Mysids from the Río de la Plata Estuary, with new record of Mysidopsis rionegrensis, Hoffmeyer 1993, and Promysis atlantica Tattersall, 1923 (: )

GUILLERMO CERVETTO1*, RAFAEL CASTIGLIONI2, LAURA RODRÍGUEZ-GRAÑA3 & DANILO CALLIARI2.3 1 Dirección Nacional de Medio Ambiente. Ministerio de Vivienda, Ordenamiento Territorial y Medio Ambiente, Galicia 1133, CP 11000 Uruguay. 2 Universidad de la República, Facultad de Ciencias, Oceanografía y Ecología Marina, Uruguay. Iguá 4225, CP 11000, Montevideo, Uruguay. 3 Universidad de la República, Grupo Ecología Funcional de Sistemas Acuáticos – CURE, Uruguay. Ruta Nacional nº 15 km 28.500, CP 27000, Rocha, Uruguay. *Corresponding autor: [email protected]

Abstract. We report four species of Mysida collected in open waters of the Río de la Plata Estuary (RPE) during spring and autumn 2001: americana, Mysidopsis tortonesei, M. rionegrensis and Promysis atlantica; for the latter two this is the first report for RPE and represents an extension in their known distribution ranges. Keywords: Mysidacea, South-Western Atlantic, distribution

Resumen. Misidáceos del estuario del Río de la Plata, incluyendo el nuevo registro de Mysidopsis rionegrensis Hoffmeyer 1993 y Promysis atlantica Tattersall, 1923: Se reportan cuatro especies de Mysidacea colectadas en aguas abiertas del estuario del Río de la Plata en otoño y primavera del 2001: Neomysis americana, Mysidopsis tortonesei, M. rionegrensis y Promysis atlantica. Para las dos últimas éste constituye el primer reporte para el Río de la Plata, y representa una extensión en el rango de distribución conocido. Palabras clave: Mysidacea, Atlantico Sudoccidental, distribución

Introduction a mean annual fresh water flow of 23000 m3 s-1 that Mysids inhabit diverse aquatic habitats but are constitutes the main point source of fresh water particularly abundant in estuaries and marine coastal input in the South Atlantic Ocean. General studies waters (Mauchline & Murano 1977, Mauchline on the plankton of the RPE are scarce, and in 1980, Morgan 1982, Wooldridge 1983, Cunha et al. particular the mysid fauna is poorly known (Murano 1999). They are core components in trophic webs 1999, Calliari et al. 2003, Miyashita & Calliari which actively consume phytoplankton and 2014). Neomysis Americana (Smith 1873) and zooplankton (Fulton III 1982a, b, Takahashi 2004) Mysodopsis tortonesei (Bacescu 1968) are so far the and transform organic detritus into biomass for two mysid species known to inhabit this ecosystem higher consumers (Zagursky & Feller 1985, Corey (Schiariti et al. 2004, 2006, Calliari et al. 2007). N. 1988). In turn mysids are food for several fish and americana was the first species reported for this bird species (Moran & Fishelson 1971; McDermott, estuary nearly 40 years back (Gonzalez 1974), and 1983, Wooldridge 1989; Carlson et al. 1997, since then only a handful of studies have focused on Takahashi et al. 2004). this group (Viñas et al. 2005, Schiariti et al. 2004, The Río de la Plata Estuary (RPE) is a 2006, Calliari et al. 2007). Improved knowledge of large-scale, shallow (average ca. 10 m) and turbid the mysid fauna of the RPE is arguable needed in estuarine environment (Guerrero et al., 1997). It has view of the significance of mysids in the diet of

