Biol Invasions (2009) 11:1827–1834 DOI 10.1007/s10530-008-9361-8

ORIGINAL PAPER

First record of sowerbyi Lankester, 1880 (: : ) in Mexico (Adolfo Lopez Mateos reservoir), with notes on their feeding habits and limnological dates

Marco A. Moreno-Leon Æ Alfredo Ortega-Rubio

Received: 12 July 2008 / Accepted: 24 September 2008 / Published online: 9 October 2008 Ó Springer Science+Business Media B.V. 2008

Abstract This paper represents the first record of found in Hong Kong were two water lily plants the freshwater jellyfish Craspedacusta sowerbyi received direct from East Africa which had been in (Lankester 1880)inMe´xico; the medusa was col- the tub for at least 15 months and also some water- lected in Adolfo Lopez Mateos (ALM) reservoir, one hyacinth plants from a local source (Herklots 1940). of the main reservoirs in Sinaloa State NW in Dr. Allman and Professor Ray Lankester, after- Mexico. This report of the population of C. sowerbyi wards Sir Ray Lankester, described the medusa, not represents an exceptional case of freshwater jellyfish only as a new , but as representing a new , on this latitude in American Continent. This study Professor Lankester naming the genus Craspedacusta provides additional information on physico chemical (June 17, 1880), and Dr. Allman suggesting the characteristics of the reservoir and qualitative and generic name Limnocodium (June 24, 1880), which quantitative analysis of the trophic spectrum of Professor Lankester in his subsequent writings on the C. sowerbyi. subject adopted (Sowerby 1941). In recent times, C. sowerbyi has been found Keywords Jellyfish Á Medusa Á Feeding habits Á sporadically and often in large numbers in ponds, Sinaloa Mexico lakes, reservoirs and rivers in the north temperate regions of the world (Rayner 1988). The species is decidedly present in temperate climates almost globally and commonly occurs on five continents; South and North America, Europe, Introduction Asia, and Australia (Acker and Muscat 1976; Pennak 1989). Was first observed in United States in 1916 ‘‘Craspedacusta sowerbyi was discovered by Mr. near Frankfort, Kentucky, in Benson Creek (Garman Sowerby in a waterlily tank in Regent’s Park, 1916). The first collections in the Great Lakes were in London, in 1880, and is believed to have been 1933 in the Huron River near Ann Arbor, Michigan brought in with waterlilies from South America or the (Woodhead 1933, 1943), (Bennitt 1932) had earlier West Indies’’. In the tub in which the medusae were summarized the published accounts from North America, and Schmitt (1939) and Zeliff (1940) have M. A. Moreno-Leon (&) Á A. Ortega-Rubio added to the compilation of North American records. Centro de Investigaciones Biolo´gicas del Noroeste SC, C. sowerbyi, has been registered in several Euro- Mar Bermejo No. 195, Col. Playa Palo de Santa Rita, Apdo. Postal 128, La Paz, BCS 23090, Me´xico pean countries: Italy, France, Sweden, Spain and e-mail: [email protected] recently Portugal (Ferreira 1985), 31 states of the, 123 1828 M. A. Moreno-Leon, A. Ortega-Rubio

