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Population demographics and life history of the round Hickorynut (Obovaria subrotunda) in the Duck River, Tennessee.

INTRODUCTION

Freshwater mussels reach their greatest diversity in North America with 90% of the 300 recognized taxa occurring in the Southeastern United States (Williams et al., 1993). The abundance and diversity of native mussels began to decline as early as the mid-19th century (Strayer et al., 2004), and they have experienced one of the highest rates of extinction of any group of organisms (Neves et al., 1997) with 84 species listed as endangered or threatened by the United States Fish and Wildlife Service (USFWS, 2013). These declines are due mostly to habitat destruction, pollution, land-use change, commercial exploitation, and exotic species introductions (Strayer et al., 2004). The decline of mussel populations and the extinction of species are well documented. For instance the greatest diversity of freshwater mussels in the world once occurred at Muscle Shoals, on the Tennessee River in Alabama. In the early 1900s, Ortmann (1925) reported 75 species at Muscle Shoals; however, Isom (1969) found that only 39 species remained, due primarily to the construction of dams along the Tennessee River.

Freshwater mussels have a unique reproductive cycle. Eggs are produced in the ovaries of the female and moved to specialized chambers within the marsupial gills. Subsequently, females uptake sperm released by males into the water column and, after fertilization, the embryos develop into larvae (glochidia) in the marsupium. During this brooding period, the female mussel is said to be gravid. Mussels can be divided into two general types of brooders. Tachytictic species are short term brooders that hold their glochidia for a relatively short period during summer and/or fall. Bradytictic species are long term brooders that hold their glochidia for an extended period, typically from fall until the following spring or summer. Once released, glochidia are obligate parasites on the gills or fins of specific fish hosts. Glochidial hosts are known only for about one-third of the mussel species in North America (O'Dee and Watters, 2000), but the identification of these hosts is essential to the restoration and management of rare species of mussels (Gordon et al., 1994). Once glochidia metamorphose into free-living juveniles, they become sessile organisms on the lake or stream bottom. Fecundity of individuals can range from less than 100 to over 1 million glochidia, depending on the species, size, and habitat (Haag and Staton, 2003; Moles and Layzer, 2008). Life spans of freshwater mussels are variable, ranging from less than 10 y to over 100 y (Bauer, 1992; Haag and Rypel, 2011). Freshwater mussels exhibit indeterminate growth, and, similar to trees, they form much narrower growth rings in the winter due to decreased growth. These narrow growth rings, known as annuli, can be used to approximate the ages of mussels (Neves and Moyer, 1988).

The Duck River, Tennessee contains one of the most diverse fish and mussel faunas in North America; historically, 69 species of mussels (Schilling and Williams, 2002) and approximately 150 species offish occurred in the river (Etnier and Starnes, 1994). In a recent survey, Ahlstedt et al. (2004) found 54 extant mussel species, including three endangered (Epioblasma ahlstedti, Lemiox rimosus, and Quadrula intermedia), two candidates for listing (Pleuronaia dolabelloides and Q. c. cylindrica), and two potential candidates for listing (Pleuronaia barnesiana and Obovaria subrotunda). The robust mussel populations in the Duck River provide a unique opportunity to document demographics of healthy mussel populations. This, in turn, can provide a scientific basis for judging the health of other populations.

This study focused on Obovaria subrotunda, a widespread species that occurs in the Ohio River drainage, the Great Lakes system, and a few tributaries in the lower Mississippi River drainage (Parmalee and Bogan, 1998). Although it is a widespread species, O. subrotunda has been extirpated from 110 of the approximately 270 water bodies where it once occurred (Butler, pets. comm.). As a result it is a species-of-concern in the United States and is a federally endangered species in Canada.

