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Newly Documented Host Fishes for the Eastern Elliptio Mussel Elliptio complanata William A. Lellis, Barbara St. John White,* Jeffrey C. Cole, Connie S. Johnson, Julie L. Devers, Ellen van Snik Gray, Heather S. Galbraith

W.A. Lellis U.S. Geological Survey, 12201 Sunrise Valley Drive, MS-300, Reston, Virginia 20192 B.S. White, J.C. Cole, C.S. Johnson, E.V.S. Gray, H.S. Galbraith U.S. Geological Survey, 176 Straight Run Road, Wellsboro, Pennsylvania 16901 J.L. Devers U.S. Fish and Wildlife Service, Maryland Fishery Resources Center, 177 Admiral Cochrane Drive, Annapolis, Maryland 21401

Abstract The eastern elliptio Elliptio complanata is a common, abundant, and ecologically important freshwater mussel that occurs throughout the Atlantic Slope drainage in the United States and Canada. Previous research has shown E. complanata glochidia to be host fish generalists, parasitizing yellow perch Perca flavescens, banded killifish Fundulus diaphanus, banded sculpin Cottus carolinae, and seven centrarchid species. Past laboratory studies have been conducted in the Midwest; however, glochidia used in these studies were obtained from adult mussels in the Great Lakes or St. Lawrence River basins, or glochidia sources were not reported. The objective of this study was to identify host fishes for E. complanata from streams in the Mid-Atlantic region. We used artificial laboratory infections to test host suitability of 38 fish and 2 amphibian species with E. complanata glochidia from the Chesapeake Bay drainage. Glochidia successfully metamorphosed into juvenile mussels on five fish species: American eel Anguilla rostrata, brook trout Salvelinus fontinalis, lake trout Salvelinus namaycush, mottled sculpin Cottus bairdii, and slimy sculpin Cottus cognatus. American eel was the most effective host, yielding the highest overall metamorphosis success (percentage of attached glochidia that transformed into juvenile mussels; $0.90) and producing 13.2 juveniles per fish overall. No juvenile E. complanata metamorphosed on other fish or amphibian species tested, including many previously identified host fishes that appear in the literature. Reasons for discrepancies in published host fish could include geographic variation in host use across the species’ range, differences in host use between lentic and lotic populations, or poorly resolved taxonomy within the genus Elliptio. Keywords: American eel; eastern elliptio; Elliptio complanata; glochidia; host fish; life history; Unionidae Received: October 22, 2012; Accepted: March 20, 2013; Published Online Early: March 2013; Published: June 2013 Citation: Lellis WA, White BS, Cole JC, Johnson CS, Devers JL, Gray EVS, Galbraith HS. 2013. Newly documented host fishes for the eastern elliptio mussel Elliptio complanata. Journal of Fish and Wildlife Management 4(1):75–85; e1944687X. doi: 10.3996/102012-JFWM-094 Copyright: All material appearing in the Journal of Fish and Wildlife Management is in the public domain and may be reproduced or copied without permission unless specifically noted with the copyright symbol ß. Citation of the source, as given above, is requested. The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service. * Corresponding author: [email protected]

Introduction Elliptio complanata (Bivalvia: Unionidae) is a common, widespread, and ecologically important freshwater mussel species that occurs throughout the Atlantic Slope Journal of Fish and Wildlife Management | www.fwspubs.org

drainage from Georgia to New Brunswick and Quebec, in the Great Lakes basins, the Saint Lawrence and Hudson Bay drainages of Ontario, and in select tributaries of the eastern Gulf of Mexico (Johnson 1970; Parmalee and Bogan 1998). Like most unionid mussels, E. complanata June 2013 | Volume 4 | Issue 1 | 75

Eastern Elliptio Host Fish

Table 1.

Historical studies reporting findings on host fish use for the freshwater mussel Elliptio complanata.

Source Young, 1911

a b

W.A. Lellis et al.

Study typea LI

Collection location for mussels and fish

Host fish Largemouth bass (Micropterus salmoides), green sunfish (Lepomis cyanellus), orangespotted sunfish (Lepomis humilus), white crappie (Pomoxis annularis), banded killifish (Fundulus diaphanus)

Not reported

Lefevre and Curtis, 1912

LI

Yellow perch (Perca flavescens)

Not reported

Matteson, 1948

LI

Yellow perch

Lake Michigan and Ocqueoc Lake in Michigan, United States

Watters et al., 2005

LI

Bluegill (Lepomis macrochirus), pumpkinseed (Lepomis gibbosus)

Not reported—St. Lawrence and Lake Champlain drainages in New York, United States (from pers. comm.)

Watters et al., 2007

LI

Bluegill, yellow perch, green sunfish, redear sunfish (Lepomis microlophus), banded sculpin (Cottus carolinae)

Not reported—St. Lawrence and Lake Champlain drainages in New York, United States (from pers. comm.)