Pan-American Journal of Aquatic Sciences (2016), 11(3): 179-187 180 G. CERVETTO ET AL. small juvenile fish (Sardina & Lopez-Cazorla 2005, Specimens were dissected and observed under a Rodríguez-Graña et al. 2008) and of their dissecting microscope (7 – 40X) and at high importance in this system which serves as nursery magnification with an inverted microscope ground for several important fish species (Martínez (40-200X). & Retta 2001, Acha et al. 2008). This study updates the knowledge of the order Results and Discusion Mysida from the RPE with the inclusion of two The analysis of whole samples corresponding further taxa to the species list, along with to both cruises resulted in four mysids species environmental information associated to their identified (Table I). N. Americana was identified and occurrence and a description of morphological described again, according to descriptions by Smith features that can prove useful as a quick diagnosis (1873) for Mysis americana, and Zimmer (1904), tool for proper identification by aquatic ecologists Cronin et al. (1962), Williams (1972), Calliari et al. without specific expertise in the of this (2001) and Schiariti et al. (2006) for N. americana. group of . Mysidopsis tortonesei had a new description by Bacescu (1968a) for M. californica, and Bacescu Materials and Methods (1968b), Brattegard (1969) and Almeida-Prado Two cruises were performed on board R/V (1972) for Mysidopsis tortonesei. Mysidopsis Aldebarán from 17th to 19th May, 2001 (cruise 1, rionegrensis was identified according description of austral fall) and from 17th to 19th November, 2001 Hoffmeyer (1993) and Promyis atlantica following (cruise 2, spring) (Fig. 1). Depth of stations ranged description of Tattersall (1923, 1951), Illig (1930), , between 6 and 36 m. Zooplankton samples were Clarke (1956), Costa (1964) and Almeida Prado collected by oblique tows of a Bongo net (19 cm (1972). diameter) fitted with a 85 μm pore-size; length and Neomysis americana Smith 1873 (Fig. 2a) angle of the cable were manipulated to ensure the Diagnosis: Our observations agreed closely with net sampled most of the water column, i.e. from 1-2 González (1974). Eyes elongated, ca. 1.5 times m above the bottom and upwards. Samples were longer than wider with cornea representing about preserved in buffered formaldehyde 5% final half of the eye surface. Antennal scale lanceolated, concentration. At the laboratory mysids were picked with small setae on both margins and 8-10 times out from whole samples and identified based on longer than wider. Telson triangle-shaped, ca. 2.5 Almeida-Prado (1974), González (1974), Mauchline times longer than wider at the base and ending in (1980), Hoffmeyer (1993), and Murano (1999).

Figure 1.- Map of the study area showing location of sampling stations. Open circles correspond to hydrographic (CTD) stations; full circles correspond to hydrographic and plankton stations; full triangles correspond to positive stations with presence of mysids.