Obovaria subrotunda is sexually dimorphic, as females have a more rounded posterior margin than males and a slight sulcus (Watters et al., 2009). A bradytictic species, Obovaria subrotunda have been found gravid every month of the year, but data on gravidity were compiled from studies in multiple river systems over time (Gordon and Layzer, 1989). Shepard (2006) identified five hosts for O. subrotunda: Etheostoma variatum (variegate darter), E. baileyi (emerald darter), E. blennioides (greenside darter), E. gore. (cumberland darter), and Percina stictogaster (frecklebelly darter). However, only one of these species, E. blennioides, occurs in the Duck River (Etnier and Starnes, 1994). Additional life history information necessary for future conservation and management of O. subrotunda is lacking.

There were two primary objectives of this study: (1) determine the reproductive biology of O. subrotunda including its spawning and brooding period, fecundity, and host fish use; (2) determine local population sizes and population demographics including age, growth, sex ratio, and size structure of O. subrotunda.

METHODS

This study was conducted in the Duck River in Marshall and Maury counties in middle Tennessee. The Duck River, a major tributary of the Tennessee River, is 468 km in length and drains 8100 [km.sup.2] of the southern portion of the Eastern Highland Rim, the Nashville Basin, and the southern portion of the Western Highland Rim physiographic provinces (Theis, 1936). From 1972-1976, the Tennessee Valley Authority (TVA) constructed Normandy Dam at Rkm 400 on the Duck River. It is operated for flood damage reduction, water supply, and recreational opportunities. Mussel declines on the Duck River were cited as early as 1968, before the construction of the dam (Isom and Yokley, 1968; van der Schalie, 1973). Isom and Yokley (1968) stated that phosphate ore mining and pollution below cities and industries had negatively affected mussels in some areas. Between 1988-2002, populations of most mussel species in the Duck River increased dramatically. These increases have been attributed to improvement in habitat, including the institution of a minimum flow and oxygenation of water released from Normandy Dam, the elimination of point source pollution, and land management practices (Ahlstedt et al., 2004). Based on preliminary sampling, we selected four study sites 113 to 144 km downstream of Normandy Dam (Fig. 1). Site 1 was located at 35.59208-86.78507, Site 2 at 35.61611-86.81274, Site 3 at 35.62093-86.81856, and Site 4 at 35.60298-86.89820.

Mussels were collected periodically by snorkeling, beginning on 22 Jul. 2010 and ending on 18 Feb. 2011. During each sampling trip, water temperature was measured and recorded. Females were carefully pried open to examine the gills, and all individuals with inflated gills were considered gravid. The spawning and development period was determined by extracting a portion of the gill contents at streamside on each occasion until gills were found to contain only fully developed glochidia. Gill content samples were taken by carefully rupturing and flushing several watertubes, and contents were stored in separate vials containing 70% ethanol for transport back to the laboratory. In the laboratory, the samples were examined with a microscope to monitor embryo development; the presence of eggs, developing glochidia, or developed glochidia was recorded. Developing glochidia were distinguished from developed glochidia by still being bound within the egg membrane.

On 22 Sept. 2010, 30 gravid O. subrotunda were collected from the study area, immediately euthanized, and stored in individual sealed plastic bags containing 70% ethanol. In the laboratory, the marsupial gills were excised and disassociated in the petri dish. Both marsupial gills of ten individuals were used to determine if fecundity varied between gills; because it did not, only the right gill was used to estimate fecundity for the remaining individuals. The gill contents were then pipetted into a zooplankton counting wheel and all glochidia and eggs were counted by direct enumeration using a dissecting microscope (40 x). Fecundity was determined by doubling the total number of glochidia and eggs in the right gill. Total length (mm) was measured for each O. subrotunda, and each shell was thin-sectioned and aged following methods of Neves and Moyer (1988). A paired t-test was used to compare fecundity between gills within individuals. A [Log.sub.10] transformation was performed on the variables (fecundity, total length, and age) and regression analyses were used to determine the relationship between fecundity, total length, and age. Analysis of covariance was used to test for similarities among ages for fecundity adjusted for total length. Significance was determined at the [alpha] = 0.05 level.