USA specially eastern states (De Vries 1992), reporting new registries of C. sowerbyi so is case of Canada, and Australia of the south (Thomas Perez et al. (2006), they report the first record in the 1950), the Islands of the Philippines, China, Japan, Proserpina reservoir in Extremadura Spain; and Fritz Asia Centrals and South America (Acker 1976), as et al. (2007) they describe the presence of C. sowerbyi well as New Zealand. in Germany, with analysis over nomenclature. In this Other Great Lakes collections have been from context, it is important to indicate that although in Lake Erie (Hubschman and Kishler 1972) and inland the last ones decades has studied and discovery Michigan lakes where it reaches its northernmost C. sowerbyi in all continents; and its presence in distribution (Smrchek 1970). Mexico had not been confirmed, being in this case of The organism is often found in artificial bodies of the equatorial location but the continent. water like ponds and quarries throughout the USA but Craspedacusta sowerbyi has a world-wide distri- is not limited to these habitats (Garman 1916; Brooks bution for Dumont (1994) the author analyzed the 1932; Schmitt 1939; Dexter et al. 1949; Lytle 1960). world distribution of the freshwater and brackish- The sporadic nature of this jelly-fish’s distribution water medusae; Dumont describes the distribution of and its preference for artificial habitats indicate that it C. sowerbyi in North American and the south portion could possibly be an aquarium release or a release of the continent; indicating the absence of this with aquatic plants (Bushnell and Porter 1967). cnidarians in Mexico (See Fig. 2). Although all of these freshwater jellyfish occupy Our paper is the first report confirmed of C. sow- similar habitats, only C. sowerbii, its minute polyps erbyi in Mexico with notes on their trophic spectrum and its medusa (2.5 cm) (Fig. 1), shows a worldwide and limnological dates. distribution (Acker and Muscat 1976; Payne 1924; Pennak 1956; Rayner 1988). Possible reasons might be the ability for several forms of vegetative repro- Materials and methods duction, such as budding a , which stays attached to form a colony and budding a motile The ALM Reservoir is located in Sinaloa state (NW frustules which attaches and builds a new polyp Mexico, Figs. 3, 4), and covers an area of 11,354 (Dejdar 1934; Reisinger 1957). hectares at an altitude of 186 amsl. Its maximum Recently Jankowski (2001), made a detailed length is 18.4 km, maximum width 9.88 km, and analysis of the distribution and presence of C. sow- maximum water depth about 45 m and Capacity: erbyi (The Freshwater medusae of the world); in this 3,071.96 Millions of m3. However the reservoir is not study the absence of cnidarians in Mexico and all the thermally stratified. equatorial portion of continent is reported. The first collection of Jellyfish in ALM reservoir Arbae`iauskas and Lesutiene¨ (2005) report the in Sinaloa state, NW. in Mexico was in autumn in invasion of C. sowerbyi into Lithuanian waters during 2006 exactly in October 27. Some of the jellyfish 2002. Papers recent continuant anywhere in the world were preserved in 95% alcohol and measured using a stereoscopic microscope, while others were main- tained alive in aquarium during a month, realizing a measurement and observes of some aspects of the reproductive biology. All collections were made with circular drags using a 45 l mesh for collect of plankton. Crasped- acusta was present in the water column of 40 cm to 1 m depth. Collections of C. sowerbyi were performed during daylight hours on the autumn with warm climate (mean October air temperature at the study site is 28.1°C). Densities of C. sowerbyi in the surface waters Fig. 1 Jellyfish collected in ALM reservoir were estimated at 50 m intervals along three 123 First record of Craspedacusta sowerbyi Lankester 1829

Fig. 2 American continent distribution of freshwater medusae (Taken of Dumont Op. cit.)

bisecting transect in three stations. Counts were made The umbrellar diameter, were determined from within a 50 period of the numbers of medusae visible medusae randomly selected from the net samples in 1 m2 of surface water (n = 300) on both sides of (n = 95). Sex of C. sowerbyi was determined by each transect. See Fig. 5. examining the gonadal tissue under a microscope. Zooplankton samples were also collected with Measurements were made using a stereo micro- mesh of 45 l, with circular routes at constant scope fitted with a calibrated ocular micrometer speed; the samples were preserved with 95% 1 day after the captures. ethanol. Temperature, pH, dissolved oxygen, con- The umbrellar diameter were determined from ductivity, and Secchi depth were measured in situ, medusae randomly selected from the net samples in laboratory were evaluated Nitrate (NO3–N), (n = 95) (Fig. 6). Nitrite (NO2–) Phosphates (PO4), and Suspended For the determination of the trophic spectrum, the Solid Total (SST). gastrovascular cavity was analyzed in sub sample of

123 1830 M. A. Moreno-Leon, A. Ortega-Rubio

The population of C. sowerbyi studied presents a single sex (females); thus sexual reproduction is infrequent (Pennak 1989). Through asexual repro- duction, a polyp may bud hydromedusae, frustules (non-ciliated larvae), and/or polyps. The qualitative analysis of the zooplanctonic community allowed establishing the trophic spectrum of the cnidarians; however the components of the zooplankton community of the reservoir one appears in Table 1. Of 50 medusas analyzed for determination of trophic spectrum, only 35 units presented/displayed Fig. 3 ALM reservoir stomach content (70%); the analysis showed that the organisms varied from 1 to 4 preys. Most of preys found in gut contents were common components of zooplankton community in reservoir, with the most frequently (Table 1) occurring preys items being Diaphanosoma montezumae, Diaptomus spp, longispina, and Keratella coclhearis. Table 2 shows the values average of the limnological characterization of ALM reservoir.

Discussion

Since the original discovery the C. sowerbyi in Kew Gardens in 1880 (Hutchinson 1967), they have been Fig. 4 Location of the study site in Sinaloa state, Mexico found to be widespread in the North American 50 organisms. Items were identified under a com- continent (Payne 1924; Schmitt 1939) and were pound microscope, and the diet was expressed as the reported in 1940 from Hawaii (Matthews 1963). percent frequency of occurrence (%FO) of each prey, Our study represents the first record confirmed of and the percent of total stomach content number C. sowerbyi and the attempt to characterize your (%N) of each prey according to Hyslop (1980). trophic spectrum and limnological conditions of the reservoir in Mexico. In reference to size, the ranges of medusae found Results in ALM reservoir were within the ranges recorded elsewhere. Pennak (1956) noted that the medusae are A total of 95 individual medusae were counted in three often not noticed until they are over 10 mm in transects across the reservoir (density = 0.95 ind./ diameter, although smaller size ranges have been 2 m ). Patches of C. sowerbyi were recorded in open recorded (Byers 1945; Beckett and Turanchik 1980; water in the station 2 (The number of medusae did not Rayner 1988). differ between transects (chi-square test, Transect 1 In a temporal study in Louisiana, Ziser and Burke versus Transect 2 Frequencies (Spreadsheet1) Chi- (1984) found that the size range of medusae during Square = 22.50000, df = 49, P \ .999581. Note: each month of summer (April–October) was highly Unequal sums of obs. & exp. variable (1–17 mm), although they observed a gen- While Pennak (1953) lists a bell diameter of eral trend toward an increasing mean medusa 22 mm as a maximum size, the largest collected diameter over their study period. In New Zealand, in ALM reservoir jellyfish have a diameter of the umbrellar diameter of C. sowerbyi ranged 10–19 mm. between 3.2 and 16.8 mm (Boothroyd et al. 2002). 123 First record of Craspedacusta sowerbyi Lankester 1831

