Northeast Natural History Conference 2011: Selected Papers 2012 Northeastern Naturalist 19(Special Issue 6):173–180 Palaemon macrodactylus Rathbun 1902 (Oriental Shrimp) in New York: Status Revisited Barbara E. Warkentine1,* and Joseph W. Rachlin2 Abstract - Based upon studies between 2001 and 2010 and the continued presence of adult shrimp including gravid females, Palaemon macrodactylus (Oriental Shrimp) is established in the estuarine waters of New York City. In summer 2010, we sampled a 1000-m2 area of the East River and found that P. macrodactylus represented 4.3% of the total shrimp population, and 15.2% of the Palaemonidae (84.8% consisted of the native species Palaemonetes vulgaris [Common Grass Shrimp]). In 2001/2002, P. macrodactylus comprised 4.2% of all palaemonids, suggesting an increase in the past decade of non-native relative to native palaemonids. While not yet appearing to be “invasive” based upon population size, the feeding habits and reproductive biology of P. macrodactylus suggest that future interactions with native shrimp may occur. A key to regional shrimp is presented. Introduction Palaemon macrodactylus Rathbun (Oriental Shrimp), a native estuarine species of Japan, Korea, and China (Beguer et al. 2007), was first discovered outside its native range in San Francisco Bay in the 1950s (Newman 1963). Following this initial discovery, P. macrodactylus has been reported from Australia (Pollard and Hutchings 1990), England (Ashelby et al. 2004), Spain (Cuesta et al. 2004), Argentina (Spivak et al. 2006), France (Beguer et al. 2007), Germany (Gonzalez- Ortegon et al. 2007), Romania (Micu and Nita 2009), and most recently Bulgaria (St. Raykov et al. 2010). In 2010, but based on 2001 surveys, P. macrodactylus was reported for the first time on the Atlantic coast of North America in the waters of New York City (Warkentine and Rachlin 2010). The finding of P. macrodactylus in so many different locations outside its native range speaks well for its ability to tolerate differing environmental conditions (Newman 1963, Siegfried 1980). The reporting of gravid females (Beguer et al. 2007, Siegfried 1980, St. Raykov et al. 2010, Warkentine and Rachlin 2010), the finding of populations over sequential years (Beguer et al. 2007, St. Raykov et al. 2010, Warkentine and Rachlin 2010), and the expansion of their range over time (Lavesque et al. 2010, Micu and Nita 2009) indicate this animal’s ability to occupy and potentially become established in many different estuaries. The initial finding of P. macrodactylus in the estuarine waters of the Bronx River, East River, and western end of Long Island Sound occurred in 2001 1SUNY Maritime College, Science Department, 6 Pennyfield Avenue, Bronx, NY 10465- 4198. 2Laboratory for Marine and Estuarine Research (La MER), Department of Biological Sciences, Lehman College of CUNY, 250 Bedford Park Boulevard West, Bronx, NY 10468-1589. *Corresponding author - bwarkentine@sunymaritime.edu. 174 Northeastern Naturalist Vol. 19, Special Issue 6 (Warkentine and Rachlin 2010). Since this discovery, we have continued to find viable populations, indicating that this non-native shrimp has become established. It is thus desirable to continue to monitor the relative abundance of P. macrodactylus compared to that of resident shrimp populations. Palaemon macrodactylus occurs together with three other shrimp of the family Palaemonidae, Palaemonetes pugio Holthuis (Daggerblade Grass Shrimp), Palaemonetes intermedius Holthuis (Brackish Grass Shrimp), and Palaemonetes vulgaris Say (Common Grass Shrimp), and one member of the family Crangonidae, Crangon septemspinosa Say (Sand Shrimp), all of which are native species. The relative abundance of these 5 shrimp species to each other will contribute towards an understanding of P. macrodactylus’ current status in this region. Methods On 2 July 2010, a single but exhaustive survey of a 1000-m2 area of the East River in the vicinity of the SUNY-Maritime College Campus (40°48'18.85"N, 73°47'41.36"W) was conducted by a team of four individuals. The sampling was accomplished by using three 1.2-m x 1.2-m push nets each with a 0.3-cm mesh. The sampling site consisted