Abstract

The narrow pigtoe Fusconaia escambia is a freshwater mussel found only in the Escambia and Yellow river basins in northwest Florida and southern Alabama. The U.S. Endangered Species Act lists it as threatened. Like other freshwater mussels (Unionidae), its life cycle involves a larval stage (i.e., glochidial) in which most species are obligate parasites on the gills or fins of fishes. Knowledge of life history, population demographics, population genetics, and threats for the narrow pigtoe is lacking throughout its range, which impedes conservation of this species. Therefore, our objectives were to 1) compare historical and current distribution data using a conservation status assessment map, 2) determine period of gravidity, and 3) identify fish hosts. We used a conservation status assessment map to examine spatial and temporal changes in narrow pigtoe distribution and the possibility that the species has been extirpated from a subbasin (i.e., Hydrologic Unit Code level 10 watershed boundary; U.S. Geological Survey National Hydrography Dataset). We determined period of gravidity for the narrow pigtoe by examining the gills of mussels in the field, and considered peak gravidity to be the month in which we encountered the greatest number of gravid females. We determined fish hosts by infecting individuals of 18 fish species with glochidia in a laboratory setting. Overall, the narrow pigtoe appears to be maintaining stable populations in Florida, but researchers have conducted too few surveys in Alabama subbasins for us to fully assess its status throughout its range. Peak months of gravidity were May–July, with the greatest percentage of gravid females observed in May, although we observed them as early as 9 March and as late as 25 October. We identified nine fish species from five genera as hosts for narrow pigtoe, with Blacktail Shiner Cyprinella venusta and Weed Shiner Notropis texanus consistently producing the greatest number of viable juvenile mussels. Host and gravidity findings from this study will be useful if propagation efforts become necessary for conservation of the narrow pigtoe.

Introduction

The Southeast is a hot spot for freshwater mussel diversity in the continental United States, but 98% of the region's mussel species are imperiled (Williams et al. 2014). In Florida, 15 freshwater mussel species are federally threatened or endangered under the U.S. Endangered Species Act (ESA 1973, as amended), and 53 species are federally threatened or endangered in Alabama (USFWS 2015). Information about life history, demographics, population genetics, and threats is lacking for many of these imperiled mussels, but all of that information is necessary for their conservation.

The narrow pigtoe Fusconaia escambia is one of the mussel species listed as threatened or endangered under the ESA (1973) in northwest Florida and southern Alabama and for which research is necessary to improve understanding of its conservation needs. The U.S. Fish and Wildlife Service (USFWS) designated narrow pigtoe as federally threatened in 2012 because of its apparent rarity, limited distribution, and susceptibility to threats such as habitat degradation and environmental contaminants (USFWS 2012). It is endemic to the Escambia River basin in Florida and Alabama (known as the Conecuh River in Alabama) and the Yellow River basin in Florida (Williams et al. 2014). Researchers do not fully understand the habitat requirements for the narrow pigtoe in these river basins but describe it as medium to large creeks and medium rivers in slow to moderate current with stable substrates (USFWS 2012; Williams et al. 2014). The narrow pigtoe is also locally abundant in Gantt and Point A reservoirs on the Conecuh River in Alabama (Williams et al. 2008; Figure 1). Between 1995 and 2012, surveyors found narrow pigtoe at 28 locations in the Escambia River and four locations in the Yellow River (USFWS 2012). During this period, they collected 166 individuals, with 23 of them from the Yellow River (USFWS 2012). Historical collection information for this species is sparse, but recent surveys (May 2013–March 2018) in Florida and Alabama should improve understanding of this species' distribution throughout its range. Additionally, comparing historical and current survey data will provide a better understanding of the status and trends of narrow pigtoe populations.

Figure 1.