Tedla and Fernando, 1969a

FO

Yellow perch

Bay of Quinte in Lake Ontario, Canada

Tedla and Fernando, 1969b

FOb

Yellow perch


Tedla and Fernando, 1970

FO

Yellow perch


Wiles, 1975a

FO

Banded killifish

Ponhook Lake and Five Islands Lake, Nova Scotia, Canada

Wiles, 1975b

FO

Banded killifish

Ponhook Lake and Shubencadie Lake, Nova Scotia, Canada

Kneeland and Rhymer, 2008

FO

White perch (Morone americana), yellow perch, banded killifish, smallmouth bass (Micropterus dolomieu), redbreast sunfish (Lepomis auritus), alewife (Alosa pseudoharengus), creek chub (Semotilus atromaculatus), white sucker (Catostomus commersonii), bluebackherring (Alosa aestivalis), threespine stickleback (Gasterosteus aculeatus), black crappie (Pomoxis nigromaculatus), brook trout (Salvelinus fontinalis)

Penobscot, St. George, and Kennebec Rivers in Maine, United States

LI, laboratory infections; FO, field observations. Field observation with metamorphosis observed in the laboratory.

requires a host fish in order to metamorphose from glochidia (larvae) into juvenile mussels. Previous laboratory host studies identified 10 fish species as hosts for E. complanata (Young 1911; Lefevre and Curtis 1912; Matteson 1948; Watters et al. 2005, 2007; Table 1). Additional studies have reported glochidia of E. complanata being attached to a total of 13 fish species in the wild in Ontario, Nova Scotia, and Maine (Tedla and Fernando 1969a, 1969b, 1970; Wiles 1975a, 1975b; Kneeland and Rhymer 2008; Table 1). The majority of laboratory studies took place in the Midwest and, while some reported sources of E. complanata glochidia in certain instances (e.g., Great Lakes), other literature provides no collection locations for the mussels or fish central to the studies. To our knowledge, no host fish studies of E. complanata have taken place in the MidAtlantic region of the United States and none have examined a wide cross-section of co-occurring fish species. Because host fish use for a single mussel species can vary among populations within and across river basins (Riusech and Barnhart 2000; Rogers et al. 2001), and because research to date on E. complanata appears to have only considered Great Lakes populations, further studies are needed to determine the ubiquity of these host fish findings across the mussel’s range. In this study, we used laboratory infections to examine suitability of potential host fish for E. complanata glochidia from the upper Susquehanna and Chester river Journal of Fish and Wildlife Management | www.fwspubs.org

basins in Pennsylvania and Maryland, major tributaries in the Chesapeake Bay watershed. Elliptio complanata is a dominant member of mussel assemblages throughout much of its range (Johnson 1970; Strayer and Jirka 1997; Nedeau 2008). Freshwater mussels play an important role in aquatic food webs and other ecological processes (Vaughn and Hakencamp 2001; Gutierrez et al. 2003) with dominant species often playing the most important roles. Therefore, understanding host fish relationships for these dominant species may be crucial for maintaining healthy mussel populations and thereby key ecosystem functions.

Methods Field collections We collected adult E. complanata primarily from Pine Creek, a tributary of the upper Susquehanna River in Tioga County, Pennsylvania; we also collected a few individuals from Andover Branch of the Chester River in Kent County, Maryland (Figure 1). We collected all mussels in late winter or early spring by snorkeling or with Plexiglas-bottom view buckets. We transported mussels in coolers of chilled river water to the U.S. Geological Survey Leetown Science Center’s Northern Appalachian Research Laboratory (NARL) or, for individuals for host trials with fishes in the Family Clupeidae, to the Joseph Manning Hatchery (JMH) in Brandywine, Maryland. We did not check gravidity in the field; instead, June 2013 | Volume 4 | Issue 1 | 76


W.A. Lellis et al.

Figure 1. Host fish suitability was tested for Elliptio complanata mussels collected from Pine Creek (A) in the upper Susquehanna River watershed (Pennsylvania) and Andover Branch (F) in the Chester River watershed (Maryland) between 1999 and 2008. Most potential host fish were obtained from Pine Creek (A) near the primary mussel source; some species were obtained from select locations throughout the Mid-Atlantic region (B–I).

mussels remained in the laboratory until they released glochidia naturally (see Laboratory Procedures). We collected fish from the wild using seines and backpack electrofishing gear, and most fish came from Pine Creek and its upstream tributaries. When collection from Pine Creek was not feasible, we obtained fish from other locations in nearby watersheds (Figure 1). In all cases, fish came from areas where mussels are not known to occur to minimize risk of prior exposure to glochidia (Arey 1932; Dodd et al. 2006). Further details of fish collections and fish sources can be found in Text S1 of the Supplemental Material. Laboratory procedures Once transported to the laboratory, mussels resided in flow-through glass aquaria with 10 cm of sand substrate. We increased water temperature and photoperiod gradually over several weeks, in accordance with local ambient conditions, to induce natural release of glochidia. Mussels typically released glochidia at 15–18uC in the form of mucous webs that remained temporarily suspended in the water column and then settled to the substrate (Figure 2A). We constructed aerated lift tubes Journal of Fish and Wildlife Management | www.fwspubs.org