of a shallow sandy beach front abutted on both sides by piers supported by wooden and concrete pilings. All shrimp collected were preserved in 10% formaldehyde. After a period of two weeks, the specimens were washed and transferred to 75% ethanol. Shrimp were identified using published keys (Ashelby et al. 2004, d’Udekem d’Acoz et al. 2005, Pollock 1998, Weiss 1995) and species descriptions (Rathbun 1902, Warkentine and Rachlin 2010). The collection was then sorted and enumerated. Relative abundance, expressed as percent occurrence, was calculated for P. macrodactylus relative to: 1) all shrimp collected, 2) members of the Palaemonidae, and 3) members of the Crangonidae. These data were compared to data obtained in 2001/2002 (Warkentine and Rachlin 2010). Since sample sizes were not uniform, percent occurrence was used to standardize the data for comparison purposes. Palaemon macrodactylus was sexed by the presence or absence of the appendix masculine (Fig. 1) on the endopodite of the second pleopod (Siegfried 1980) Figure 1. Endopodite of the second pleopod of Palaemon macrodactylus showing the comparison between female (A) and male (B) appendage structures. Arrow indicates the appendix masculine of the male. 2012 B.E. Warkentine and J.W. Rachlin 175 in order to determine sex ratios. These data were also compared to those obtained in 2001/2002. Keys utilized to identify members of the Palaemonidae and Crangonidae found in New York’s estuarine waters were modified to incorporate P. macrodactylus. The characteristics selected in the modification of these keys, and in constructing the new one (Appendix 1), were for the most part those that can be seen in the field. Results Table 1 presents the relative abundance of all shrimp of the family Palaemonidae from the 2001/2002 collection (Warkentine and Rachlin 2010) and is used as the basis for comparing the relative abundance (Table 2) of shrimp collected in this current study. Palaemonetes pugio was the most abundant member of the shrimp fauna, accounting for 71.7% (n = 2151) of the collection. Palaemonetes vulgaris and P. intermedius made up 15.4% (n = 462) and 8.7% (n = 261) of the collection, respectively. Palaemon macrodactylus only made up 4.2% (n = 125). Table 2 shows the results of the enumeration of the 419 shrimp taken from the 1000-m2 sampling site in the East River. Crangon septemspinosa made up the bulk of the collection at 71.8 % (n = 301). Palaemonetes vulgaris made up 23.9% (n = 100). The relative abundance of Palaemon macrodactylus was 4.3% (n = 18) of the total shrimp population, a figure comparable to its relative abundance (4.2%) in 2001/2002 (Table 1). Unlike the 2001/2002 collection, which contained all three native species of Palaemonidae (Table 1), the 2010 collection only contained P. vulgaris (Table 2). The relative abundance of P. macrodactylus to this species, in the current study, was 15.2%. While the 2001/2002 and the 2010 samples are from different sites Table 2. Relative abundance (% occurrence) of shrimp collected from the East River during 2010. Relative abundance Species Number collected (% occurrence) Crangon septemspinosa 301 71.8 Palaemonetes vulgaris 100 23.9 Palaemon macrodactylus 18 4.3 Total 419 100.0 Table 1. Relative abundance (% occurrence) of shrimp collected from the Bronx and East rivers from 2001 to 2002 (Warkentine and Rachlin 2010). Relative abundance Species Number collected (% occurrence) Palaemonetes pugio 2151 71.7 Palaemonetes vulgaris 462 15.4 Palaemonetes intermedius 261 8.7 Palaemon macrodactylus 125 4.2 Total 2999 100.0 176 Northeastern Naturalist Vol. 19, Special Issue 6 within this contiguous estuarine system, making direct comparisons problematic, it is useful to look at the values to assess the relative percentage of P. macrodactylus to the other shrimp populations at each site. Given this caveat, if one looks only at Palaemonetes vulgaris and Palaemon macrodactylus from 2001/2002, the relative abundance of P. macrodactylus is 21.3%. A further contrast to the 2001/2002 study is the presence of Crangon septemspinosa in this 2010 study. When comparing the relative abundance of P. macrodactylus to just this native shrimp a value