Winter Swarming Behavior by the Exotic Cladoceran Daphnia Lumholtzi Sars, 1885 in a Kentucky (USA) Reservoir

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Winter swarming behavior by the exotic cladoceran Daphnia lumholtzi Sars, 1885 in a Kentucky (USA) reservoir

John R. Beaver1,*, Thomas R. Renicker1, Claudia E. Tausz1, Jade L. Young2, Jennifer C. Thomason2, Zachary L. Wolf2, Amber L. Russell3, Mac A. Cherry4, Kyle C. Scotese1 and Dawn T. Koenig1 1BSA Environmental Services, Inc., 23400 Mercantile Road, Suite 8, Beachwood, OH 44122, USA 2U.S. Army Corps of Engineers, Louisville District Office, Division of Water Quality, P.O. Box 59, Louisville, KY 40201-0059, USA 3U.S. Army Corps of Engineers, Engineer Research and Development Center, 3909 Halls Ferry Road,Vicksburg, MS 39180-6199 USA 4U.S. Geological Survey, Ohio-Indiana-Kentucky Water Science Center, 9818 Bluegrass Parkway, Louisville, KY 40299-1906, USA Author e-mails: [email protected] (JRB), [email protected] (TRR), [email protected] (CET), [email protected] (JLY), [email protected] (JCT), [email protected] (ZLW), [email protected] (ALR), [email protected] (MAC), [email protected] (KCS), [email protected] (DTK) *Corresponding author

Received: 25 July 2017 / Accepted: 14 December 2017 / Published online: 27 January 2018 Handling editor: Ian Duggan

Abstract

We describe swarming behavior in the invasive cladoceran Daphnia lumholtzi Sars, 1885 in a Kentucky, USA, reservoir during winter 2017. The taxon is a highly successful tropical invader and has spread throughout the lower latitude systems in the USA since its discovery in 1991. Other than a few isolated reports, the abundance of D. lumholtzi is often <1 organism L-1. Previous studies indicate that D. lumholtzi is a largely thermophilic species often peaking in abundance in late summer after native daphnids are gone from the water column of lakes and reservoirs. Prior to our study, there have been no published reports of swarming behavior by this species. We document the occurrence of massive swarms (>10,000 organisms L-1) of sexually reproducing females of this exotic cladoceran at water column temperatures <10 °C. Key words:zooplankton, swarm event, invasive species, ephippia

Introduction summer (Work and Gophen 1999a; Havens et al. 2000; Lennon et al. 2001; Havel and Graham 2006) The large cladoceran, Daphnia lumholtzi (Sars, 1885), when native daphnids are rare or absent from the native to Africa, Asia and Australia, was discovered water column (Havens et al. 2011). Despite its wide in the USA in the early 1990s and documented from distribution, there is little evidence that this taxon several locations in the southeastern USA (Havel has displaced endemic cladocerans (Work and Gophen and Hebert 1993), eventually spreading across much 1999a; Havens et al. 2011; Sousa et al. 2016). of the southern portion of the US and into the Typically D. lumholtzi only achieves abundances of Laurentian Great Lakes (Tudorancea et al. 2009). ca. 1 individual L-1 and is rarely found at concen- Daphnia lumholtzi is a highly successful invader trations higher than endemic daphnids (Havens et al. given its wide distribution in the continental US 2011). Daphnia lumholtzi exhibits long carapace (Havel and Shurin 2004; Havel et al. 2002, 2005; spines that are believed to deter predation by Walker et al. 2013). Rapid expansion in habitats juvenile fish (Swaffar and O’Brien 1996). Both head outside of its native range in South America have spines and tail spines have been observed to increase also recently been documented (Kotov and Taylor in response to predator kairomones (Sorensen and 2014; Sousa et al. 2016). Highest density and biomass Sterner 1992; Dzialowski et al. 2003) and increasing of D. lumholtzi are usually observed in mid to late temperatures (Yurista 2000).