using air stones that we placed inside 2-cm-diameter rigid, acrylic tubes and positioned the tubes in each tank to collect suspended glochidia in 100-mm mesh nylon sieves at the water surface (Figure 2B). We collected settled glochidia by using a siphon. We tested the viability of glochidia by exposing at least three subsamples of ,100 glochidia to salt; glochidia that snapped shut in response were considered viable (Zale and Neves 1982). We used glochidia from a release event in infections only if we observed at least 90% viability in three test samples. To infect fish with glochidia, we introduced individuals of each fish species into aerated 17.0–18.5uC water baths to mimic natural early summer water temperatures in Pine Creek, each containing a concentrated solution of viable glochidia collected within 8 h of natural release. We typically exposed fish in batches of multiple individuals depending upon numbers and sizes of fish available for testing. We infected small fish in 1-L beakers and larger fish in 19-L buckets or large, circular cattle tanks (0.6 or 1.2 m diameter, water depth ,15 cm). We infected American eels Anguilla rostrata, Atlantic sturgeon Acipenser oxyrhynchus, brook trout Salvelinus June 2013 | Volume 4 | Issue 1 | 77


W.A. Lellis et al.

Figure 2. Photograph of adult female Elliptio complanata releasing glochidia bound in a mucous strand (A) and diagram of aerated lift tubes used to capture suspended glochidia (B).

fontinalis, and lake trout Salvelinus namaycush both ways in different years: cattle tanks in 2000 and buckets or beakers in 1999, 2001, 2007, and 2008. In all containers, vigorously aerated water facilitated contact between fishes and glochidia. After a minimum of 40 min, we transferred fish to a second water bath without glochidia for an additional ,60 min, also at 17.0–18.5uC, where glochidia that had not fully attached during the initial exposure fell off. After infections, we transferred fish to 38- or 76-L aerated glass aquaria or to cattle tanks where we monitored them for the remainder of the experiment, generally 40–60 d. Fish ate a combination of commercial and frozen fish food for the duration of the experiment. Each aquarium or tank had a false bottom with a screen top that allowed shed glochidia and juvenile mussels to fall to the bottom of the aquarium, but prevented fish from feeding on or otherwise damaging them. Aquaria were siphoned 1 d after infections and then approximately three times each week until at least 1 wk after we found the last glochidium or juvenile mussel to ensure we did not miss any glochidia or juveniles. We filtered material that we siphoned from each aquarium through two sieves (500 and 100 mm) to separate glochidia and juveniles from unconsumed fish food and transferred them to a petri dish. We counted glochidia and metamorphosed juvenile mussels with a dissecting microscope with a polarizing lens (Johnson 1995). We identified juvenile mussels by their opaque shells and the presence of an active foot. Infections of 38 fish species and two amphibian species occurred at various times during multiple years (1999, 2000, 2001, 2007, and 2008; Table 2; Table S1, Supplemental Material). With the exception of infection trials of three fish species (common shiner Luxilus cornutus; rainbow trout Salvelinus namaycush; Atlantic salmon Salmo salar), juvenile E. complanata metamorphosed on at least one fish species in a given glochidial release event or we retested them during a second release event in which we observed juveniles, thereby confirming viability of glochidia used in infections. A Journal of Fish and Wildlife Management | www.fwspubs.org

glochidial release event was defined as a 3- to 4-d period of on-going glochidial release during which we typically conducted multiple trials. This method of ensuring the presence of juveniles after a given release event minimized the possibility of false negative results, although we cannot rule out the possibility of false negatives for the three species mentioned. We tested several select species, including the previously documented host yellow perch Perca flavescens, repeatedly. We also retested several newly identified hosts in additional trials to confirm initial results (Table 2). Trials for 35 fish and two amphibian species took place at NARL with glochidia from Pine Creek. Trials for three additional species (sensitive alosid species which could not be transported to or held at NARL: American shad Alosa sapidissima, blueback herring Alosa aestivalis, and hickory shad Alosa mediocis) took place at JMH with glochidia from Chester Creek. We captured and held alosid species during their upstream migration in Maryland during early spring 2008; during this time glochidia from naturally releasing E. complanata in Pine Creek were not available for infections. We also assessed the possibility of E. complanata glochidial metamorphosis without the use of a host fish because prior studies had shown this to occur in two other unionid species (Lefevre and Curtis 1911; Barfield and Watters 1998; Lellis and King 1998). We placed released E. complanata glochidia in aerated, flowthrough aquaria without fish and monitored them as already described for metamorphosis to juveniles. Similarly, we placed prematurely sloughed glochidia that had not undergone metamorphosis into petri dishes and monitored them for any continued development after sloughing. Finally, we also examined the gills of gravid E. complanata to detect any potential metamorphosis in the marsupial gills. Host suitability evaluation We assessed the relative suitability of host species by three methods. First, we estimated proportional metamorphosis success by dividing the number of June 2013 | Volume 4 | Issue 1 | 78