of 6.0% was obtained. A comparison of sex ratios (Table 3) for P. macrodactylus shows that the ratio was 1.0:1.1 male to female in the 2001/2002 sample and 0.8:1.0 male to female in 2010, both sample sets approximating a 1:1 ratio. From Table 3 it can also be seen that gravid females were collected during both sampling periods. The percentage of gravid females in the 2001/2002 collection was 80% in the 2001/2002 collection and 100% in 2010. Discussion The relative abundance of P. macrodactylus to that of native shrimp is a useful metric for evaluating the species’ potential impact. The relative abundance of P. macrodactylus to native shrimp in 2010 was comparable to its relative abundance in 2001/2002 (Warkentine and Rachlin 2010). As noted above, these collections, a decade apart, came from two different locations and habitats within the same estuarine system, making direct comparison of results problematic. An examination of the two data sets (Tables 1 and 2) clearly shows a difference in species composition. The absence of Crangon from the 2001/2002 study is refl ective of the habitat from which these collections were made (wooden pilings associated with a decomposing dock), which differed significantly from the habitat from which the 2010 samples were collected. This latter site, while having pilings associated with it, consisted mostly of a shallow sandy beach, a habitat more conducive to crangonids (Gosner 1978). The original sampling site for the 2001/2002 study has undergone extensive re-construction, channelization and removal of the wooden pilings as part of the development of a community park. These modifications precluded effective re-sampling at this site during the 2010 season. The alternative site selected in 2010 is in a protected area within the SUNY-Maritime Campus and should remain undisturbed for several years, providing a consistent monitoring station for future studies. The presence of P. macrodactylus, along with the consistent occurrence of gravid females, for more than a decade indicates that this species has become established. While the concept of an “invasive species” is at present ill defined, Table 3: Male-to-female sex ratios for Palaemon macrodactylus and the percentage of gravid females collected during the two sampling seasons. Sampling period Male Female Sex ratio % of gravid females 2001/2002 59 66 1.00:1.12 80 2010 8 10 0.80:1.00 100 2012 B.E. Warkentine and J.W. Rachlin 177 it is a term that is continuously used both in the lay and scientific literature to indicate the negative impact of non-native species. Using just the metric of relative abundance, it would appear that P. macrodactylus is currently non-invasive. However, Ashelby et al. (2004) and Micu and Nita (2009) indicate that since P. macrodactylus has a greater reproductive potential and a longer life span (2–3 years) than that of native shrimp species, it could potentially have a competitive edge. The life span for the three native species of Palaemonidae found in association with P. macrodactylus in the New York City East River estuarine complex is 6 to 13 months, with a reproductive season that extends from April to October (Anderson 1985). While the reproductive seasons of the native Palaemonidae overlaps that of P. macrodactylus in this area (Warkentine and Rachlin 2010), their much shorter life span only affords them one reproductive season per generation as opposed to potentially 2–3 seasons for P. macrodactylus. This difference could contribute to an increase in relative abundance and distributional expansion of P. macrodactylus in this area over many years. On the other hand, Crangon septemspinosa has a life span equal to that of P. macrodactylus. Two- and three-year-old C. septemspinosa have been reported to move into Connecticut estuarine systems to reproduce in the spring and remain to reproduce again in the fall (Modlin 1980). The reproductive potential of C. septemspinosa is similar to that of P. macrodactylus in that they both produce two cohorts per year (Modlin 1980, Omori and Chida 1988). Since these two species have common reproductive characteristics, it would appear that neither species has a competitive reproductive