First record of the Neotropical cladoceran Diaphanosoma fluviatile ^{in the Great Lakes basin}

Abstract

The ctenopod Diaphanosoma fluviatile has been reported primarily from the Neotropical region and occasionally from the southern United States. D. fluviatile was collected in the Great Lakes basin (the Maumee River, Western Lake Erie, and Lake Michigan) in 2015 and 2018, far north from its previously known distribution. The occurrence of this southern species in the Maumee River and Great Lakes may be the result of an anthropogenic introduction, although a natural range expansion cannot be excluded. This report documents the northernmost record of D. fluviatile in the Nearctic region, extending the known distribution of the species to 42°N, which is a notable increase of 11 degrees latitude. Our detection of D. fluviatile is the first record of this southern species from the Laurentian Great Lakes drainage.

Introduction

The neotropical crustacean Diaphanosoma fluviatile Hansen, 1899 (Cladocera: Ctenopoda: Sididae) was first identified from zooplankton samples collected from the Maumee River in Toledo, Ohio, during an assessment of the planktonic fauna of Great Lakes Harbors in September 2015. The species was subsequently identified in samples from the Western basin of Lake Erie (Figure 1), collected as part of the U.S. EPA Great Lakes National Program Office’s (GLNPO) routine biological monitoring of Lake Erie in August 2015 and August 2018. D. fluviatile is primarily a Neotropical species reported from Argentina (Fernandes et al. 2012), Brazil, Venezuela, Haiti (Korovchinsky 1992), Nicaragua (Cisneros et al. 1991), and Mexico (Elias-Gutierrez et al. 2001). In the Nearctic region, D. fluviatile has only been previously reported from southern states, one locality in Florida, two localities in Louisiana (Korovchinsky 2002), and two localities in Texas (Lopez et al. 2008), where the species was presumed near the northern extent of its natural range. We herein provide the northernmost record of this species, with notes on its identification and diagnostic features for future use.

Figure 1.

Map of Lake Erie sampling locations and the Maumee River location for 2015 and 2018. Points where D. fluviatile were found are marked with a green circle.

Materials and methods

Samples from the Maumee River (Toledo, Ohio) were collected in September 2015 with a 153 μm mesh 0.5 m-diameter plankton net lowered from a small boat until the net line became slacked and was towed vertically through the water column. In July and September 2018 Maumee River samples were taken with a 53 μm mesh 15 cm-diameter miniature plankton net, towed horizontally through the water column. Maumee River samples were collected as part of an effort to characterize the planktonic fauna of Great Lakes harbors. Samples were preserved in 90% ethanol and analyzed at the Cornell Biological Field Station (CBFS). Samples from Western Lake Erie were collected in August 2015 and August 2018 as part of the U.S. EPA GLNPO’s Biology Monitoring Program (Barbiero et al. 2018). These samples were collected aboard the R/V Lake Guardian using a 153 μm mesh 0.5 m-diameter plankton net towed vertically from two meters above the lake bottom to the surface. Lake Erie samples were preserved with a buffered sugar 4% formalin solution and stained with Rose Bengal dye (U.S. EPA 2016b). D. fluviatile was first observed in the September 2015 Maumee River samples in May of 2018 while looking at Diaphanosoma species as part of a cladoceran taxonomy workshop conducted by Kay Van Damme. The September sample was not initially analyzed as part of the harbor monitoring project, any Diaphanosoma observed from samples taken earlier that year were misidentified and recorded as either D. birgei or Diaphanosoma sp. Fifty random Diaphanosoma were removed from the Maumee River samples and Lake Erie GLNPO stations ER 58 (southern end of the Western basin), ER 59, and ER 92 (Northern end of the Western basin, Figure 1; Supplementary material Table S1) and identified to species. Lake Erie and Lake Michigan 2018 sites were enumerated and density/biomass calculated in accordance with EPA GLNPO SOP (U.S EPA 2016a). While there were zooplankton samples from additional GLNPO stations available, many stations did not have any Diaphanosoma at all or had them in very low densities. Therefore the three stations with the highest Diaphanosoma densities were chosen for a more in depth taxonomic analysis.