For the host study, we used a backpack electrofisher to collect fish from the upper Duck River and its tributaries. Emphasis was placed on species of the family Percidae occurring in the Duck River drainage because Shepard (2006) tested nine families and 48 species of fish and found that O. subrotunda glochidia only metamorphosed on five species in the family Percidae. The 11 Etheostoma sp. used in the host trials were the percid species encountered during intensive sampling on the Duck River. Two cyprinid species and Cottus carolinae were tested because they were abundant at the sampling sites. Fish were transported in coolers to the laboratory where they were acclimated at a rate of 2 C a day to a temperature of 20 C. In Nov. gravid O. subrotunda were collected and placed into separate plastic bags in case glochidia were expelled during transport. Mussels were held in a flow-through raceway at the Normandy Fish Hatchery until needed. Glochidia were prepared for infestation by rupturing marsupia and disassociating glochidial masses into a container of clean aquarium water. A subsample of glochidia was used to assess viability by exposing them to a weak saline solution; viable glochidia close quickly when stimulated. We conducted two host trials using the same methods. The first infestation was conducted on 17 Nov. 2010 and included nine percid species and two cyprinid species. The second infestation was conducted on 5 Jul. 2011 and included two percid species and Cottus carolinae. Glochidia were pipetted into separate buckets, filled with 7 L of clean aquarium water, and an air stone was placed into each bucket to suspend glochidia. Fish were separated by species, placed in buckets for 30 min to allow glochidia to attach to the gills, and then transferred to another set of buckets for 5 min to allow unattached glochidia to settle out. Fish were returned to aerated aquaria to recover and were maintained at a temperature of 19 C ([+ or -]0.42 SE) for the first infestation and 22 C ([+ or -] 0.11 SE) for the second infestation. Bottom contents of the aquaria were siphoned daily, and the siphonate was passed through a 120 [micro]m sieve to retrieve all particulate matter. The particulate matter was examined with a microscope for metamorphosed juveniles. Siphoning ceased 1 wk after the last juvenile was recovered and examination of fish revealed no encysted glochidia. The number of transformed glochidia and the days to transformation were recorded.

Because O. subrotunda is sexually dimorphic, age and growth analyses were conducted separately for males and females. One hundred fresh dead shells (50 males and 50 females) were collected from muskrat middens. Thin-sections were prepared following the methods of Neves and Moyer (1988). Two consecutive sections (~200 [micro]m in thickness) were cut from the umbo to the shell margin with a Buehler Isomet low-speed saw with a diamond wafering blade. Thin-sections were examined with a dissecting microscope, and the number of growth arrests, for each thin-section, were counted twice. The distal edge of each annulus on each thin-section was marked, and the marks were transferred onto the uncut valve. To determine length-at-annulus, the distance between the anterior and posterior ends of each marked external growth line was measured to the nearest 0.1 mm with dial calipers. The first, and sometimes the second, annulus was missing due to erosion of the umbo region on older individuals; ages of these individuals were estimated by adding 1 or 2 y to the number of visible annuli. Length-at-age was computed using the von Bertalanffy growth curve (VBGC) (von Bertalanffy, 1938). The VBGC is expressed as:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

where [L.sub.[infinity]] is the theoretical maximum (asynaptotic) length, k is a growth coefficient indicating how quickly [L.sub.[inifinity]] is approached, t is time or age in years, [t.sub.0] is time in years when length would theoretically be equal to zero, and e is the base of the natural logarithm. Total length and age of each shell was [Log.sub.10] transformed and regression analysis was used to estimate the relationship between total length and age. Analysis of covariance (ANCOVA) was used to compare regression equations for each sex.

A systematic sampling design, with three random starts, was used for quantitative sampling following methods described by Strayer and Smith (2003). The area of the sampling plots was predetermined for each site. The number of quadrat samples was calculated using the formula:

n = [s.sup.2]/[0.10.sup.2] x [bar.x]]

where n is the number of quadrats, [s.sup.2] is the variance, 0.10 is a precision of [+ or -] 10%, and [bar.x] is the mean density. The number of quadrats needed to estimate density with a precision of [+ or -] 10% at each site was calculated based on preliminary sampling. The mussel bed length, the river width, and the number of quadrats were used to determine the distance between quadrats laterally and longitudinally. The distance between quadrats was calculated using the formula:

d = [square root of L x W/n/k]

where d is the distance between quadrats, L and W are the length and width of the study site, n is the total number of quadrats, and k is the number of random starts (Smith et al., 2001; Strayer and Smith, 2003). Random coordinates were generated to obtain the three starting locations. A measuring tape was run along each bank parallel to each other, and a third measuring tape was set perpendicular to the flow to locate sampling points. At each point, the lower left hand corner of a quadrat (0.25 [m.sup.2]) was placed on the substrate. Quadrats were excavated to a depth of about 10 cm with a hand trowel, all excavated material was placed into a 3 mm mesh bag, and a unique alphanumeric tag was placed into each bag to identify the quadrat location. At streamside the contents of each bag were emptied into 12 and 6 mm mesh sieves to separate mussels from sediment. Mussels and the sample tag were placed into 6 mm mesh bags, identified to species, and total length was measured to the nearest millimeter. Total length, gravidity, and sex were recorded separately for each quadrat and mussels were placed back into the substrate. All four sites were sampled using this protocol during Sept.-Nov. 2010. A portion of Site 1 was also quantitatively sampled a second time on 1 Oct. 2010 to increase the O. subrotunda sample size for the length frequency analysis. Density and population estimates of O. subrotunda were calculated from the quantitative sampling data and analyzed using the Mussel Estimation Program (version 1.5.2, 20 Mar. 07) available from the Leetown Science Center, U.S. Geological Survey (http://www.lsc.usgs.gov/aeb/2068/index.asp). The second quantitative sample from Site 1 was not included in this analysis. Chi-square goodness-of-fit tests were used to compare sex ratios at each site, and significance was determined at the [alpha] = 0.05 level. All statistical analyses were performed using the Statistical Analysis Systems software (SAS statistical software, version 9.2, SAS Institute, Inc., Cary, North Carolina).

RESULTS

A total of 151 females were examined for gravidity from Jul. 2010-Feb. 2011 (Table 1). In Jul. all females examined were gravid. Most females released all of their glochidia within a 3 d period in early Aug. and recharged their gills within 2 wk. We found only eggs in the marsupial gills on 26 Aug., but fully developed glochidia were present 19 d later. All females [greater than or equal to] 18 mm long examined from Aug.-Feb. were fully gravid (Table 1). Due to high flows no further sampling was conducted after Feb.

Fecundity was determined for 30 individuals collected on 22 Sept. 2010 from Site 1. There was no difference in the number of glochidia in the right and left marsupial gills (t = 0.10, df = 9, P = 0.92); therefore, fecundity was determined for the remaining 20 females by doubling the number of glochidia found in the right gill. Mean fecundity was 36,101 ([+ or -] 2849 SE) and ranged from 7122 to 76,584. Age of individuals ranged from 1 to 11 y old and total length ranged from 21-36 mm. There was a positive linear relationship between fecundity and length and fecundity and age (Table 2). However, fecundity did not differ among age groups adjusted for length (F = 1.82, df = 6, 28, P = 0.14).

A total of 14 fish species representing three families were artificially infested with glochidia. The subsample of glochidia exposed to a weak saline solution responded by snapping shut indicating they were viable. Metamorphosis of glochidia did not occur on ten species (Etheostoma caeruleum, E. crossopterum, E. aquali, E. rufilineatum, E. blennius, E. simoterum, E. zonale, E. camurum, Luxilus chrysochephalus, and Notropis telescopus). In the first trial, metamorphosis of glochidia occurred 20 to 33 d post-infestation on Etheostoma obama and E. blennoides at 19 C ([+ or -] 0.42 SE). Sixteen transformed juveniles were collected from 26 E. obama with a mean number of 0.62 juveniles per fish, and 19 transformed juveniles were collected from 15 E. blennioides with a mean number of 1.30 juveniles per fish. In the second trial, metamorphosis of glochidia occurred 27 to 31 d post-infestation on E. flabellare and Cottus carolinae at 22 C ([+ or -] 0.11 SE). Two transformed juveniles were collected from six E. flabellare with a mean number of 0.33 juveniles per fish, and four transformed juveniles were collected from eight C. carolinae with a mean number of 0.50 juveniles per fish.