43 J.R. Beaver et al.

Figure 1.Map of Nolin Reservoir showing locations of dam (bold black line), littoral swarm sample sites (swarm 1 and swarm 2) and non-swarm site (03310900, closest to dam). Inset shows location of Nolin Reservoir within the state of Kentucky and within the continental USA. Scale bar refers to reservoir map.

Large, monospecific aggregations of zooplankton behavior in D. lumholtzi b) the swarms displayed the (i.e., swarms) have been reported for a number of fresh- highest densities of D. lumholtzi reported thus far in water and marine species (Young 1978; Ambler 2002 the scientific literature and c) the swarms occurred and references therein). Concentrations of organisms during winter, at temperatures far below the expected are typically several orders of magnitude higher in range for D. lumholtzi. these swarms compared to other locations and are confined to the top strata of the water column. Swarms Methods are often located in the littoral region of the water bodies and may be several meters across. Typically, Site description zooplankton swarms involve masses of organisms Nolin Reservoir (commonly known as Nolin River swimming in the same direction, at the same speed. Lake) is a highly dendritic reservoir located in Such swarms are believed to be a defense against Edmonson, Grayson and Hart counties, Kentucky, predation, by acting to confuse predators and to USA (Figure 1). Surface area of the reservoir is decrease the probability of being captured (Jensen et approximately 23.4 km2 and maximum reservoir depth al. 1998; Ambler 2002). Swarms have been recorded is approximately 28.3 m and 20.7 m during summer for a number of species of cladocerans (Ratzlaff 1974; and winter pool, respectively. The drainage area of Jakobsen and Johnsen 1988; Young and Taylor 1990), Nolin Reservoir is approximately 1,820 km2 and is particularly daphnids (Young 1978; Mitchell et al. fed primarily by inflow from the Nolin River in the 1995). However, to date there are no published reports northeast corner of the reservoir. The reservoir dam in the scientific literature of swarming behavior by regulates outflow in the southwest corner of the D. lumholtzi in either its native or its invaded range. reservoir and is operated by the U.S. Army Corps of This study reports an incidence of extraordinarily Engineers for the primary purpose of flood control. large D. lumholtzi swarms during winter in a Water residence time for Nolin Reservoir varies Kentucky, USA reservoir. This event was unique from seasonally. The Kentucky Division of Water has historic reports of D. lumholtzi in that a) it is the first classified Nolin Reservoir as a stable eutrophic scientific report, to our knowledge, of swarming system in the latest lake assessment.

44 Winter swarm of Daphnia lumholtzi in a Kentucky reservoir

Figure 2.Macroscopic view of D. lumholtzi swarm 2 in Nolin Reservoir (A) on January 3, 2017, upstream of the dam tower, photo by D. Rodgers (B) on January 5, 2017, downstream of the dam tower, photo by D. Rodgers and (C) on January 4, 2017 in a collected whole water swarm sample, photo by J. Thomason.