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Table I.- Species of mysids found in the Rio de la Plata estuary during autumn and spring 2001. Family Subfamily Genus Species Reference Mysidae Leptomysinae Mysidopsis tortonesei Bacescu 1968 Mysidopsis rionegrensis Hoffmeyer 1993 Promysis atlantica Tattersall 1923 Mysinae Neomysis americana Smith 1873, fide Zimmer 1909 two strong external spines framing two smaller harbour (Gonzalez 1974). N. americana has been internal spines. Lateral margins of telson with one recently reported as invasive on the Eastern Atlantic, robust spine (longer and wider at its base) every 1-3 in coastal waters from the Netherlands (Wittmann et smaller spines (pattern most evident in the distal half al. 2012). of the telson). Uropods with setae on both margins; In South America, N. americana is currently exopodite of uropodes 1.5 times longer than common in southern Brazilian, Uruguayan and endopodite. A conspicuous chromatophore present in northern Argentinean coasts (Hoffmeyer 1990, Viñas the marsupium of brooding females. et al. 2005; Calliari et al. 2001; Schiariti et al. 2004, Neomysis americana was the most abundant Cervetto et al. 2006, Calliari et al. 2007, Cardelli et mysid species recorded in both spring and autumn al. 2006). cruises. It occurred in oligo- to polihaline conditions Mysidopsis tortonesei Bacescu 1968 (Fig. 2b) in the range <1 to 33.37, but was most abundant at Diagnosis: Morphology in accordance with salinities <28, with a clear preference for salinities description by Almeida-Prado (1974). Globular between 15 and 20 (Calliari et al. 2007); spatial round eyes with small lateral projection over distribution of N. americana in the RPE has been peduncular structures. Antennal scale lanceolated shown to be associated with the bottom salinity front with setae all along the margin. First five abdominal (Schiariti et al. 2006). segments with conspicuous chromatophores. Telson N. americana was present in 55% of samples almost twice as long as wide at the base, quickly and 77% of individuals found were juveniles. Sex narrowing near the base but then narrowing very ratio (female:male) was skewed towards females smoothly until the distal. At its base, the telson (71%, F:M ratio = 2.4), similarly to findings by presents three spines on each side, then a short Viñas et al. (2005) on the Argentinean sector of the naked segment of the margin follows, after which a estuary (Samborombón Bay), although the fraction number of ca. 20 spines are present which increase of brood-carrying females was higher in our study in length and width from proximal to distal (77%) compared to the former one (20%). In the extremes. The distal end of telson is round shaped present study spawners were nearly always present and with two pairs of strong and long spines. in samples corresponding to middle and upper Exopod of uropods with setae along the whole estuarine stations. margin. Endopod of uropod with spines along the This species appears to have a disjunct whole margin. distribution along the Atlantic coast of the Americas Mysidopsis tortonesei has been found in (Miyashita & Calliari 2014): it is found in coastal several sites along the Brazilian coast including waters from Canada (ca. 46º N, Prouse 1986) and Paraıba, Sao Paulo, Parana, and Rio Grande do Sul the USA down to ca. 41º N (Brown et al. 2005), 37º (Miyashita & Calliari 2014 and references therein). N (Hulburt 1957, Herman 1963), 35º N (Williams For the RPE it was first reported in 2004 (Schiariti 1972), and 30º N (Williams et al., 1974). It is absent et al. 2004). from Mexican, Central America and northern South In the current sets of samples M. tortonesei American coastal waters, but found again at lat. ca was most abundant during the autumn cruise when it 30ºS (Tramandaí, Brazil). On South Atlantic waters represented 35% of total mysids collected, being N. americana is a cryptogenic species (sensu found in 41% of samples. Juvenile individuals Orensanz et al. 2002); it is not known whether it is amounted to 55%, sex ratio was 1.5 and 40% of endemic or if it was introduced from the North adult females had broods developed. These results Atlantic in the late 60’s or early 70’s, as it was first match observations by Almeida-Prado (1973) during reported in South America in 1973 at Montevideo April at Cananeia estuary, Brazil, (25º30’ S) in terms

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Figure 2.- Drawings of telsons and photographs of whole corresponding to the four mysid species collected in the Rio de la Plata waters during 2001. a.- Neomysis americana, b.- Mysidopsis tortonesei, c.- Mysidopsis rionegrensis, d.- Promysis atlantica. of juvenile to adult, and sex ratios. The fraction of evidencing a preference for salinities > 28 (Calliari brood-carrying females in samples from the RPE et al., 2007), which suggested complementary was comparable to the maximum found by spatial distribution in relation to N. americana (i.e. Almeida-Prado (1973) at Cananeia, also during almost non-overlapping). Salinity preferences at the autumn. During our study M. tortonesei was found RPE were broadly consistent with previous studies in stations closer to the outer limit of the estuary and from Brazil and the one available for this same its abundance positively correlated with salinity, ecosystem (Almeida-Prado 1973, Schiariti et al.,