One hundred shells (50 males and 50 females) were aged from thin-sections and there was a 98% agreement between the first and second aging. Ages of individuals estimated from thin-sections ranged from 1 to 13 y for females and 1 to 14 y for males. Mean lengths ([l.sub.l]) at annulus formation were fitted to the von Bertalanffy growth equation separately for males ([l.sub.l] = 49.5(1 - [e.sup.-0.272(t + 0.002)])) and females ([l.sub.l] = 40.3(1 - [e.sup.-0.247(t - 0.195)])) and used to predict values for length (Fig. 2). Predicted length-at-age indicated that both males and females exhibit the greatest amount of growth in their first four growing seasons. On average, males grew 11.79 mm in length the first year, 9.00 mm the second year, 6.85 mm the third year, and 5.22 mm the fourth year; growth then declined to a mean of 0.54 mm for years 11 to 14. On average females grew 10.31 mm in length the first year, 6.57 mm the second year, 5.13 mm the third year, and 4.01 mm the fourth year; growth then declined to a mean of 0.57 mm for years 11 to 13. Analysis of covariance indicated that males grew significantly faster than females (F = 12.94, df = 1, 96, P = 0.0005).

A total of 1419 mussels, representing 29 species, were collected from excavated quadrats, and Obovaria subrotunda represented 9% of all mussels collected. Mean density of O. subrotunda ranged from 0.26 to 3.66 mussels/[m.sup.2] and estimated local population size ranged from 365 to 4394 among sites (Table 3). Estimated density and population size for O. subrotunda was highest at Site 4 where it accounted for 41% of all mussels collected (Table 3). Estimated density and population size of O. subrotunda was second highest at Site 1 and accounted for 7% of all mussels collected (Table 3). Obovaria subrotunda accounted for 4% of all mussels collected at Sites 2 and 3. Estimated densities of O. subrotunda were similar at Sites 2 and 3, but Site 3 had a higher estimated population size than Site 2 because the mussel bed at Site 3 occupied a larger area (Table 3). There was a total of 165 individuals (74 males, 75 females, and 16 juveniles) used to calculate the sex ratio and to construct the length-frequency distributions. The overall sex ratio (M:F) was not significantly different from 1:1 ([chi square] = 0.007, df = 1, P = 0.93). The sex ratios at Sites 1, 3, and 4 were not significantly different from 1:1 (P = 0.41); however, the sex ratio at Site 2 had significantly more females than males ([chi square] = 7.4, df = 1, P = 0.007). A length-frequency distribution for all sites combined showed that 90% of females were between 20 and 31 mm in length (Fig. 3). Based on the length-age relationship calculated using the von Bertalanffy growth equation, these females were 1 to 5 y of age. Seventy percent of males were between 22 and 39 mm in length and 1 to 5 y of age. Juveniles (<1 y old) accounted for 10% of all O. subrotunda captured in the quadrat samples. However, one-half of these juveniles were captured at Site 3.