advantage. However, more research would need to be done to evaluate this. While no studies have been conducted to determine if P. macrodactylus is a stronger competitor, it has been documented that it does share dietary elements with native shrimp (Beguer et al. 2007, Micu and Nita 2009, Siegfried 1982). Siegfried (1982), in looking at the dietary composition of P. macrodactylus and the native Crangon franciscorum Stimpson (California Bay Shrimp) from California waters, found dietary overlap to be >80%. Feeding habits of Palaemon macrodactylus and its native shrimp counterpart Palaemon longirostris Milne- Edwards (Delta Prawn) residing in the Guadalquivir estuary of Spain also showed strong overlap (Beguer et al. 2007). Dietary overlap between P. macrodactylus and two native shrimp, Palaemon elegans Rathke (Rockpool Prawn) and P. adspersus Rathke (Baltic Prawn), found together in the coastal regions of the Black Sea, would most likely occur if resources diminished (Micu and Nita 2009). Thus, the existence of dietary overlap between P. macrodactylus and native shrimp could result in potential competitive interactions leading to a negative impact on the native species (Ashelby et al. 2004, Gonzalez-Ortegon et al. 2010, Micu and Nita 2009). Since Palaemon macrodactylus has a high degree of dietary overlap with native crangonids and because of its potentially greater reproductive capacity when compared to other members of the Palaemonidae, there exists a need to continue to monitor the status of this population of non-native shrimp in the estuarine system of the New York Bight, as well as periodically survey for possible range 178 Northeastern Naturalist Vol. 19, Special Issue 6 expansions. Since first discovering P. macrodactylus in 2001 (Warkentine and Rachlin 2010), we have come to learn that it has been found in the estuarine waters in Mystic, CT (J.T. Carlton, Williams-Mystic Program, Mystic, CT, pers. comm.). Continuous monitoring of this species will allow for an early detection of any negative ecological impacts and also allow us to gauge any range extensions in our waters. To facilitate the monitoring of this “new” shrimp, we have developed a dichotomous key (Appendix 1), which includes Palaemon macrodactylus along with the other commonly occurring shrimp species. Acknowledgments The authors wish to acknowledge the field assistance of students from SUNY-Maritime College and Lehman College of CUNY. This project was partially supported from grants from Congressman Joseph E. Serrano’s WCS/NOAA Lower Bronx River Partnership Grants Program and a grant from the PSC-CUNY Research Award Program of the City University of New York. Literature Cited Anderson, G. 1985. 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Recent expansion of the Oriental Shrimp Palaemon macrodactylus (Crustacea: Decapoda) on the western coast of France. Aquatic Invasions 5:S103–S108. 2012 B.E. Warkentine and J.W. Rachlin 179 Mica, D., and V. Nita. 2009. First record of the Asian prawn Palaemon macrodactylus Rathbun, 1902 (Caridae: Palaemonoidea: Palaemonidae) from the Black Sea. Aquatic Invasions 4:597–604. Modlin, R.F. 1980. The life cycle and recruitment of the Sand Shrimp, Crangon septemspinosa, in the Mystic River estuary, Connecticut. Estuaries 3:1–10. Newman, W.A. 1963. On the introduction of an edible oriental shrimp (Caridea, Palaemonidae) to San Francisco Bay. Crustaceana 5:119–132. Omori, M., and Y. Chida. 1988. Life history of a caridean shrimp Palaemon macrodactylus with special reference to the difference in reproductive features among ages. Nippon Suisan Gakkaishi 54:365–375. Pollard, D.A., and P.A. Hutchings. 1990. A review of exotic marine organisms introduced to the Australian region. II. Invertebrates and algae. Asian Fisheries Science 3:223–250. Pollock, L.W. 1998. A Practical Guide to the Marine Animals of Northeastern North America. Rutgers University Press, Rutgers, NJ. 367 pp. Rathbun, M.J. 1902. Japanese stalk-eyed crustaceans. Proceedings of the United States National Museum 26:23–55. Siegfried, C.A. 1980. Seasonal abundance and distribution of Crangon franciscorum and Palaemon macrodactylus (Decapoda, Caridea) in the San Francisco Bay-Delta. Biological Bulletin 159:177–192. Siegfried, C.A. 1982. Trophic relations of Crangon franciscorum Stimpson and Palaemon macrodactylus Rathbun: Predation on the Opossum Shrimp, Neomysis mercedis Holmes. Hydrobiologia 89:129–139. Spivak, E.D., E.E. Boschi, and S.R. Martorelli. 