Taxonomic sorting was done using an Olympus SZX7 dissecting microscope identifying crustacean zooplankton specimens to genus level. Specimens of Diaphanosoma were then mounted on semi-permanent slides using 76 × 25 mm frosted edge glass slides, 18 mm round micro cover glass, glycerol, and Permount™. Semi-permanent slide mounts were transferred to an Olympus CX41 compound microscope for identification to species level. Specimen measurements, density, and biomass calculations were made according to a standard operating procedure (U.S. EPA 2016a). Taxonomic analysts used Balcer et al. (1984) to identify specimens to genus level and subsequently used Korovchinsky (1992, 2018a) for the species level identification of Ctenopoda.

Results

Morphological notes

Diaphanosoma fluviatile was originally described in 1899 (Hansen 1899). At a gross morphological level (Figure 2), D. fluviatile resembles other Diaphanosoma species known to the Laurentian Great Lakes such as Diaphanosoma birgei Kořinek, 1981 and members of the Diaphanosoma brachyurum Lievin, 1848 group. However, a number of diagnostic morphological characteristics define D. fluviatile as a distinct taxon. Morphological notes on the D. fluviatile adult parthenogenetic female specimens collected from the Laurentian Great Lakes drainage are as follows. Head shape noticeably rectangular with a fairly well developed dorsal margin (Figure 3). Compound eye relatively large, its diameter reaching to almost half the width of the head. Antennule relatively short. Swimming antennae nearly reaching posterior margin of valves. Ventral valve margins form a small narrow inflexion. Distal margin of antennal basiopodite with a small medially placed spine. Antennal segment 1 of twosegmented antenna with a small sharp spine placed at the distal corner (Figure 4A). Antennal setation of two-segmented antenna 4–8 and antennal setation of three-segmented antenna 0–1–4. Ventral margin of valves ornamented with long thin setules. Postero-ventral and posterior valve margins ornamented with very fine long denticles alternated by long thin setules (Figure 5A). More than 35 fine denticles and long setules along the postero-ventral and posterior valve margin. A single inner dorsal spine is situated at the posterior-most terminus of the valve, approaching the posterior margin. Postabdomen somewhat narrow with fine lateral denticles, postabdominal claw short and curved with uniform pecten and 3 basal spines (Figure 4B). Postero-dorsal margin of carapace with prominent indentation.

Figure 2.

Habitus of adult parthenogenetic female of D. fluviatile from the Maumee River. Photomicrograph by Elizabeth A. Whitmore.

Figure 3.

Head shape of D. fluviatile (A) and D. birgei (B). Photomicrograph by Elizabeth A. Whitmore.

Figure 4.

Spine on distal corner of segment 1 of 2 segmented antenna (A) and postabdominal claw (B) of D. fluviatile. Photomicrographs by Elizabeth A. Whitmore.

Figure 5.

Postero-ventral margin of D. fluviatile showing both fine denticles close to each other and long setules (A), Posterior valve margin of D. birgei showing spaced large denticles, alternated by shorter denticles (B). Photomicrographsby Elizabeth A. Whitmore.

Once we were confident in our ability to identify this new taxon, we revisited the three August 2015 GLNPO station samples from Western Lake Erie that contained relatively high densities of Diaphanosoma and identified 50 random individuals using the Korovchinsky (1992, 2018a) key. The depth of the Lake Erie stations in 2015 ranged from 5.5 m to 7.7 m, and the surface water temperature for these stations ranged from 23.9 °C to 26 °C. In 2018 the depths of the Lake Erie stations ranged from 6.7 m to 9 m and the surface temperature ranged from 24.3 °C to 26 °C. In Lake Michigan in 2018 the site that had D. fluviatile was a depth of 129 m (sample depth was only 100 m) and had surface temperatures of 23.8 °C (Table S1) We found that the southwestern stations (ER 58 and ER 59) closer to the Maumee River had the highest densities of D. fluviatile in August of both 2015 and 2018 (Figure 6, Table S1). At station ER 58 in 2015 14% of the Diaphanosoma population was D. fluviatile while the remaining 86% were D. birgei. In 2015 station ER 59 in 2015 was the only station where Diaphanosoma brachyurum (6% of the population) was detected. The D. fluviatile population that year at ER 59 was the same as D. brachyurum (6%) and the rest of the subsampled population was D. birgei. At the northern station further from the Maumee only 2% of the Diaphanosoma subsampled population were D. fluviatile in 2015 (the remaining were again D. birgei, Figure 6). In 2018 Western Lake Erie had a range of D. fluviatile densities from 1871.19 individuals/m3 (station ER 59, which was the closest station to the Maumee River) to 30.77 individuals /m3 (station ER 61, Table S1). D. fluviatile was also detected at a single location (station MI 11) from Lake Michigan in August 2018, where the species’ density was very low (2.19 individuals/m3, Table S1). A random subsample of 50 Diaphanosoma taken from the Maumee River samples collected in 2015 were all identified as D. fluviatile. The Maumee River was revisited in July and September of 2018 and results show that D. fluviatile was still the sole Diaphanosoma species present in that location.