DISCUSSION

In the Duck River, the brooding period of O. subrotunda was unusually long. Ortmann (1919) indicated that O. subrotunda was gravid from Sept. through May; he considered the one gravid individual he found in early Aug. to be quite unusual. Similarly, gravid O. subrotunda are uncommon after Apr. in the North Fork Hughes River, West Virginia (P. Morrison, per. comm.). In contrast O. subrotunda in the Duck River brooded glochidia until early Aug. and then spawned by mid to late Aug. It is unknown if this prolonged brooding period is due to genetic or environmental factors. Brooding impedes respiration and feeding efficiency (Tankersley and Dimock, 1993; Tankersley, 1996), and ova production requires a substantial allocation of energy. Females of some species do not spawn every year; presumably, during the nonspawning (pausing) years, these females are replenishing depleted energy reserves (Bauer, 1998; Moles and Layzer, 2008). All female O. subrotunda examined between 26 Aug. and 18 Feb. were gravid, indicating they do not pause. The short time span between expelling glochidia and recharging their marsupia indicates that the later stages of oogenesis were well under way while females brooded the previous cohort. Thus, brooding females acquired sufficient energy for maintenance, growth, and gamete production. The prolonged brooding period and the synchronous release of glochidia (most females released in a 3 d period) may be a strategy targeting young-of-the-year (YOY) host fish at a time when they are most abundant and perhaps most susceptible to infestation. In Tennessee YOY darters can comprise >60% of early fall darter populations (Simmons et al., 2008). Earlier in the summer, YOY may be less susceptible to infestation because of their smaller size, behavior, or habitat use. Though they were not confirmed by collecting glochidial infected fish from the wild, most of the hosts we identified in the laboratory are common widespread species in the eastern United States (Etnier and Starnes, 1994). Hosts of O. subrotunda identified in our study are also used by several other mussel species occurring in the Duck River. For instance E. flabellare is a host for Medionidus conradicus (Zale and Neves, 1982), Ptychobranchus subtentum, Lasmigona costata (Luo, 1993), and Epioblasma ahlstedi (Jones et al., 2006). The use of the same host species by multiple mussel species raises the possibility of host competition because after being infested with glochidia, fish can develop immunity to subsequent glochidial infestations (Arey, 1923; Rogers and Dimock, 2003), and fish with developed immunity to glochidia of one species are immune to glochidia of other species (Doddet al., 2005). Strayer (2008) modeled the effects of developed immunity on mussel abundance and suggested that cross-species immunity could result in interspecific competition for hosts. However, species should avoid competition if possible (Pianka, 1978). Since developed immunity may be lost over time, temporal partitioning of hosts would be a viable alternative to interspecific competition. Other species that use the same hosts as O. subrotunda tend to release glochidia in the spring or early summer when YOY may not be present or because of their behavior and habitat use may not be susceptible to infestation. By releasing glochidia in early Aug., O. subrotunda may be capitalizing on the large number of immunologically naive fish (YOY that have never encountered glochidia) and fish infested in Aug. could be used as hosts by other species the following spring.

A host attraction strategy has not been reported previously for O. subrotunda (Shepard, 2006; Watters, 2008) or for other Obovaria species (Haag and Warren, 2003; Zannatta and Murphy, 2006). Mussels lacking specific host-targeted strategies tend to be host generalists (Barnhart et al., 2008). However, only Cottus carolinae and three of the 11 Etheostoma spp. tested in this study were suitable hosts, indicating that O. subrotunda is somewhat of a host specialist. Our observation of a conglutinate released in Aug., when most females synchronously expelled their broods, could explain the lack of a documented host targeted strategy for O. subrotunda and perhaps other Obovaria species, if conglutinates are formed only near the end of the brooding cycle.

Fecundity in freshwater mussels is usually a function of size and age (Downing et al., 1993; Haag and Staton, 2003). Fecundity of O. subrotunda was related to both size and age, but the relationship with size explained a greater amount of variation. Moreover, fecundity adjusted for length did not differ among ages. Fecundity of O. subrotunda is similar to like-sized species. For instance, Jones et al. (2010) found that fecundity for Lemiox rimosus ranged from 4132 to 58,700 glochidia in the Duck River, and Rogers et al. (2001) reported fecundity of a single Etheostoma florentina aureloa to be 20,000 glochidia. These two species, as well as O. subrotunda, can be classified as small mussels (Parmalee and Bogan, 1998). In contrast fecundity of larger species such as Actinonaias ligamentina and Lampsilis siliquoidea is more than an order of magnitude greater than for O. subrotunda (Perles et al., 2003; Moles and Layzer, 2008).