W.A. Lellis et al.

metamorphosed juveniles by the total number of juveniles and glochidia from each aquarium during the trial. For each fish species, we then calculated a single overall metamorphosis success value for multiple infection trials of each species by using summed values of glochidia and juveniles that we recovered in all trials. Second, we estimated per capita juvenile production for each host species by dividing the total number of juveniles produced in each trial by the total number of fish infected in that trial. For multiple trials, we summed total numbers of juveniles across all trials and divided the result by the total number of fish infected. Third, we qualitatively evaluated the length of time that glochidia remained on fishes. In this method, we categorized results into one of three categories: 1) all glochidia dropped off fishes in 1–3 d, indicating a lack of encystment or rapid rejection by the host immune response (Arey 1932; Waller and Mitchell 1989); 2) glochidia dropped off $4 d after infection but before completing metamorphosis into juvenile mussels, indicating successful encystment but inability to metamorphose; or 3) glochidia successfully achieved metamorphosis into juvenile mussels.

Results Five previously unreported host fishes for E. complanata were identified in this study: American eel, lake trout, brook trout, mottled sculpin (Cottus bairdii) and slimy sculpin (Cottus cognatus; Table 2). Metamorphosis success was highest on American eels ($0.90 for both elvers and yellow eels), but per capita juvenile production varied among eel developmental stages. Yellow eels had the highest per capita juvenile production of any fish species (13.2; range among multiple trials, 1.6–87.0), while elvers produced only 0.2 juveniles per fish (range, ,0.1–0.9). Among other suitable host species, metamorphosis success was highest on slimy sculpins (0.71, single trial) and lake trout (0.48 overall, 0.47 and 0.48 in two trials). Juvenile production on lake trout (7.4 juveniles per fish; range, 6.7–10.0) was comparable to, but less variable than on yellow eels, and production was low on slimy sculpins (1.7, single trial). Metamorphosis success and juvenile production were also low on mottled sculpins (0.14 and 1.5, respectively, in a single trial) and very low but variable on brook trout (0.01; range, 0.0–0.16 and 0.1; range, 0.0–6.0, respectively). The time necessary for juvenile metamorphosis overlapped in all host species, but metamorphosis began somewhat earlier on trout (16 d) than on eels (20 d) and sculpins (24 d), and the metamorphosis period extended the longest in eels (43 d). From all five host species, we also collected glochidia that were sloughed early or that encysted but did not metamorphose. However, the mean number of days to sloughing was higher in fish that tested positive as hosts (12.7 d) than in any nonhosts (mean = 7.5 days in nonhosts in which encystment occurred and mean = 2.6 days in nonhosts with failed encystment). No previously identified host fishes for E. complanata produced juvenile mussels in our study. Atlantic slope fish species (native and introduced) that served as hosts Journal of Fish and Wildlife Management | www.fwspubs.org

in past studies include banded killifish Fundulus diaphanus, yellow perch, bluegill Lepomis macrochirus, pumpkinseed Lepomis gibbosus, largemouth bass Micropterus salmoides, and green sunfish Lepomis cyanellus. In our study, glochidia remained attached for up to 10 d in most species, and as many as 14 or 17 d in fallfish and yellow perch (comparable to the period necessary for metamorphosis in host species). For some species, glochidia remained attached for fewer than 3 d (Table 2; Figure 3). Other species closely related to previously confirmed hosts also failed to produce juveniles (e.g., rock bass Ambloplites rupestris, redbreast sunfish Lepomis auritus, smallmouth bass Micropterus dolomieu), and glochidia typically remained attached for no more than 9 d. Previously identified hosts not native to the MidAtlantic region (i.e., banded sculpin Cottus carolinae, orangespotted sunfish Lepomis humilus, redear sunfish Lepomis microlophus, and white crappie Pomoxis annularis) were not tested here. Thirteen of 38 fish species and one of two amphibian species sloughed all glochidia within 0–3 d, indicating they rejected glochidia early on by immune response (Arey 1932; Figure 3). For four other fishes and redspotted newts Notophthalmus viridescens, we never observed sloughed glochidia, indicating that larval mussels failed to successfully attach during infection trials. Failed attachment or early sloughing occurred in approximately half of clupeid, centrarchid, and cyprinid fishes. Of all nonhost species, 16 retained glochidia for $ 4 d, indicating encystment occurred (most species shed glochidia in 4–10 d, while fallfish and yellow perch retained glochidia 14 and 17 d, respectively); however, these species sloughed all attached and encysted glochidia, and no glochidia that attached to these fish metamorphosed into juvenile mussels. These species included approximately half of cyprinids and centrarchids tested, as well as banded killifish, striped bass, rainbow trout, and all species in the Family Percidae. No marsupial metamorphosis or metamorphosis without a host fish was observed.