Sample collection Lugol’s solution, gently homogenized, and subsampled into Utermöhl chambers. Counts and taxonomic iden- On January 3, 2017 swarms in calm, littoral areas of Nolin Reservoir were observed from the shore tifications were then performed using an inverted light (Figure 2), along with audible water turbulence. Whole microscope (Leica DMIL) at 800X. Phytoplankton from USGS station 03310900 (non-swarm samples) water samples were collected mid-day on January 4, 2017 at two swarm sites (swarm 1: 37.280 °N, - were analyzed using the membrane filtration technique (McNabb 1960) at 630X magnification (Leica DMLB) 86.229 °W, swarm 2: 37.279 °N, -86.247 °W) for the analysis of both zooplankton and phytoplankton. with a count threshold of 400 natural units (colonies, Concurrently, triplicate whole water samples were filaments and unicells). Phytoplankton biovolume for both swarm and non-swarm samples was collected at a site outside of the swarms, near Nolin Reservoir dam (USGS station 03310900), for estimated based on geometric shapes (Hillebrand et additional phytoplankton analyses. Samples from al. 1999). 100 mL from each zooplankton aliquot was filtered USGS station 03310900 were preserved with Lugol’s solution immediately following collection. A multi- through 35 µm mesh in order to transfer organisms parameter water-quality sonde, also stationed at USGS into ethanol. Zooplankton samples were then homogenized using a magnetic spinner at low speed and site 03310900, recorded water temperature, chlorophyll-a, pH, dissolved oxygen and turbidity at subsampled into Utermöhl chambers. Samples were 15-minute intervals both before and after the swarm counted using inverted light microscopes (Wilovert) at 100X to determine total abundance (organisms L-1). events took place, according to guidelines described After total abundance was determined, 100 individuals in Wagner et al. (2006). Phytoplankton and were examined from each sample and were clas- zooplankton samples were shipped overnight to BSA sified into four groups: males, females without eggs, Environmental Services, Inc. in Beachwood, Ohio, females with eggs and females with ephippia. For USA. The zooplankton, phytoplankton, and multi- females with eggs, the numbers of eggs were counted, parameter water-quality data are reported in Cherry and a mean was computed for number of eggs per et al. (2017) at https://doi.org/10.5066/F7BZ657V. female. Ten individual specimens from each sample were measured for body length (excluding head and Identification and enumeration tail spines), and biomass estimates were calculated Upon arrival at the laboratory, separate aliquots were based on established length/width relationships for taken from the whole water swarm samples for Daphnia ambigua Scourfield, 1947 found in McCauley zooplankton and phytoplankton analyses. Phyto- (1984). Length was compared between the two swarms plankton from swarm samples were preserved with using a t-test.

45 J.R. Beaver et al.

Figure 3. Photomicrographs of D. lumholtzi from swarm 1 including (A) female without eggs (B) female with eggs (C) female with ephippium and (D) male. Photos by T. Renicker.

Results Table 1. Daphnia lumholtzi abundance (# L-1), biomass (µg d.w.L-1), mean eggs per female, and size data for swarm samples taken on Microscopic analysis confirmed the presence of D. 1/4/2017. lumholtzi in the swarm samples. No other zooplankton species (crustaceans or rotifers) were observed within Swarm 1 Swarm 2 the swarm. Swarm specimens exhibited relatively Total 13,724 12,400 Female w/o eggs 11,665 9,920 reduced head and tail spines generally not Abundance Female w/ eggs 1,510 2,480 exceeding body length (Figure 3), unlike D. lumholtzi (#L-1) specimens typically observed in summer samples Female w/ ephippia 412 – where head and tail spines can greatly exceed body Male 137 – Biomass length. Densities of D. lumholtzi in the two whole- Total 284,953.3 192,906.8 (μg d.w. L-1) water swarm samples were 13,724 L-1 and 12,400 L-1, Eggs mean #/indiv. 7.1 8.1 for swarm 1 and swarm 2 respectively. Swarm popu- Min 0.53 0.58 lations were dominated primarily by female specimens Size (mm) Mean 1.70 1.80 (Table 1). Within the population of females, females Max 2.09 2.33 without eggs (11,665 L-1 and 9,920 L-1) were more

46 Winter swarm of Daphnia lumholtzi in a Kentucky reservoir

A 8 B 30 7 25 )

-1 6 20 5

4 15

3 10 2 (FNU) Turbidity Chlorophyll-a (µg L 5 1

0 0

Figure 4. Sonde data showing (A) chlorophyll-a (surface, µg L-1) and (B) turbidity (surface, FNU) at USGS station 0331900 beginning December 14, 2017 and ending January 14, 2017.