Watters et al. (2009) stated that few O. subrotunda live longer than 12 y and individuals can grow quickly for the first 4-5 y. Our results agree with their observations, as only three individuals aged were more than 12 y old, and the oldest age examined was 13 y for females and 14 y for males. A male 57 mm long collected alive in a quadrat sample was not aged but could have been older. A regression of age on length ([R.sup.2] = 0.78) predicted that this individual was 15 y old; however, the unaccounted variation in the regression suggests this individual could have been somewhat younger or older than predicted. Additionally, both males and females exhibited the greatest amount of growth in their first 4 y. Observed age, total length, and growth rate were greater in males than females. Most sexually dimorphic mussels exhibit differences in age and growth between sexes (Haag and Rypel, 2011). Freshwater mussels experience life history trade-otis between reproduction and growth (Heino and Kaitala, 1997; Haag and Rypel, 2011). Presumably, female O. subrotunda are putting forth more energy into reproduction than males and therefore grow more slowly than males. Based on aging of gravid females, O. subrotunda is sexually mature at age 1. This is significant in that many freshwater mussels become sexually mature at age 3 or later (Weaver et al., 1991; Jirka and Neves, 1992; Eads et al., 2006; Davis and Layzer, 2012); however, it is not a unique trait as Haag and Staton (2003) found Lampsilis ornata reached sexual maturity in its first growing season. In contrast to O. subrotunda, O. unicolor does not reach maturity until age 4 (Haag, 2012). Ridgway et al. (2011) found that maximum adult life span in bivalves is significantly and positively correlated with age at maturity. Because O. subrotunda has a shorter life span compared to many freshwater mussels (Bauer, 1992; Christian et al., 2000; Anthony et al., 2001; Moles and Layzer, 2008; Haag and Rypel, 2011), it may compensate by having an early age at sexual maturity. In general early maturity is associated with short to moderate life spans and low to intermediate fecundity (Haag, 2012).

Overall O. subrotunda density has increased in the Duck River over the past 30 y. In 1979 O. subrotunda density was 0.05 mussels/[m.sup.2] (Ahlstedt, 1986). In 1988 no O. subrotunda were collected in quadrat samples, but one individual was found in snorkel surveys (Jenkinson, 1988). Density increased to 0.31 mussels/[m.sup.2] in 2002 (Ahlstedt et al., 2004), and in 2010, O. subrotunda density was 0.89 mussels/[m.sup.2]. As stated earlier, this increase has been credited to the institution of a minimum flow and oxygenation of water released from Normandy Dam, the reduction of point source pollution, and land management practices (Ahlstedt et al., 2004). Berg et al. (2008) found that most freshwater mussel populations have sex ratios close to 1:1. With the exception of Site 2, Obovaria subrotunda exhibited a balanced sex ratio. Site 2 had significantly more females then males, but the fewest individuals were collected at Site 2. Thus, the unbalanced sex ratio at Site 2 may be due to the small sample size. There was evidence of recent O. subrotunda recruitment over several years due to the presence of young individuals over many size classes. Specifically, the population was made up mostly of individuals that were 1-5 y of age and were recruited into the population since the most recent survey by Ahlstedt et al. (2004). Recent recruitment was most evident at Site 3 where 40% of individuals collected in the quadrat samples were < 1 y. Many mussel populations are comprised mostly of large old individuals with little or no recruitment because of human pressures on the population (e.g., Hardison and Layzer, 2001). Conversely, the O. subrotunda population in the Duck River was characterized by recent recruitment, multiple age classes, and with all females participating in reproduction indicating the population was healthy and possibly still increasing.

CONCLUSIONS

The robust O. subrotunda population in the Duck River provided a unique opportunity to study population and life history characteristics of a healthy population. The increase of population size and density, and the high proportion of 1 to 5 y olds in the Duck River can be attributed to several things. Firstly, O. subrotunda uses common, widespread fish species as hosts. The increase in population size and regular recruitment indicates that releasing conglutinates in early Aug. when YOY host fishes are abundant is a highly effective glochidial infection strategy. Secondly, O. subrotunda is sexually mature at 1 y meaning individuals are important contributors to the reproducing population at an early age. Lastly, the water quality and the physical habitat in the river have improved in the past 30 y allowing continued recruitment, survival, and growth of O. subrotunda in the Duck River. In contrast, O. subrotunda has been extirpated or is in a state of decline throughout much of its range. Populations of many species in the Duck River have increased concurrently with O. subrotunda showing that if the causes of mussel declines can be identified (particularly habitat degradation) and ameliorated, O. subrotunda as well as other imperiled mussel species have the potential to be recovered throughout their ranges.