Figure 6.

Population composition of Maumee River and western Lake Erie Diaphanosoma. Each column represents a total of 50 animals.

Discussion

The most common Diaphanosoma species found in Western Lake Erie in August 2015 and 2018 was D. birgei. D. fluviatile can be differentiated from D. birgei by very fine denticles interspersed by long thin setules (Figure 5A) contrasted by the presence of large denticles interspersed with small groups of setules along the posterior ventral margin of the carapace in D. birgei (Figure 5B). The head of D. birgei is characterized by a noticeable rounded dorsal protrusion, and is generally less quadrate in shape in comparison to D. fluviatile (Figure 3). The life history of Diaphanosoma in the Great Lakes is not well documented; it is known that they are found from May to October, their population reaching a peak in the early fall, they prefer the nearshore or more sheltered offshore (not deep offshore), and reproduce parthenogenetically in the summer and sexually in the fall (Balcer et al. 1984). D. fluviatile is a species reported from both lentic and lotic environments, therefore this record from the Maumee River, Lake Erie, and Lake Michigan is consistent with the ecology reported for the species (Panarelli et al. 2013; Campanelli Mortari and Henry 2016). However, the biology of this southern ctenopod species remains largely unstudied (Korovchinsky 1992).

The occurrence of D. fluviatile in the Maumee River, Lake Erie and Lake Michigan extends the known distribution of this southern species by eleven degrees latitude, from 31°N to 42°N. The ecosystem risk to the Laurentian Great Lakes posed by this species is considered uncertain (U.S. Fish & Wildlife Service 2018). The occurrence of D. fluviatile in Lake Erie is well north of the species’ presumed natural range and the mode of introduction is not known (U.S. Fish & Wildlife Service 2018). The low abundance of D. fluviatile in Lake Michigan may be indicative of a recent introduction. Several previous introductions of non-indigenous crustaceans to the Great Lakes have been attributed to ballast water from transoceanic vessels (Grigorovich 2003). Diaphanosoma spp. resting eggs have been collected from ballast water of Great Lakes ships and those resting eggs were successfully hatched (Bailey et al. 2004; Gray et al. 2005). Although we initially detected D. fluviatile from the Maumee River in Toledo, Ohio, an area with considerable anthropogenic influence and transoceanic vessel traffic, a range expansion by natural means such as transportation overland via animals (Gray and Arnott 2011) cannot be excluded. It is also possible that the species have been overlooked in collections from intermediate latitudes. In any case, this detection of a southern cladoceran species in Western Lake Erie and Lake Michigan is consistent with range expansions northwards of various taxa (Post 2013). Lake Erie is the shallowest, warmest, and most productive of the Laurentian Great Lakes (Connolly et al. 2017) and we therefore expect the lake to be particularly suited for colonization by exotic species, in particular southern species from warmer climates. Alternatively, and not unusual in Diaphanosoma, this species identified in the northern U.S. could belong to a cryptic species complex, in which case morphological features alone would be insufficient to assess its identity. Diaphanosoma contains notoriously difficult taxa to identify, we suggest that more thorough investigations into North American Diaphanosoma to determine the status of cryptic species complexes which may be necessary to properly assess species distributions.

Several non-indigenous cladoceran species have previously been reported from the Laurentian Great Lakes, including representatives from the orders Onychopoda: Bythotrephes cederströmii Schodler, 1877 (there is some debate as to whether this is B. cederströmii or a hybrid between B. cederströmii and B. brevimanus (Korovchinsky 2015, 2018b)), Cercopagis pengoi Ostroumov, 1891 (MacIsaac 1999), and Anomopoda: Daphnia lumholtzi Sars, 1885 (Muzinic 2000), Bosmina (Eubosmina) maritima Muller, 1868 (De Melo and Hebert 1994) To our knowledge, D. fluviatile is the first non-indigenous representative from the order Ctenopoda to be detected in the Laurentian Great Lakes.

Supplementary Material

Table S1

Table S1. Site locations, conditions, and Diaphanosoma community densities and biomass estimates for August 2015 and August 2018.