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2004). At the RPE M. tortonesei was found in the nature of its occurrence in the RPE ecosystem: salinity range 16 – 31, while in Cananeia low whether individuals found here were part of a numbers occurred at salinity ca. 14 and increased population from the outskirts of the RPE, or if they strongly at salinity >25. represented individuals occasionally advected from a Mysidopsis rionegrensis Hoffmeyer 1993 (Fig. 2c) population further south. In the latter case, another Diagnosis: Morphology of animals examined issue regards the frequency and extension of such corresponded closely to description by Hoffmeyer incursions. These are aspects that deserve further (1993). Large and laterally inclined eyes. Antennal attention in next studies. scale lanceolated and slightly rounded, with the Promyis atlantica Tattersall 1923 (Fig. 2d) internal margin concave and the external slightly Diagnosis: Observations of individuals from the convex. Telson widest at its base, streching to ca. 1/3 RPE closely resembled descriptions by of maximum width near the distal end, but then Almeida-Prado (1974), unless otherwise noted. slightly widening until the distal end; a pair of Conic eyes on a long cylindrical pedunculum, in a chromatophores are present at the basal region. position nearly perpendicular to the main Margins of telson result concave-shaped and have antero-postero body axis. Lanceolated scale with short spines. Distal region of telson rounded and fine setae along the whole margin. Telson linguiform with robust spines. Exopod of uropod with long ca. 2.5 times as long as broad and with a cleft setae on both margins, endopod of uropods with without spinules or setae nearly one sixth the length short setae on both margins and large statocyst. of the telson; spines present along external margins Previous records of Mysidopsis rionegrensis of the telson which increase in robustness from restrict its distribution to the location of first proximal to distal end, finishing with two strongest description, the San Matías Gulf (Hoffmeyer 1993) spines. The number of spines (22-25) corresponded and Nuevo Gulf (Menendez et al. 2011), as well as with that described by Almeida-Prado and diverges to Buenos Aires Atlantic coastal waters (Schiariti et from Tattersall (1923; fide Almeida-Prado 1974) and al., 2004). Clarke (1956), differences already discussed by In the present set of samples M. rionegrensis Almeida-Prado (1974). A slight difference between was found during the spring cruise when only three our observations and Almeida-Prado is that in our specimens were collected in the outermost region of specimens the series of spines on the margins of the the RPE. Individuals found corresponded to 1 male telson do not start from the base but in the proximal and 2 females. third of the telson length. Endopod of uropod with This species was first described for the San large statocyst and inner margin armed along its Matias Gulf (41°S, Argentina) during the spring length with spines of varying size. Exopod of season (Hoffmeyer 1993). The location of first uropods with setae along its whole length. description suggested this was a primarily marine The known distribution of this species is also species living under high salinities and moderately of a discontinued type with occurrences on the cold waters. More recently M. rionegrensis was Atlantic coast of both (North and found during a spring cruise at a location slightly South Carolina, ca. 32 -35º N, Clarke 1956, Wigley north of Golfo de San Matías (El Rincón, ca. 39º S; & Burns 1971, Williams 1972; and Texas, ca. 28ºN Schiariti et al. 2004) in a temperature range of 13 to Price 1982) and South America (Rio de Janeiro, 18 ºC and salinities from 33.7 to 33.9. Governador Island, Tramandaí, latitudinal range 23 - This is the first report of the occurrence of M. 30º S; Tattersall 1923, Costa 1964, Almeida-Prado rionegrensis in the RPE, which extends its known 1973, 1974, Tavares & Bond-Buckup 1990), and distribution range nearly 5º latitude northwards. Lagoa dos Patos estuary (Gama 2008) . During our study M. rionegrensis occurred at In the current set of samples Promysis temperatures between 16.8 - 18.2 ºC and salinities atlantica was found during the autumn cruise, also between 23.2 - 29.7. These are similar thermal in very low abundances, mostly adult males and one conditions to those observed by Schiriati et al. juvenile. The present study is the first report on P. (2004); however, in RPE M. rionegrensis occurred at atlantica in the RPE and represents and extension of salinities much lower than previously reported for ca. 5º latitude to the south of its formerly known this same species, suggesting it has important southernmost occurrence. At the RPE P. atlantica tolerance to relatively diluted salinities. The low was found at a salinity range of 20 – 21 and number of specimens collected precludes definite temperatures from 14 to 15 ºC, well below the statements, though. The same holds as regards the temperature range reported for this same species in