Acknowledgments.--The Tennessee Wildlife Resources Agency provided primary funding for this research. Additional funds and support were provided by the Center for Management, Utilization, and Protection of Water Resources at Tennessee Technological University and the Tennessee Cooperative Fishery Research Unit. We thank Kendall Moles, Stephanie Barton, Travis Dailey, Grant Lynch, Ron Cicerello, and Stephanie Chance for assistance with the field work. We also thank Don Hubbs, David Berg, and two anonymous reviewers for providing helpful comments on an earlier draft. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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SUBMITTED 3 FEBRUARY 2012

ACCEPTED 19 JUNE 2013

CHASE A. EHLO (1)

Tennessee Cooperative Fishery Research Unit, Tennessee Technological University, Cookeville 38505

AND

JAMES B. LAYZER

U.S. Geological Survey, Tennessee Cooperative Fishery Research Unit, Tennessee Technological University, Cookeville 38505

(1) Corresponding author present address: Native Fish Lab, Marsh and Associates, LLC, Tempe, AZ 85282; e-mail: chase.ehlo@gmail.com

TABLE 1.--Gravidity, spawning, and glochidial development of Obavaria
subrotunda collected from the Duck River, Tennessee from Jul. 2010 to
Feb. 2011

                        Percent                                  Temp
Date             Site    gravid     N        Gill contents         C

22-Jul-10         1       100      12                             27
8-Aug-10          1        75      16                             28
11-Aug-10         1        8       13                             28
12-Aug-10         1        0        7                             28
16-Aug-10         3        0        4                             27
26-Aug-10         1       100      16    Eggs                     26
9 Sept. 2010      1       100       2    Developing and fully     22
                                           developed glochidia
14 Sept. 2010     1       100       2    Glochidia                22
22 Sept. 2010     1       100      14                             24
1-Oct-10          1       100      11                             20
2-Oct-10          3       100       2                             17
18-Oct-10         2       100      10                             16
11-Nov-10         4       100      24                             13
18-Feb-11         1       100      18                             10

TABLE 2.--Relationship between fecundity, age, and total length for
Obovaria subrotunda collected from Site 1 in the Duck River,
Tennessee. [B.sub.0] represents the intercept of the line and
[B.sub.1] represents the slope of the line

Dependent variable   [B.sub.0]    [B.sub.1]    Independent variable

Logo Fecundity          4.01         0.74      [Log.sub.10] Age
Logo Fecundity         -0.83         3.65      [Log.sub.10] Mussel
                                                 length

Dependent variable   [R.sub.2]       P

Logo Fecundity          0.61      <0.0001
Logo Fecundity          0.75      <0.0001

TABLE 3.--Site locality and population characteristics of Obovaria
subrotunda determined from quantitative sampling at four sites in the
Duck River,  Tennessee. The total number collected at each site is the
combined number of males, females, and juveniles

         River         Area       Number of      Density
Site   kilometer    ([m.sup.2])    quadrats     (90% C.I.)    Males

1        286.7         1200          118           1.25         19
                                               (1.01-1.56)
la       286.7          360           62            --          17
2        281.4          880          106           0.42         1
                                               (0.28-0.61)
3        280.6         3800          304           0.26         6
                                               (0.22-0.31)
4        257.6         1200           71           3.66         32
                                               (3.14-4.27)

                               Population
                                estimate       Relative
Site   Females    Juveniles    (90% C.I.)    abundance (%)

1         16          2           1505            7.2
                              (1208-1875)
la        14          1            --             --
2         10          0           365             4.2
                               (247-539)
3         6           8           1000            4.1
                               (850-1177)
4         28          5           4394           41.1
                              (3772-5120)
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Author:Ehlo, Chase A.; Layzer, James B.
Publication:The American Midland Naturalist
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Date:Jan 1, 2014
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