A new report of Craspedacusta sowerbii ( Lankester , 1880 ) in southern Chile

Craspedacusta sowerbii (Lankester, 1880) is a cnidarian thought to originate from the Yangtze River valley in China. However, C. sowerbii is now an invasive species in freshwater systems worldwide. In Chile, C. sowerbii was first recorded in 1942 by Porter and Schmitt in the Marga-Marga Reservoir, in Valparaíso. Since then, there have been few further Chilean records of this species. Here, we report the presence of C. sowerbii medusae in Santa Elena Lake, Bulnes, Región del BíoBío, along with limnological parameters.

The cnidarian C. sowerbii is found in diverse subtropical and warm-temperate aquatic systems of the world, with medusa most commonly found in warm, stagnant waterbodies such as lakes, dams and ponds (Dumont 1994;Jankowski 2001).The lifecycle is well known, and includes both polyp and medusa phases (DeVries 1992; Lewis et al. 2012;McClary 1959).The medusa prey on zooplankton communities ranging in size from 0.2-2.0mm (Dodson and Cooper 1983), especially copepods (Jankowski et al. 2005;Smith and Alexander 2008;Jankowski and Ratte 2000).
Medusa are usually incidentally detected, and the scarce monitoring for this species is surprising in light of the potential ecological effects on trophic chains in freshwater systems (Jankowski and Ratte 2000).The present work expands knowledge of Craspedacusta sowerbii occurrence in Chile to Santa Elena Lake, Región del Bío-Bío, and in addition, provides environmental data associated with its occurrence.

Description of study area
Santa Elena Lake is shallow (Z max: 14 m), with an area of 59 ha and a perimeter of 5,132.92m, located in Bulnes, Región del Bío-Bío, south-central Chile (36º47′41.01″S;72º22′56.97″W).The lake is situated 100 km northeast of Laguna Grande de San Pedro where the medusae were reported in 1969 (Quezada 1969) and 228 km north of Lago Lanalhue where the medusae were reported in 1973 (Quezada 1973) (Figure 1).The lake is listed as a conservation and biodiversity priority by the Biodiversity Regional Strategy of Bulnes Municipality (CONAMA 2002).The climate is temperate Mediterranean, with annual average temperatures ranging from 13.5 °C to 14.0 °C, and is warmer in January (28.8 °C monthly average) and colder in July (3.7-5.0 °C).Annual average precipitation is 1,025 mm, with July being the wettest month, and a dry season occurring from December through March (CETSUR 2008).The lake watershed is influenced by human activities such as agriculture, forestry (González-Acuña et al. 2004), and tourism.

Distribution in Chile
Distribution in Latin America  2).Environmental data: Potential environmental correlates were assessed at the time the medusae were collected at mid-day.Surface UVA-UVB radiation was measured with UVA-UVB meter ST-513.Due to the depletion of the ozone layer in the southern hemisphere, UV radiation was measured as an environmental parameter because it can be harmful to aquatic organisms.These data are provided as a reference for future studies.Water surface temperature was measured with an IR LASER Thermometer, model CHY-110.Subsequently, water samples were taken using a Wildco ® water collector to generate temperature, pH, dissolved oxygen (ThermoScientific ® Orion3STAR DO portable) and chemical (nitrogen, phosphorous) profiles for the lake.Nitrogen and phosphorous concentrations at 1.0, 5.0 and 10.0 m depths were measured using standard methods for water analyses (APHA 2005).
Phytoplankton and zooplankton sampling for qualitative composition were undertaken using silk plankton nets (mesh size 25 µm).Phytoplankton and zooplankton were identified morphologically using published descriptions (phytoplankton: Graham et al. 2009;zooplankton: Balcer et al. 1984).

Results
Although the density of C. sowerbii was not measured, there appeared to be a bloom of medusae on the lake surface.At the time of sampling, the water temperature was around 20.1°C throughout the water column (Table 2; Figure 3), showing that the lake was mixed and, according to Minchin et al. (2016), within the temperature range associated with the occurrence of Craspedacusta sowerbii medusae.Secchi disk measurements were 3.31 m (Figure 3), likely indicating the lake was in a clear-water phase, similar to the conditions specified by Lampert et al. (1986) when zooplankton grazing is high in a eutrophic lake.The water pH profile was 7.5, and the nitrogen and phosphorus concentrations were below 1.0 mgL -1 and 3.3 mgL -1 , respectively.Oxygen levels were above 7 mgL -1 up to 2 m deep in the water column and dropped to < 5 mgL -1 towards the bottom of the lake (Table 2, Figure 3).UVA-B radiation was 21 mW*cm -2 at the water surface.Phytoplankton was scarce (primarily diatoms and green flagellates) and zooplankton was mainly comprised of Daphnia pulex Leydig (1860), Daphnia sp.(O.F. Müller, 1785), Macrocyclops albidus Jurine (1820), Eucyclops sp.Claus, 1893 and undetermined species of copepod nauplii (Table 3).

