> 5 °C in spring and < 15 °C in fall). These results generally agree with and complement laboratory studies of M. speciosa in the Pacific Northwest where M. speciosa hosts parasites that cause substantial fish mortalities. Although abundance of M. speciosa near the mouth of the Detroit River was 33-fold lower in 2013 than it was in 1961, this population has persisted for five decades and, therefore, has the potential to harbor parasites that may cause fish mortalities in the Great Lakes.
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This paper reviews the alien polychaete species in the world’s oceans and their impacts on the marine ecosystems and humans. A total of 292 polychaete species belonging to 164 genera and 39 families have been transported around the world’s oceans with human-mediated assistance. Almost 15% of total number of known polychaete genera and 3.4% of total number of species are included in this phenomenon. A total of 180 species have become established in the world’s oceans and 31 species (casual species) have a potential to establish viable populations in a new location. The most speciose genera are Hydroides (16 species) and Polydora (16 species), both accounting for 10% of the total number of alien species. The families Spionidae (53 species) and Serpulidae (46 species) have the highest number of alien species. The Mediterranean Sea (134 species), and the coasts of the Hawaii Islands (47 species) and the USA Pacific (34 species) have been intensively invaded by alien polychaetes. The origins of alien species vary among regions. Alien polychaete species in the Mediterranean Sea mostly originated from the Red Sea and Indo-Pacific areas. Benthic habitats of the areas between 408N and 408S were colonized by polychaetes mostly originating from other tropical and subtropical regions. The Suez Canal and shipping are the major vectors for species introductions. Some species imported and exported as fishing baits have become established at nonnative localities. The invasive polychaete species have greatly altered habitat structures in some areas, restructured the food webs, and created important economic problems.
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Several specimens of a polychaete worm, Manayunkia speciosa Leidy, were found during a limnological survey of the Ottawa River. The specimens occurred only in substrates composed of silt and sand and in moderately moving waters. They were not found in the polluted areas of the Ottawa River. An up-dated record of the species in North America, from 1858 to the present, is also given.
Article
An annotated checklist and bibliography of 197 species (representing 78 genera and 26 families) of non-marine polychaetes of the world is presented, including synonymies, information on ecology, distribution, habitat, and references to the taxonomic and biological literature. Over half (57%) of the checklist species are represented by just three families as follows: Nereididae (61 species including Namanereis, Namalycastis, Neanthes and Hediste), Aeolosomatidae (27 species, mostly Aeolosoma) and Sabellidae (24 species including Caobangia and Manayunkia). Other well-represented taxa are the epizoic histriobdellid Stratiodrilus (11 species), the inland-sea-specialist ampharetid Hypania and related genera (5 species), and the freshwater-tolerant spionid Marenzelleria (5 species). One new combination is proposed for the nereidid Nereis tenuipalpa Pflugfelder, 1933, viz. Paraleonnates tenuipalpa n. comb.
Article
Author Institution: Department of Zoology and Entomology, The Ohio State University, Columbus, Ohio 43210
Article
An annotated checklist and bibliography of 197 species(representing 78 genera and 26 families) of non-marine polychaetes of the world is presented, including synonymies, information on ecology, distribution, habitat, and references to the taxonomic and biological literature. Over half(57%) of the checklist species are represented by just three families as follows: Nereididae(61 species including Namanereis, Namalycastis, Neanthes and Hediste), Aeolosomatidae(27 species, mostly Aeolosoma) and Sabellidae(24 species including Caobangia and Manayunkia). Other well-represented taxa are the epizoic histriobdellid Stratiodrilus(11 species), the inland-sea-specialist ampharetid Hypania and related genera(5 species), and the freshwater-tolerant spionid Marenzelleria(5 species). One new combination is proposed for the nereidid Nereis tenuipalpa Pflugfelder, 1933, viz. Paraleonnates tenuipalpa n. comb.
Article
Author Institution: Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon.
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The fresh-water polychaete Manayunkia speciosa Leidy was found in Cayuga Lake, New York, in depths of ca. 20 m or less. It was common in the northern and southern areas of the lake where densities of more than 1,000/sq. m were found occasionally. Past and recent distributional records and the small size of the species suggest a much broader distribution in the Nearctic region than is presently known.