Discussion Young (1911) and Lefevre and Curtis (1912) conducted the earliest host identification studies of E. complanata in Missouri. Missouri is outside of the E. complanata range, yet interestingly the authors did not report the source locations of the mussels and fish used in these studies. Young (1911) summarized general observations of glochidial attachment and metamorphosis by four mussel species, including E. complanata, on four centrarchid species and banded killifish. She concluded that ‘‘the most successful infections were made’’ on these fishes; however, a reader cannot glean which fish species served as a host for which mussel species from this descriptive study, and it is consequently unclear which fish were hosts for E. complanata. Lefevre and Curtis (1912) definitively identified yellow perch as a host for E. complanata through artificial infections conducted in the laboratory, and glochidia metamorphosed within 14–16 d at 23uC. Likewise, Matteson (1948) showed yellow perch to be a host for E. complanata from Lake June 2013 | Volume 4 | Issue 1 | 79


W.A. Lellis et al.

Table 2. Results of host fish infection trials using glochidia of Elliptio complanata from Susquehanna River (PA) and Chester River (MD) watersheds, conducted between 1999 and 2008. Asterisk indicates early studies in which no fish counts were kept for select trials; numbers of glochidia and juveniles from trials with no fish counts are shown in parentheses. Numbers of glochidia and juveniles per fish were calculated only for trials with fish counts. No. trials represents the total number of infection trials conducted; No. fish, the total number of fish infected among all trials; No. shed gloch, the total number of shed glochidia observed across all trials for a given fish species; Days to shed gloch, days of the experiment during which shed glochidia were observed; No. gloch per fish, the total number of glochidia observed for a given fish species divided by the total number of fish tested of that species; No. juvs, the total number of juvenile mussels observed across all trials for a given fish species; Days to meta, days of the experiment during which metamorphosed juvenile mussels were observed; No. juvs per fish, the cumulative number of juveniles recovered during all trials of a given fish species divided by the cumulative number of fish of that species tested; Meta success, metamorphosis success for each fish species, or total number of juvenile mussels observed for a given fish species divided by the total number of glochidia and juvenile mussels observed for that species. See Table S1 (Supplemental Material) for detailed results of each trial, including water temperatures ranges and numbers of glochidia and juveniles observed. Days to No. shed gloch gloch per fish

No. trials

No. fish

No. shed gloch

Atlantic sturgeon

2

*

1

Anguilla rostrata

American eel (elvers)

3

1–15

0.18

Anguilla rostrata

American eel (yellow)

3

119

166

1–14

1.39 1,570

Alosa aestivalis

Blueback herring

1

12

295

1–2

24.58

Alosa mediocis

Hickory shad

1

10

99

1–2

9.90

Alosa sapidissima

American shad

1

19

0

—

—

Campostoma anomalum Central stoneroller

1

42

25

Exoglossum maxillingua Cutlip minnow

2

30*

Species

Common name

No. juvs

Days to No. juvs meta. per fish

Meta. success

Family Acipenseridae Acipenser oxyrhynchus

2

*

0

—

—

—

21–43

0.24

0.94

20–37

13.19

0.90

0

—

—

—

0

—

—

—

0

—

—

—

Family Anguillidae 80*

16 (2)

252 (233)

Family Clupeidae

Family Cyprinidae 3

0.60

0

—

—

—

6 (0)

3

0.20

0

—

—

—

68 (0)

2–7

0

—

—

—

0.24

0

—

—

—

Luxilus cornutus

Common shiner

1

*

Nocomis micropogon

River chub

2

17

Notropis hudsonius

Spottail shiner

2

14

61

1–7

4.36

0

—

—

—

Notropis rubellus

Rosyface shiner

1

6

14

1–5

2.33

0

—

—

—

Pimephales notatus

Bluntnose minnow

1

20

0

—

—

0

—

—

—

Rhinichthys atratulus

Eastern blacknose dace

1

6

2

7

0.33

0

—

—

—

Rhinichthys cataractae

Longnose dace

1

7

0

—

—

0

—

—

—

Semotilus corporalis

Fallfish

1

10

6

8–14

0.60

0

—

—

—

2

36*

3

1.42

0

—

—

—

—

—

0

—

—

—

0.70

0

—

—

—

—

4

1–3

*

Family Catostomidae Catostomus commersonii White sucker

51 (10)

Family Ictaluridae Ameiurus natalis

Yellow bullhead

1

*

Noturus insignis

Margined madtom

2

30*

0

Oncorhynchus mykiss

Rainbow trout

1

Salmo salar

Atlantic salmon

1

Salvelinus fontinalis

Brook trout

4

115*

Salvelinus namaycush

Lake trout

3

114*

Banded killifish

1

10

Cottus cognatus

Slimy sculpin

2

Cottus bairdii

Mottled sculpin

1

22 (1)

2–3

*

2 (2)

5

*

0

—

—

*

1 (1)

2

*

0

—

—

—

1,736 (4)

1–18

15.06

11 (0)

18–31

0.10

0.01

927 (8)

2–14

8.08

847 (0)

16–37

7.43

0.48

106

1–8

0

—

—

—

24–33

1.67

0.71

25–32

1.45

0.14

Family Salmonidae

Family Fundulidae Fundulus diaphanus

10.6

Family Cottidae 3* 20

Journal of Fish and Wildlife Management | www.fwspubs.org

2 (0) 183

1–8

0.67

5–7

9.15

5 (0) 29

June 2013 | Volume 4 | Issue 1 | 80


Table 2.