abundant than females with eggs (1,510 L-1 and Table 2.Phytoplankton biovolume (µm3 L-1) for non-swarm and 2,480 L-1). Females with eggs averaged approximately swarm samples. 7–8 eggs per clutch. Females with resting eggs Phytoplankton -1 -1 Nolin Reservoir Site Date Time (ephippia) (412 L ) and male specimens (137 L ) Biovolume (µm3 L-1) were only present in swarm 1. Mean length of D. Non-swarm 1 1/4/2017 9:30 2.51E+08 lumholtzi was similar between the two swarm samples, Non-swarm 2 1/4/2017 9:40 4.37E+08 with swarm 1 being slightly smaller on average Non-swarm 3 1/4/2017 10:00 2.26E+08 (1.70 mm) than swarm 2 (1.80 mm) (t(42)=0.76, Mean Non-swarm 3.05E+08 p > 0.05), mostly due to smaller egg-bearing females. Swarm 1 1/4/2017 12:00 2.95E+07 Phytoplankton populations inside the swarms ave- Swarm 2 1/4/2017 13:00 3.79E+07 raged nearly an order of magnitude less than outside Mean Swarm 3.37E+07 of the swarms (Table 2) and displayed limited diversity, consisting almost entirely of the Cyanobacterium Chroococcus microscopicus. The diversity of phyto- Discussion plankton in the non-swarm samples was high, avera- ging 18 species per sample. Non-swarm phytoplankton Since D. lumholtzi became established in North populations included C. microscopicus, but also America in the early 1990s, its seasonal dynamics contained several species of diatoms (Bacillariophyta) and distribution patterns have been in accordance and green algae (Chlorophyta), as well as representati- with the extensive literature and expectations for a ves from Euglenophyta, Cryptophyta and Chrysophyta. tropical invader in cooler, higher latitude ecosystems. Beginning in mid-December, 2016, chlorophyll-a Experimental studies indicate that the physiological concentrations began increasing and peaked at condition of D. lumholtzi at temperatures greater than approximately 6 µg L-1 in late December (Figure 4A), 25 °C is more robust than native daphnids (e.g. Work indicating that an increase in phytoplankton biomass and Gophen 1999b; Lennon et al. 2001). Although preceded the D. lumholtzi swarm. On January 3, 2017 there have been previous observations of D. lumholtzi (concurrent with the initial visual observation of D. in a North American reservoir during winter months lumholtzi swarms) chlorophyll-a concentrations rapidly (Sorensen and Sterner 1992, temperatures ranging decreased to about 1.5 µg L-1. Turbidity rapidly from 11–20 °C), peaks in D. lumholtzi abundance are increased (indicative of swarm formation) from more commonly reported to occur during late summer approximately 12 FNU on December 31, 2016 to a when water column temperatures are greatest (Work peak of approximately 25 FNU on January 6, 2017 and Gophen 1995; East et al. 1999; Havens et al. 2000; (Figure 4B). Temperatures in the top 5 meters of the Havel and Graham 2006). The late summer period in water column were approximately 8 °C during the North American lakes and reservoirs corresponds to swarm event. Sonde data also indicated that the surface a time of low algal food quality and an otherwise of the water column during the swarm was circum- poorly occupied niche by native daphnids (Lennon neutral (pH ~7.7) and well oxygenated (~9.2 mg L-1). 1999; Beaver et al. 2014). Considering the broad