Article
Relationships amongst the various clades of fabriciin sabellids are largely unresolved. One potential solution is to introduce further characters, as well as to describe new species. In this paper characters based on reproductive system are used in descriptions of two new species of Fabriciola Friedrich and a new species of Manayunkia Leidy from Papua New Guinea. Fabriciola is identified by the presence of non-vascularized, ventral filamentous appendages, but there are two distinct groups of species within the genus. The new species Fabriciola cri n. sp., and F. minuta n. sp., reflect this heterogeneity, Fabriciola cri, having red peristomial and pygidial eyes, and pin-head chaetae, is unusual in having spermathecae in the radiolar crown of females. Fabriciola minuta has black peristomial and pygidial eyes and a distinctive peristomial collar also seen in F. baltica Friedrich, F. liguronis Rouse and F. parvus Rouse. Fabriciola minuta is the first fabriciin described, apart from species in Brandtika Jones and Monroika Hartman, to have only two abdominal chaetigers as an adult. It has spermathecae in the radiolar crown of females that resemble those found in Manayunkia species. A new species of Manayunkia, M. mizu, resembles other species in this genus in having pseudospatulate inferior notochaetae in thoracic chaetigers 2–5. It also has spermathecae in the radiolar crown (in females), a total of 14 pinnules and a small number of thoracic uncini per fascicle.
Article
The abundance and distribution of the freshwater polychaete, Manayunkia speciosa, in 1961, are described for western Lake Erie. Previous records reveal that the species has either been generally overlooked or presently its numbers have greatly increased in the area considered. Although annelids of the class Polychaeta live predominantly in marine and brackish environments, a few species occur in fresh water. One freshwater species, Manayunkia speciosa Leidy, was first discovered in the Schuylkill River, Pennsyl- vania, by Joseph Leidy (1858), and first reported from the Great Lakes (Duluth, Minnesota, harbor, western Lake Superior) by Meehean (1929). Individuals of this genus were later collected and described from Lake Erie, east of the Bass Islands, by Krecker (1939). He believed them to be specifically different from the worms found previously in the United States, and proposed the name M. eriensis. Additional specimens were recorded from this general area by Pettibone (1953), who, following the interpretation of Hartman (1951), considered them to be M. speciosa and relegated M. eriensis to synonomy. Through personal communica- tion with Dr. N. Wilson Britt, I have learned that he recorded this species from western Lake Erie in 1954. M. speciosa was found from Lake Erie again in 1961, when personnel of the U.S. Bureau of Commercial Fisheries collected samples for a study of the benthos of the extreme western end of the lake. This species was found in many of the samples—often in great numbers (fig. 1). It was most abundant at a station in the mouth of the Detroit River where one station yielded an average of 45,292 per square meter. One sample with a Petersen dredge (approximate area of 1/14 m2) contained more than 6,530 worms. Such abundance is in sharp contrast to findings in the earlier studies. Pettibone (1953) reported "Some 23 specimens. . . ."; Krecker (1939) found a single specimen originally and "additional specimens" later; and Wright (1955) reported no polychaetes in his 1928-30 study of the bottom fauna of western Lake Erie and the mouth of the Detroit River. Wright's study and the 1961 survey by the Bureau of Commercial Fisheries covered the same area and had many stations in common. To wash the bottom samples, Wright used even smaller mesh screening materials (0.5 mm) than were used in the 1961 study (ca. 0.65 mm, U.S. Standard No. 30). Wright is of the opinion (personal communication) that a few individuals could have been overlooked because of the low magnification used in sorting his samples, but that it is unlikely that the worms would have escaped notice if they had been abundant. The distribution and frequency of occurrence of M. speciosa in western Lake Erie apparently is influenced by the Detroit River and its outflow. The species was not found off the mouth of the Maumee River. This wide variation in popula- tion density may be due to differences in sediment type, nature of the currents, water quality, or other factors. Although organic substances are known to favor the occurrence of certain marine polychaetes (Reish, 1960), the possible