Conservation status assessment map showing historical vs. present distribution of the narrow pigtoe Fusconaia escambia in the Escambia and Yellow river basins in Alabama and Florida at the HUC10 subbasin scale. Subbasins with darker shades of red indicate more recent records; white subbasins indicate no reported detection of narrow pigtoe. Subbasins in which surveys detected narrow pigtoe, as well as other subbasins of interest, are labeled with the last three digits of the 10-digit HUC code and -E or -Y for Escambia or Yellow river basin, respectively. Black points represent sites at which surveys have detected narrow pigtoe, white points represent surveys conducted since 2008 (1 January 2008–31 December 2018), and gray points represent surveys conducted before 2008. The map also provides locations of Point A and Gantt reservoirs (104-E).

Figure 1.

Conservation status assessment map showing historical vs. present distribution of the narrow pigtoe Fusconaia escambia in the Escambia and Yellow river basins in Alabama and Florida at the HUC10 subbasin scale. Subbasins with darker shades of red indicate more recent records; white subbasins indicate no reported detection of narrow pigtoe. Subbasins in which surveys detected narrow pigtoe, as well as other subbasins of interest, are labeled with the last three digits of the 10-digit HUC code and -E or -Y for Escambia or Yellow river basin, respectively. Black points represent sites at which surveys have detected narrow pigtoe, white points represent surveys conducted since 2008 (1 January 2008–31 December 2018), and gray points represent surveys conducted before 2008. The map also provides locations of Point A and Gantt reservoirs (104-E).

Along with information about the status of the narrow pigtoe, life history information is lacking for this species. The freshwater mussel (Unionidae) life cycle involves a larval stage (i.e., glochidial stage) in which most species are obligate parasites on the gills or fins of fishes (Williams et al. 2014). Mussels can be host generalists or specialists, and each mussel species uses a specific suite of fish hosts (Haag 2012). If a glochidium does not attach to the correct host fish species, it cannot complete its life cycle, so, for conservation, it is important for researchers to know the mussel's host-fish requirements. Additionally, knowing the period of gravidity for mussels is valuable for mussel propagation efforts so that researchers can better understand the time of year when glochidia (from the wild or from hatchery broodstock) are mature and ready to attach to a host fish. Our goal in this study was to improve understanding of the population status and life history of the narrow pigtoe. Specifically, our objectives were to 1) compare historical and current distribution data using a conservation status assessment map, 2) determine the period of gravidity, and 3) identify host fish.

Methods

Distribution

We mapped the current and historical distribution of the narrow pigtoe in Florida and Alabama following methods described by Johnson et al. (2016). First, we compiled narrow pigtoe collection records and localities from survey data, field notes, and museum specimens. We compiled survey data and field notes from the Florida Fish and Wildlife Conservation Commission Freshwater Mussel Database (Gainesville, Florida) and two collections databases from the USFWS (Table 1). We examined museum specimens of narrow pigtoe at six institutions, and biologists with extensive experience identifying the fauna verified their identification (Table 1). Historical surveys often unclearly described their survey methods, which were usually more qualitative than quantitative, but recent surveys (May 2013–March 2018) by Florida Fish and Wildlife Conservation Commission biologists followed quantitative methods described by Johnson et al. (2016), which employ timed visual–tactile methods in all habitat types from the stream bank out toward the thalweg. Two to six biologists conducted snorkel surveys for a total of 1 person-h (e.g., two snorkelers surveying for 30 min), but deep sites (> 2.5 m) required scuba diving. Biologists identified mussels to species, counted them, identified them as live or dead, and checked them for gravidity (Johnson et al. 2016).

Table 1.

Agencies and entities that provided narrow pigtoe Fusconaia escambia collection records and localities (1917–2018) from survey data, field notes, and museum specimens.

Agencies and entities that provided narrow pigtoe Fusconaia escambia collection records and localities (1917–2018) from survey data, field notes, and museum specimens.
Agencies and entities that provided narrow pigtoe Fusconaia escambia collection records and localities (1917–2018) from survey data, field notes, and museum specimens.