Fig. 5 Location of sampling stations in ALM reservoir

3

2 Station N W

1 25°6’15.73” 107°23’21.97”

2 25°8’32.97” 107°21’40.62” 1 3 25°10’1.77” 107°24’13.50”

The abundance of C. sowerbyi medusae in ALM reservoir was lower (0.95 Org/m2) than the range reported by Angradi (1998), Boothroyd et al. (2002), and Perez et al. (2006) but higher than reported by Spadinger and Maier (1999) or Davis (1955). How- ever, the number of medusae per m2 was probably underestimated in our study due to the water’s turbidity. The presence of medusae C. sowerbyi in ALM reservoir in summer and autumn is consistent with the widely-reported observation occurring at times of high water temperatures, although water level and food abundance; Perez, Op. cit. and Lytle (1962) have also been suggested as regulating mechanisms. Fig. 6 Microscopical details of adult jellyfish

123 1832 M. A. Moreno-Leon, A. Ortega-Rubio

Table 1 Diet of C. sowerbyi expressed as frequency of causes significantly lower abundances of bosminids occurrence (%FO) and percent of prey (%N) and cyclopoid (Jankowski and Ratte 2000; Prey category (%FO) (%N) Jankowski 2004). Similarly to other published data (Boothroyd et al. Cladocera 2002), nauplii were not recorded in the gut content of Daphnia longispina 34.29 11.36 C. sowerbyi in the Proserpina reservoir. Whether this D. Magna 25.71 8.33 was because they were not preyed upon, or because Diaphanosoma montezumae 31.43 12.88 they were more rapidly digested and thus were Bosmina longirostris 25.71 7.58 missed in the analysis, is uncertain. Dodson and Cerodaphnia spp. 20.00 6.82 Cooper (1983) found in laboratory experiments that Copepoda nauplii were consumed at high rates by C. sowerbyi. Megacyclops viridis 11.43 3.79 In our study, C. sowerbyi fed on five rotifer taxa, Eucyclops spp. 8.57 2.27 whereas in New Zealand (Boothroyd Op. cit.) only Diaptomus montezumae 25.71 8.33 Asplanchna was recorded in jellyfish stomach con- Cyclops spp. 11.43 4.55 tent. Dodson and Cooper (1983) also demonstrated Macrocyclops spp. 11.43 3.03 that C. sowerbyi selected large and predaceous rot- Rotifera ifers such as Asplanchna, and avoided small rotifers. Anuraeopsis fissa 25.71 8.33 The impact of this widespread jellyfish is unclear. Polyarthra spp 5.71 1.52 Dodson and cooper (Op. cit.) proposed C. sowerbyi Keratella coclhearis 28.57 9.85 preference for predatory zooplankton, such as the Brachionus spp. 25.71 6.82 rotifer Asplanchna, could influence relative zoo- Testudinella spp. 8.57 4.55 plankton species structure. Spadinger and Maier (Op. cit.) agreed with theorized affects on zoo plankton communities finding that C. sowerbyi Table 2 Values for some limnological variables of ALM hydromedusae prefer larger zooplankton (0.4–1.4 mm) reservoir and vigorous prey such as copepods. Variable Value In reference to the limnological conditions of the water body, our studies agree with the reported for Total phosphorus 3.31 mg/l William and Kennedy (2007) who determined the Conductivity 150 lS/m limnologists’ characteristics of the Lagoa Misteriosa Ph 7.3 water body in Brazil classifying it like meso-eutro- Surface water temperature 27.5°C phic (See Table 2). Transparency (Secchi disc) 1.5 m Dissolved oxygen 6.5 mg/l Acknowledgements We thanks to Jose Eden Cuadras and Rogelio Moreno Urias by your valuable support in the camp NO –N 2.34 mg/l 3 activities. Authors want to thank the economic support of the NO2–N 0.23 mg/l CONACYT-SAGARPA 2005, 12078 Project and CONACYT- SST 0.023 mg/l SEMARNAT 2006-C01-23449 Project. Chlorophyll ‘‘a’’ 3.1–4.6 lg

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