Manayunkia speciosa Leidy (Polychaeta: Sabellidae): introduction of this nonindigenous species in the Neotropical Region (Uruguay river, South America)

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.


Introduction
Manayunkia speciosa Leidy (Sabellidae, Fabriciinae) 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 redescribed 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 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(Bartholomew et al. , 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°5,018 0 S 58°12,647 0 W; 33°5,205 0 S 58°2 2,415 0 S; 33°5,940 0 S 58°25,202 0 W; 33°7,441 0 S 58°22,968 0 W, 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 lS cm -1 (from 46.7 to 177 lS cm -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 deposited 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 (1858Leidy ( , 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 in sparse numbers, indicates that the population is capable of carrying out the initial phases of reproduction.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, overexploitation 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 intensive 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 environments 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 establishing whether this introduction of the polychaete is recent or not; nor, given the current state of knowledge, can we predict whether or not M. speciosa, as a new invasive species, would be especially aggressive in South American ecosystems.
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 nevertheless escaped notice either because of the polychaete'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.