We constructed a conservation status assessment map (CSA map) following methods described by the Georgia Department of Natural Resources (Georgia DNR 2019) and Johnson et al. (2016). This type of map is useful for assessing the spatiotemporal distribution of a species at the subbasin level (Hydrologic Unit Code level 10; HUC10), which is a scale that is appropriate for and commonly used in conservation of aquatic species. We developed the CSA map using ArcMap 10.3 (Esri, Redlands, CA), and main data components included U.S. Geological Survey National Hydrography Dataset HUC10 basin boundaries and all narrow pigtoe collection records and survey data. We included all positive and negative localities from our compiled field notes and survey data in this analysis.

The CSA map allowed us to examine two things: 1) spatial and temporal changes in narrow pigtoe distribution and 2) the possibility that the species had been extirpated from a subbasin. Our analysis using the CSA map was similar to that described by Johnson et al. (2016). We determined spatial and temporal changes in narrow pigtoe status by comparing the number of positive narrow pigtoe surveys (at least one narrow pigtoe found) per location per year in each subbasin. The number of narrow pigtoe found would have been a better metric, but that information was not reliably available. The extirpation of narrow pigtoe from a subbasin was considered possible if there had been no positive surveys from that subbasin since 2008 (1 January 2008–March 2018), despite adequate survey effort. We considered survey effort adequate when 10 or more total surveys had been conducted since 2008 or at least one survey was positive. We chose 2008 as our cutoff year because it was 10 y prior to when we conducted this analysis and it roughly represents the lifespan of an adult narrow pigtoe.

Period of gravidity

We compiled gravidity information for the narrow pigtoe from Florida Fish and Wildlife Conservation Commission surveys in the Escambia River in Florida from June 2014 through October 2018. Because a female narrow pigtoe is indistinguishable from a male based on shell characteristics, we examined all mussels for gravidity in the field. We gently opened shell valves and examined the gills without the aid of magnification. We considered a mussel gravid if its gills were inflated or had a grainy appearance due to the presence of eggs or glochidia. We also examined and recorded gill color. Since we did not use magnification to examine the gill contents of gravid mussels, the specific stage of gravidity (e.g., a mussel brooding eggs, immature glochidia, or mature glochidia) for each mussel is not available from this study. We considered peak gravidity to be the month in which we observed the greatest percentage of gravid females.

Host identification

We collected potential host fish and gravid mussels for host-fish trials in May and June of 2014 and 2015. We collected the fish from the Blackwater River because it is naturally devoid of mussels (Williams et al. 2014), which ensured the fish had not developed an immunity to glochidia from a previous glochidial infection (Reuling 1919; Rogers and Dimock 2003). We collected all fish using boat electrofishing gear or a seine, and held the fish in a flow-through aquarium system for at least 2 wk before use in a trial. We monitored gravidity of narrow pigtoe at three locations on the Escambia River in Escambia County, Florida: the Molino boat ramp (30°43′25.14″N, 87°18′20.73″W), a location about 1 km upstream of the Molino boat ramp (30°43′49.52″N, 87°18′38.33″W), and the Mystic Springs boat ramp (30°51′14.79″N, 87°18′40.913″W). We took gravid mussels to the laboratory and held them in aerated containers of well water at room temperature (approximately 21°C) until the mussel naturally released conglutinates (packages of glochidia; Haag and Warren 2003; Harriger et al. 2015).

Prior to infecting fish with glochidia, we determined the number of viable glochidia available for each trial. First, we determined the percentage of glochidia that were viable (i.e., immature vs. fully developed) by observing their reaction to salt crystals (NaCl). Fully developed, viable glochidia snap rapidly when introduced to salt (Zale and Neves 1982). We determined the total number of glochidia (viable and nonviable) in a known volume of water by calculating the average number of glochidia in four subsamples and extrapolating to the known volume. Finally, we multiplied the total number of glochidia by the percentage of viable glochidia to determine the total number of viable glochidia available. The target viable glochidia concentration for infecting potential host fish was 2,000–4,000 viable glochidia/L of water (Dodd et al. 2006; Johnson et al. 2012; Johnson et al. 2016; McLeod et al. 2017). We used four narrow pigtoe for host trials in this study: one individual for the 2014 trials, one individual for trials 1 and 2 in 2015, one individual for trial 3 in 2015, and one individual for trial 4 in 2015. We did not determine fecundity for any of the mussels used in this study.