W.A. Lellis et al.

Continued.

Species

Common name

No. trials

No. fish

No. shed gloch

Days to No. shed gloch gloch per fish

No. juvs

Days to No. juvs meta. per fish

Meta. success

Family Moronidae Morone saxatilis

Striped bass

1

6

140

1–4

23.33

0

—

—

—

Ambloplites rupestris

Rock bass

1

16

77

3

4.81

0

—

—

—

Lepomis auritus

Redbreast sunfish

1

4

121

1–8

30.25

0

—

—

—

Lepomis cyanellus

Green sunfish

1

4

19

1–5

Lepomis gibbosus

Pumpkinseed

1

3

468

1–5

Lepomis macrochirus

Bluegill

1

3

10

2

Micropterus dolomieu

Smallmouth bass

1

20

15

Micropterus salmoides

Largemouth bass

2

3*

26 (0)

1

3

19

Family Centrarchidae

Poxomis nigromaculatus Black crappie

4.75

0

—

—

—

0

—

—

—

3.33

0

—

—

—

3

0.75

0

—

—

—

2

8.67

0

—

—

—

2–9

6.33

0

—

—

—

0.33

0

—

—

—

0

—

—

—

156

Family Percidae Etheostoma olmstedi

Tessellated darter

2

12*

5 (1)

3–5

Etheostoma zonale

Banded darter

2

10*

1,635 (1)

1–7

Perca flavescens

Yellow perch

3

96*

330 (1)

Percina peltata

Shield darter

1

4

American toad (tadpole)

2

100*

Red-spotted newt

1

10*

163.4

2–17

3.43

0

—

—

—

7

1.00

0

—

—

—

29 (20)

2–3

0.09

0

—

—

—

0 (0)

—

—

0

—

—

—

4

Family Bufonidae Anaxyrus americanus Family Salamandridae Notophthalmus viridescens

Michigan and Ocqueoc Lake in the lower Michigan peninsula, and also tested six centrarchid species, two cyprinid species, and three darter species, none of which served as hosts. To our knowledge, the only other laboratory assessments of E. complanata host fishes are the identifications of bluegill, pumpkinseed, yellow perch, green sunfish, redear sunfish, and banded sculpin as hosts for E. complanata from lakes in the St. Lawrence and Lake Champlain drainages of upper New York state (Watters et al. 2005, 2007; G.T. Watters, personal communication.). Other studies have documneted E. complanata glochidia attached to yellow perch and banded killifish in the wild in Lake Ontario, and in Nova Scotian lakes, respectively (Tedla and Fernando 1969a, 1969b, 1970; Wiles 1975a, 1975b; Table 1). Using molecular genetics techniques, Kneeland and Rhymer (2008) identified glochidia of E. complanata on the gills of 13 fish species, with highest incidence of infection on white perch Morone americana and yellow perch. Five centrarchid and two clupeid fishes also were infected, as well as brook trout, banded killifish, and threespine stickleback Gasterosteus aculeatus. Documentation of glochidial attachment in the wild provides important information about potential fish hosts; however, confirmation of metamorphosis is critical in determining whether a given fish species actually produces juvenile mussels. In this study, E. complanata glochidia remained attached to 16 fish species for up to 17 d without ever achieving Journal of Fish and Wildlife Management | www.fwspubs.org

metamorphosis; in the wild, E. complanata glochidia may well attach temporarily to fish that ultimately do not serve as hosts. Elliptio complanata is ubiquitous and often the dominant member of mussel assemblages in the Northeast and Mid-Atlantic regions. For example, in the Delaware River (Pennsylvania, New York, New Jersey) E. complanata was present in 99.6% of stream reaches surveyed, and its average density in these reaches often exceeded 20/m2 (W. Lellis, unpublished data). Consequently, we would expect E. complanata to complete metamorphosis without a host fish (a phenomenon that was not observed in our study) or use a host fish that was historically native, abundant, and widespread. While brook trout and sculpins are common and often dominant species in high-gradient cold water streams in Pennsylvania, including Pine Creek (Cooper and Wagner 1971; Cooper 1983), they occur less commonly in lower gradient and warmer streams where E. complanata is often abundant. Similarly, lake trout are found primarily in deep, cold, oligotrophic lakes and are typically absent from streams in the Susquehanna River basin and elsewhere within the range of E. complanata. Other previously identified hosts for E. complanata (e.g., yellow perch, largemouth bass, sunfishes) occur frequently in rivers in Pennsylvania and elsewhere, but are more numerous in ponds, reservoirs, and lakes than in lotic systems (Jenkins and Burkhead 1993; Pennsylvania Fish and Boat Commission [PFBC] 2009). These other June 2013 | Volume 4 | Issue 1 | 81