Discussion
Although, C. sowerbii has previously been recorded in the central and southern regions of Chile (Figueroa and De los Ríos 2010;Caputo-Galarce et al. 2013;Quezada 1969;Quezada 1973;Porter and Schmitt 1942; Schmid-Araya and Zúñiga 1992) (Figure 1),   Although records of low dissolved oxygen affecting C. sowerbii blooms are limited, some studies have shown a direct relationship between dissolved oxygen and other medusae populations (Purcell et al. 2001;Purcell et al. 2007).Dissolved oxygen levels in Santa Elena Lake ranged from 7.4 mgL -1 to 7.7 mgL -1 in the first two meters of the water column, then reduced to <5 mgL -1 from 3 m down to the bottom of the lake (Table 2, Figure 3).Low oxygen levels indicate eutrophication (Smith 1998), and can be attributed primarily to decomposition by bacteria and respiration of plants and animals (Cole 1983).The cnidarian is more common in eutrophic lakes (Arai  2001; Jankowski 2001; Raposeiro et al. 2011).As such, the eutrophic Santa Elena is a suitable location for the cnidarian to thrive.
The northernmost (Schmid-Araya and Zúñiga 1992) and southernmost (Caputo-Galarce et al. 2013) reported site of C. sowerbii medusa in Chile are located 554 km north and 502 km south of Santa Elena Lake respectively.Hence, Santa Elena Lake is located in the mid-point, almost equidistant, from previous reports of the medusae.Furthermore, Santa Elena Lake is separated by only 100 km to the northeast from Laguna Grande de San Pedro, where medusae were reported by Quezada (1969).The polyp stage of C. sowerbii was not observed in this study.However, it may be relevant to take into account for future biomonitoring.For example, Duggan and Eastwood (2012) determined that the C. sowerbii polyp stage is more widespread than where medusae are observed, and can include lakes and areas widely separated from where the medusae have been recorded.The appearance and distribution of medusae may be associated with migrating birds (Dumont 1994) and/or human intervention (Marsden and Hauser 2009), but further work is required to establish causal links in this case.Santa Elena Lake hosts a high diversity of migratory birds that might potentially play a long-distance dispersal role as a vector of propagules within the southern cone and across different eco-regions.It is also advisable to identify potential niches and point sources of propagules, especially in the abundant small lakes and shallow ponds of Región del Bío-Bío and other southern regions of Chile.Such ecosystems host a wide diversity of migratory birds (Garay et al. 1991) like Santa Elena Lake.Early detection of both the polyp and medusa stages using molecular tools would be helpful, but little molecular analyses of non-native or native populations have been undertaken to date (Karaouzas et al. 2015).We suggest greater monitoring of this and other lakes in the area, since lakes surrounding Santa Elena Lake might be already colonized by C. sowerbii or will be in the future.

Conclusions
The limnological conditions of Santa Elena Lake seem ideal for growth of C. sowerbii.The presence of C. sowerbii and synergistic environmental elements such as hypoxia, high temperatures and appropriate prey elements such as zooplankton abundance require further investigation.Thus, biomonitoring, including the use of molecular tools, for several years over different seasons, is necessary in order to determine whether the presence of C. sowerbii is continuous or irregular throughout the year.It is important to determine the origin of this medusa colonization and the parameters that caused the medusa to thrive.

Figure 1 .
Figure 1.Map of Chile showing sites and years of sighting for Craspedacusta sowerbii, including this study (Id 7).

Figure 3 .
Figure 3. Dissolved oxygen, temperature profiles and Secchi disk measurement of Santa Elena Lake on 8 April 2014.

Table 1 .
List of migratory birds at Lake Santa Elena

Table 2 .
Limnological profile of a water column at the deepest point in the lake (36º48′048″S; 72º22′95.7″W) in Santa Elena Lake.Data were taken on April 8 th 2014.

Table 3 .
Composition of net plankton from Santa Elena Lake in mid-fall (April 8 th ).