We infected 18 fish species with glochidia over the course of the study using methods similar to those of Harriger et al. (2015). The focal fish species in this study were Cyprinella spp. and Notropis spp., since researchers consider mussels of the genus Fusconaia to be host specialists on Cyprinidae (Williams et al. 2014). We placed five or six individuals of the various fish species together in 4.73-L buckets with 1.5 L of water and glochidia. We ensured that contents of the bucket were aerated and stirred gently so that glochidia remained suspended in the water. We used an air stone and the associated air hose to stir contents of the buckets. After 30 min, we returned each fish to its own tank in the aquarium system. In 2015 only, we rinsed each fish with clean water to remove unattached glochidia before returning fish to tanks to more closely follow standard methods (e.g., Johnson et al. 2012). We placed a filter cup (5.1-cm polyvinyl chloride tubing with 64-μm mesh on one end) at the outflow of each tank to collect glochidia and transformed juvenile mussels. We took no measures to prevent fish from ingesting transformed juvenile mussels.

We monitored the transformation of glochidia into juvenile mussels by examining filter cups approximately every 48 h from July through August in 2014 and 2015. We counted the total numbers of glochidia, viable juvenile mussels, and nonviable juvenile mussels for each fish. We identified viable juveniles by the presence of a foot and movement, and considered any juvenile that showed no movement to be nonviable (Haag and Warren 1997; Harriger et al. 2015). We considered any fish that produced viable juvenile mussels to be a host. We determined the suitability of each fish species as a host by evaluating three criteria: percentage of metamorphosis, number of viable juvenile mussels produced, and percentage of a fish species that produced viable juvenile mussels (O'Brien and Brim Box 1999; Harriger et al. 2015). We calculated percentage of metamorphosis success (%M) as %M = (viable juveniles/[viable juveniles + nonviable juveniles + glochidia]) × 100 for each fish in the study (Dodd et al. 2006; Johnson et al. 2012; Harriger et al. 2015). Considering these three criteria helps determine the importance of a host relative to the other hosts identified in the study (O'Brien and Brim Box 1999; Harriger et al. 2015).

Many studies conduct one or two host fish trials, and each trial includes several replicates for each fish species. This method works well when larger numbers of glochidia (> 4,000) can be collected from a mussel in a short amount of time before glochidia viability declines (McLeod et al. 2017). However, some mussels, like narrow pigtoe in this study, release conglutinates fractionally over several days or weeks, making it difficult to collect sufficient numbers of glochidia in a short amount of time (McLeod et al. 2017). Therefore, we conducted six trials over the course of this study to achieve replication and representation of potential host fish species. For each trial, we tested up to 10 fish species, and each species was represented by one individual (n = 1). Since minnows were the focal fish group, six minnow species had four replicates over the course of six trials. Other fish species had fewer replicates.

Results

Distribution

We found 217 records of the narrow pigtoe in the Escambia and Yellow river basins since 1917. We provide an archive of this data set, which includes all available metadata associated with all narrow pigtoe specimens and freshwater mussel surveys (Table S1, Supplemental Material). Before 2008, researchers encountered this species in 96 of 440 (21.8%) surveys, with positive surveys in 16 and 2 subbasins in the Escambia and Yellow river basins, respectively. Since 2008 (1 January 2008–March 2018), researchers encountered the narrow pigtoe in 121 of 328 (36.9%) surveys, with positive surveys in 10 and 2 subbasins in the Escambia and Yellow river basins, respectively. Six subbasins in the Escambia River historically occupied by narrow pigtoe lacked detections since 2008. We summarized these data in the CSA map (Figure 1) and in Table 2.