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Figure 3. Bars show the range of days during which glochidial attachment and production of juveniles were observed among tested fish species in host fish identification trials conducted between 1999 and 2008. Light gray bars indicate Elliptio complanata glochidia detaching 1–3 d post infection, dark gray indicates glochidia detaching in $4 d, and black indicates production of metamorphosed E. complanata juveniles. Dashed lines indicate fish species that sloughed no glochidia (i.e., presumably no glochidia ever attached). See Table S1 (Supplemental Material) for detailed results of each trial, including water temperature ranges and numbers of glochidia and juveniles observed in each trial.

species may be important hosts in some situations (e.g., lentic habitats), but their limited occurrence, combined with their marginal suitability or apparent unsuitability as hosts, make them unlikely to be important hosts for E. complanata in streams such as Pine Creek. In contrast, American eels are widespread and abundant in undammed Atlantic coastal river systems, and historically constituted as much as 25% of fish biomass in several rivers (Atlantic States Marine Fisheries Commission [ASMFC] 2000). Although reduced in numbers and somewhat restricted in distribution in impounded river systems, American eels remain prominent components of lotic fish assemblages in many Atlantic Slope river systems. This, combined with their robust metamorphosis of glochidia, makes them a far more likely candidate for the primary host fish of E. complanata in this region. Interestingly, elvers under 10 cm tested in this study produced very few metamorphosed juveniles, potentially as a function of gill filament size and surface area. This suggests intraspecific variation in host suitability, which warrants further research. Many other resident fish species occur along the Atlantic Slope that we did not test in our study. While we did test a broad range of fish taxonomic groups, testing other species for Journal of Fish and Wildlife Management | www.fwspubs.org

host suitability is warranted in future studies, as well as confirming unverified negative results reported here (e.g., common shiner, rainbow trout, and Atlantic salmon). Discrepancies between the findings of this and other studies of host fish suitability for E. complanata is curious, but may lie in the unresolved taxonomy of the genus Elliptio. Elliptio phylogeny has long been debated, particularly in the southern Atlantic Slope region, and remains in question today (Bogan 2002; Watters 2008; Haag 2010). A major biogeographical boundary separating distinctive Northern Atlantic and Southern Atlantic mussel faunas occurs in the vicinity of the lower Chesapeake Bay (Haag 2010), and immigration of mussels among many Atlantic Coast rivers may be low or nonexistent, with the result that populations in these rivers represent largely independent phylogenetic lineages (King et al. 1999; Bogan 2002). Variation in host use occurs even within relatively stable taxa, although this variation spans a much lower taxonomic breadth of fish species than reported for E. complanata (Riusech and Barnhart 2000; Rogers et al. 2001). Because of its large geographic range and high likelihood of extensive population genetic divergence, similarly high variation June 2013 | Volume 4 | Issue 1 | 82


in host use within the E. complanata group seems plausible. To our knowledge, no other studies have documented American eel as a suitable host fish for any unionid mussels; however, eels have rarely been the focus of tests, making their viability as hosts largely unknown. Availability of suitable host fish has long been shown to impact distribution and abundance of freshwater mussels (Williams et al. 1993; Watters 1996; Kelner and Sietman 2000) and loss of migratory fish hosts is of particular concern because mussels with access only to local host fish with limited dispersal capabilities risk their own isolation (Schwalb et al. 2011a; Vaughn 2012). Other migratory fish species are known hosts for Atlantic Slope mussels, including striped bass and juvenile Atlantic salmon, both hosts for the dwarf wedgemussel Alasmidonta heterodon (Wicklow 2004; White 2007), and American shad, a host for the alewife floater Anodonta implicata (Smith 1985). Blueback herring Alosa aestivalis and white perch can also serve as hosts for A. implicata (B. Watson, Virginia Department of Game and Inland Fisheries, personal communication). In the Interior Basin, black sandshell Ligumia recta metamorphose on sauger Sander canadensis (Khym and Layzer 1995), the primary host for the ebonyshell Fusconaia ebena and elephant-ear Elliptio crassidens is skipjack herring Alosa chrysochloris, and the hickorynut Obovaria olivaria uses shovelnose sturgeon Scaphirhynchus platorynchus as a host (Watters 1994). Use of migratory hosts or other fish that swim long distances is likely advantageous for mussel dispersal and in many cases necessary for population survival (McLain and Ross 2005; Schwalb et al. 2011b). Given that eels proved a robust host for E. complanata in our study, have an extensive historic range, and likely play an important role in glochidial dispersal for this abundant and ubiquitous mussel, future research may be warranted to examine suitability of eels as hosts for other mussel species. Such studies may be of particular interest because eels have experienced a significant decline in North America during the past 50 y, particularly in dammed river systems (Freeman et al. 2003; Hitt et al. 2012). At the very least, ongoing loss of these fish by overharvest, stream blockage, and other anthropogenic stressors (ASMFC 2000; Freeman et al. 2003; Limburg and Waldman 2009) may significantly impact E. complanata abundance and distribution in many coastal watersheds. Decoupling of these fish and mussel species or the displacement of either from coastal rivers may produce significant ecosystem-level effects that are not yet well understood.