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Brazilian waters (19 – 27ºC, Almeida-Prado 1973). the South Atlantic. Pp 1-42. In: Boltovskoy, As commented for M. rionegrensis, further D. (Ed.) South Atlantic Zooplankton, information is necessary in order to establish the Backhuys Publishers, Leiden, The temporary vs. permanent character of P. atlantica Netherlands. occurrence in RPE waters. This work adds two new species to the list of Brown, H., Bollens, S. M., Madin L. P. & Horgan, mysids from the RPE, which also implies an extension of their biogeographical distribution. One E.F. 2005. Effects of warm water intrusions on interesting aspect to note is the fact that for three out populations of macrozooplankton on Georges of four currently known mysids inhabiting RPE Bank, Northwest Atlantic. Continental Shelf (Mysidopsis tortonesei, Mysidopsis rionegrensis and Research, 25: 143-156. Promysis atlantica), this large scale estuary Calliari, D., Cervetto, G., Bastreri, D. & Gómez, M. represents (so far) either the southern or the northern 2001. Short-term variability in abundance and limit of their biogeographical distribution. That vertical distribution of the opossum-shrimp would suggest a role of the RPE as an ecological Neomysis americana in the Solís Grande river barrier for the distribution of mysid species in South estuary, Uruguay. Atlântica, 23: 117-125. Atlantic coastal waters, a pattern already Calliari, D., Defeo, O., Cervetto, G., Gomez, M., documented for other littoral or inner shelf taxa Gimenez, L., Scarabino, F., Brazeiro, A. & (Escofet et al. 1979, Gianuca 1983, Spivak 1997, Norbis, W. 2003. Marine life of Uruguay: a Boltovskoy et al. 1999). critical update and identification of priorities for future research. Gayana 67(2): 341-370. Acknowledgements Calliari, D., Cervetto, G., Castiglioni, R. & This work was partly funded by contract PDT Rodriguez-Graña, L. 2007. Salinity S/C/OP/36/10 form DINACYT, Uruguay. C. preferences and habitat partitioning between Mesones, L. Ortega and A. Martínez (Dirección dominant mysids at the Río de la Plata estuary Nacional de Recursos Acuáticos) provided (Uruguay). Journal of the Marine Biological environmental data and access to zooplankton Association of the UK, 87, 501–506. samples. Comments by three anonymous reviewers Cardelli, N. V., Cervellini, P. M. & Piccolo, M. C. contributed to improve an early version of this paper 2006. Abundancia estacional y distribución and are greatly appreciated. espacial de Mysidacea en el Atlántico sudoccidental, estuario de Bahía Blanca References (38º42’-39°26´S y 62º28’-61°40’W). Revista Acha, E. M., Mianzan, H., Guerrero, R., Carreto, J., de Biología Marina y Oceanografía 41(2): Giberto, D., Montoya N. & Carignan M. 177 –185. 2008. An overview of physical and ecological Carlson, J. K., Randall T. A. & Mroczka, M. E. processes in the Rio de la Plata Estuary. 1997. Feeding habits of winter Flounder Continental Shelf Research, 28: 1579–1588. (Pleuronectes americanus) in a habitat Almeida-Prado, M.S., 1973. Distribution of exposed to anthropogenic disturbance. Mysidacea (Crustacea) in the Cananeia Journal of North Atlantic Fisheries Science, region. Boletim de Zoologia e Biologia 21: 65-73. Marinha, Nova Serie , 30: 395-417. Cervetto, G., Calliari, D., Rodríguez, L., Lacerot, G. Almeida-Prado, M.S., 1974. Sistemática dos & Castiglioni, R. 2006. Zooplancton de Mysidacea (Crustacea) na regiao de Cananéia. ambientes costeros de Uruguay: añadiendo Boletim do Instituto Oceanografico, Sao piezas al rompecabezas. Pp 105-111. In: Paulo , 23: 47-87. Conde, D., Rodríguez, L., Scarabino, F. & Bacescu, M. 1968. Étude des quelques Leptomysini Menafra, R. (Eds.) Bases para la (Crustacea Mysidacea) des eaux du Brésil et conservación y manejo de la costa de Cuba; Description d´un genre et de cinq Uruguaya . Vida Silvestre, Uruguay. autres taxons nouveaux. Annali del Museo Clarke, W. D. 1956. A further description of Civico di Storia Naturale Giacomo Doria, Promysis atlantica Tattersall (Crustacea, 77: 232- 249. Mysidacae). Acta Musei Moraviae, (1755): Boltovskoy, D., Gibbons, M. J., Hutchings, L. & 1-5. Binet, D. 1999. General biological features of Corey, S. 1988. Quantitative distributional patterns

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Received: May 2016 Accepted: August 2016 Published: October 2016

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