2006. Presence of Palaemon macrodactylus Rathbun 1902 (Crustacea: Decapoda: Caridea: Palaemonidae) in Mar del Plata harbor, Argentina: First record from southwestern Atlantic waters. Biological Invasions 8:673–676. St. Raykov, V., M. Lepage, and R. Perez-Dominguez. 2010. First record of Oriental Shrimp, Palaemon macrodactylus Rathbun, 1902 in Varna Lake, Bulgaria. Aquatic Invasions 5:S91–S95. Warkentine, B.E., and J.W. Rachlin. 2010. The first record of Palaemon macrodactylus (Oriental Shrimp) from the eastern coast of North America. Northeastern Naturalist 17:91–102. Weiss, H.M. 1995. Marine animals of southern New England and New York: Identification keys to common nearshore and shallow-water macrofauna. Connecticut Department of Environmental Protection, Hartford, CT. Bulletin 115. Section 10.16 180 Northeastern Naturalist Vol. 19, Special Issue 6 Appendix 1. Key to Palaemonid and Crangonid Shrimp in New York City and Vicinity. 1a. The rostrum is short and only reaches to the end of the eyes. The claws of the first set of pereiopods are subchelate. The body is somewhat dorsal-ventrally flattened. ............................................................... (Family Crangonidae) Crangon septemspinosa 1b. The rostrum is very long and extends well beyond the eyes. All claws are chelate. The body is more laterally compressed .......................................... (Family Palaemonidae) 2 2a. Teeth on the dorsal surface of the rostrum extend to the tip .....................................3 2b. Teeth on the dorsal surface of the rostrum do not extend to the tip. Only one dorsally located rostral tooth is present behind the margin of the eye socket. Two or three teeth are present on the ventral surface of the rostrum. Mandibles without palp (this character requires careful dissection of the mouth parts) ...................................Palaemonetes pugio 3a. Four or five teeth are present on the ventral surface of the rostrum. There is a single row of setae on the ventral surface of the rostrum. One or two dorsally located rostral teeth are present behind the margin of the eye socket. Mandibles without palp (this character requires careful dissection of the mouth parts) .................................................... 4 3b. Three to five teeth are present on the ventral surface of the rostrum. There is a double row of setae on the ventral surface of the rostrum. Three dorsally located rostral teeth are present behind the margin of the eye socket. Mandibles with palp. ...............................................................................................Palaemon macrodactylus* 4a. One dorsally located rostral tooth is present behind the margin of the eye socket. ...............................................................................................Palaemonetes intermedius 4b. Two dorsally located rostral teeth are present behind the margin of the eye socket. .................................................................................................... Palaemonetes vulgaris _______________________________________________________ *Palaemon macrodactylus females can be distinguished in the field by looking for the presence of a pale whitish stripe running along the entire dorsal surface; this character is often not apparent in males. This characteristic is more obvious in larger individuals (≥2 cm) and is lost in preservation. Another characteristic is that the second pair of pereiopods extends well beyond the first and third pair. This feature is in contrast to the Palaemonetes species found in this region, whose first three pair of pereiopods are relatively equal in length. While these two characteristics can serve as initial identifiers of P. macrodactylus in the field, it is important to link them to other species-specific characteristics (in particular the presence of mandibular palps) to confirm identification.