Supplemental Material Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding author for the article. Text S1. Summary of test fish sources and fish collection methods used in preparing for host fish infection trials conducted using glochidia of Elliptio complanata from Susquehanna River (PA) and Chester River (MD) watersheds between 1999 and 2008. Journal of Fish and Wildlife Management | www.fwspubs.org

W.A. Lellis et al.

Found at DOI: http://dx.doi.org/10.3996/102012JFWM-094.S1 (11 KB DOCX). Table S1. Detailed results of host fish infection trials conducted using glochidia of Elliptio complanata from the Susquehanna River (PA) and Chester River (MD) watersheds, carried out between 1999 and 2008. Fish ID represents an identifying number for tested fish species in taxonomic order; SciName, fish scientific name; ComName, fish common name; Family, fish taxonomic family; Release Event, each multi-day period of on-going glochidial release during which multiple trials were conducted; Trial ID, identifying number for each infection trial in order by date; Fish Count, number of fish tested in a given trial; Date Infected, date the infections for each trial were performed; Temp (uC), range of water temperatures observed in each tank during the course of each trial; No. Gloch, total number of glochidia recovered in each tank; Gloch/Fish/Tank, number of glochida recovered from each tank divided by the number of fish held in that tank; Gloch/Fish/Trial, the number of glochidia recovered from all tanks in a given trial divided by the number of fish used in that trial; Gloch/Fish/Spp, the cumulative number of glochidia recovered during all trials of a given fish species divided by the cumulative number of fish of that species tested; Days to Gloch, days of the experiment during which shed glochidia were observed; No. Juv, number of juvenile mussels recovered during each trial; Juv/Fish/ Tank, number of juveniles recovered from each tank divided by the number of fish held in that tank; Juv/ Fish/Trial, number of juveniles recovered from all tanks in a given trial divided by the number of fish used in that trial; Juv/Fish/Spp, cumulative number of juveniles recovered during all trials of a given fish species divided by the cumulative number of fish of that species tested; Days to Meta, days of the experiment during which metamorphosed juvenile mussels were observed; Meta Succ Tank, metamorphosis success in each tank, or number of juvenile mussels recovered from a given tank divided by the total number of glochidia and juvenile mussels recovered from that tank; Meta Succ Trial, metamorphosis success in each trial, or number of juvenile mussels recovered for a fish species in a given trial divided by the total number of glochidia and juvenile mussels recovered for that fish species in that trial; Meta Succ Spp, metamorphosis success for each fish species, or total number of juvenile mussel observed for a given fish species over multiple trials divided by the total number of glochidia and juvenile mussels observed for that species. Found at DOI: http://dx.doi.org/10.3996/102012JFWM-094.S2 (85 KB XLS). Reference S1. ASMFC (Atlantic States Marine Fisheries Commission). 2000. Interstate fishery management plan for the American eel (Anguilla rostrata). Fishery Management Report No. 36 of the Atlantic States Marine Fisheries Commission. Found at DOI: http://dx.doi.org/10.3996/102012JFWM-094.S3 (633 KB PDF). June 2013 | Volume 4 | Issue 1 | 83


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Reference S2. Lefevre G, Curtis WC. 1912. Studies on the reproduction and artificial propagation of fresh-water mussels. Bulletin of the U. S. Bureau of Fisheries 30:109– 201. Found at DOI: http://dx.doi.org/10.3996/102012JFWM-094.S4 (3.9 MB PDF). Reference S3. White BS. 2007. Evaluation of fish host suitability for the endangered dwarf wedgemussel Alasmidonta heterodon. Masters Thesis, The Pennsylvania State University, University Park, PA. Found at DOI: http://dx.doi.org/10.3996/102012JFWM-094.S5 (1.4 MB PDF). Reference S4. Young D. 1911. The implantation of the glochidium on the fish. University of Missouri Bulletin Science Series, 2(1): 1–16. Found at DOI: http://dx.doi.org/10.3996/102012JFWM-094.S6 (7.1 MB PDF).

Acknowledgments We thank D. Dropkin and R. Bennett of the U.S. Geological Survey (USGS), R. Horwitz and P. Overbeck at the Academy of Natural Sciences in Philadelphia, and P. Ferreri of Penn State University for assisting in field collections and identifications of fish. D. Honeyfield of the USGS and J. Mohler at U.S. Fish and Wildlife Service Northeast Fishery Center provided select hatchery raised fish, and C. Stence and K. White of Maryland DNR provided migratory fish species for testing. D. Sien and staff at Joseph Manning Hatchery assisted with tank maintenance. We thank K. Hawk, J. Hotter, C. Morrow, and K. Shaw for assisting in laboratory infection trials. W. Haag reviewed a draft of this manuscript and provided valuable feedback. The authors also thank two anonymous reviewers and the Subject Editor for their helpful comments.

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