47 J.R. Beaver et al. agreement between previous reports on the timing of despite lower water temperatures (Havel and Shurin maximum abundance of D. lumholtzi, the swarms 2004). Kentucky Reservoir (commonly known as observed in this study were highly unusual in the Kentucky Lake), located only about 250 km from timing of their occurrence. Nolin Reservoir, experiences annually recurring Environmental factors (both biological and physical) populations of D. lumholtzi (Levine and White 2009), contributing to zooplankton swarm development are albeit at relatively low concentrations. A swarm of D. poorly understood. Several drivers of swarming lumholtzi of similar composition to the one in this behavior in aquatic invertebrates have been examined study was described from Lake Cumberland (also a (Folt and Burns 1999), including predator avoidance reservoir), located approximately 145 km from Nolin (Pijanowska and Kowalczewski 2007), food availa- Reservoir, in October 2009 (Steinitz-Kannon and bility (Jakobsen and Johnsen 1988) and opportunity Lenca 2013), however this event was poorly for sexual reproduction (Young 1978). Experimental documented. Frisch et al. (2013) found that several studies show that swarming behavior by daphnids genetic strains of D. lumholtzi are present in the can occur in response to kairomones (chemical signals United States, which may be adapted to a range of emitted by predators and received by prey) from fish temperatures along a latitudinal gradient. It is likely and invertebrate predators such as Chaoborus that the same strain of D. lumholtzi occurs in (Pijanowska 1994; Jensen et al. 1998; Kvam and reservoirs nearby to Nolin, as it has been shown to Kleiven 1995). Fish kairomone production is also survive short-term human-mediated transfer between associated with increased spine length in D. lumholtzi water bodies (Havel and Stelzleni-Schwent 2000). when organisms are exposed in a pre-embryonic This implies that similar events to the one observed state (Dzialowski et al. 2003; Yurista 2000). in this study are possible elsewhere in the region. If Like most freshwater zooplankton, D. lumholtzi dispersal of D. lumholtzi continues to grow in scope, produces resting eggs prior to diapause. Resting eggs it is likely that similar swarm events could occur are encased into a hard ephippium (containing two elsewhere in the country. fertilized eggs) that is often deposited into the sediments to hatch once more favorable conditions are Conclusions encountered. Daphnia lumholtzi produces an order of magnitude more ephippia than native daphnids The abundance of D. lumholtzi reported in the (Acharya et al. 2006). Environmental cues that can current study far exceeds any published values. The trigger production of ephippia can include photope- occurrence of such large swarms of D. lumholtzi riod, desiccation, or temperature. Fish kairomones under the observed environmental conditions has are also associated with higher production of resting implications for future invasions. The strategy of eggs in mature females (Alekseev 2004; wintertime emergence and dropping of genetically Slusarczyket al. 2005). Ephippia frequently hatch en nuanced ephippia—during a period of low predation masse based on favorable environmental cues risk and limited competition from other daphnids— (Hairston et al. 1990; Hairston and Cáceres 1996), could represent a previously undetected route for which results in increases in water column abundance. successful invasion of new habitats. However, it is Given the unusual seasonal timing of the observed difficult to draw conclusions based on a single, events, it is possible that a strong and sudden isolated incident. Further monitoring of similar sites environmental cue (or suite of cues) induced D. in the future is needed to place this event in a lumholtzi ephippia to emerge (possibly from broader ecological context. ephippia deposited during a previous, undocumented swarm event). Temperature increase may be an Acknowledgements environmental cue breaking diapause; limited This study was funded by the U.S. Army Corps of Engineers. The distribution of D. lumholtzi in northern lakes and U.S. Geological Survey provided expertise for sampling as part of reservoirs where eggs in sediments are not subjected an interagency partnership that is funded by the U.S. Army Corps to elevated water temperatures supports this notion of Engineers. We thank the U.S. Army Corps of Engineers Nolin Reservoir staff and personnel, specifically, Libby Watt and Deryck (Lennon 1999). However, in this case it is unlikely Rodgers for being diligent public servants and reporting the event that temperature played a role. The increase in and the U.S. Army Corps of Engineers Huntington District Water chlorophyll-a, indicative of increased phytoplankton Quality Team members, Stephen Foster and Thaddeus Tuggle, for population growth, in the weeks preceding the their support in the initial investigation and sampling effort. Any opinions expressed in this paper are those of the author(s) and do swarm events is one possible environmental trigger not necessarily reflect the views of the U.S. Army Corps of that could explain the strange timing of the swarms. Engineers; therefore, no official endorsement should be inferred. Daphnia lumholtzi has had some invasion success Any mention of trade names or commercial products does not in reservoirs at higher latitudes in North America, constitute endorsement or recommendation for use.

48 Winter swarm of Daphnia lumholtzi in a Kentucky reservoir

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