Table 2.

Summary of positive and negative detection surveys for the narrow pigtoe Fusconaia escambia in the Escambia and Yellow basins in Florida and Alabama before 2008 and since 2008 (1 January 2008–31 December 2018). Subbasins (i.e., HUC10s) with the most recent detections are listed first. The table indicates level of survey effort (Y = adequate, N = not adequate) given to each subbasin. The table provides year of the most recent detection of narrow pigtoe and the most recent survey year for each subbasin.

Summary of positive and negative detection surveys for the narrow pigtoe Fusconaia escambia in the Escambia and Yellow basins in Florida and Alabama before 2008 and since 2008 (1 January 2008–31 December 2018). Subbasins (i.e., HUC10s) with the most recent detections are listed first. The table indicates level of survey effort (Y = adequate, N = not adequate) given to each subbasin. The table provides year of the most recent detection of narrow pigtoe and the most recent survey year for each subbasin.
Summary of positive and negative detection surveys for the narrow pigtoe Fusconaia escambia in the Escambia and Yellow basins in Florida and Alabama before 2008 and since 2008 (1 January 2008–31 December 2018). Subbasins (i.e., HUC10s) with the most recent detections are listed first. The table indicates level of survey effort (Y = adequate, N = not adequate) given to each subbasin. The table provides year of the most recent detection of narrow pigtoe and the most recent survey year for each subbasin.

Since 2008, surveyors have detected the narrow pigtoe in three subbasins in the Escambia River in Florida and seven subbasins in Alabama (Table 2; Figure 1). We considered survey effort adequate for all 10 of these subbasins (Table 2). All six subbasins in which surveyors have not recently detected the narrow pigtoe are in the Alabama portion of the Escambia River basin and have not received adequate survey effort (Table 2; Figure 1). All 13 Escambia subbasins in which surveyors have never detected the narrow pigtoe have not been adequately surveyed (Figure 1). Based on our criteria, the narrow pigtoe has not been extirpated from any subbasins in the Escambia basin that have been surveyed since 2008. Whether this species has been extirpated from the six subbasins with no positive detections since 2008 is unclear because survey efforts have not been adequate in those subbasins (Table 2; Figure 1). Four Escambia subbasins (105-E, 305-E, 306-E, 503-E; Figure 1) lack records of narrow pigtoe but are bordered upstream and downstream by subbasins in which surveyors have detected the narrow pigtoe (mostly since 2008; Figure 1), which suggests increased survey efforts may detect this species in these subbasins.

All occurrences of narrow pigtoe in the Yellow River basin have been from the mainstem Yellow River in Florida (Figure 1). Narrow pigtoe historically occurred only in subbasins 304-Y and 308-Y and surveyors have detected it there within the past 10 y (Table 2; Figure 1). Surveyors have never detected this species in the upper portions of the Yellow River basin or in the Shoal River subbasin, although we considered survey effort to be inadequate in all six nondetection subbasins in these areas (Figure 1). The narrow pigtoe does not appear to have been extirpated from any historically occupied subbasins (Table 2; Figure 1).

Period of gravidity

In gravidity investigations, we examined 550 individuals from the Escambia River in Florida, of which 103 were gravid. The color of gravid gills ranged from bright pink-salmon to cream. Based on laboratory examination of gravid females kept for the host fish study, individuals with inflated pink gills typically contained eggs and immature glochidia, while individuals with inflated cream-colored gills typically contained fully developed glochidia. In some individuals, gills contained both immature and fully developed glochidia, and the color of those gills was a combination of pink-salmon and cream (Figure 2). Individuals with cream-colored, noninflated gills were not gravid.

Figure 2.

Photograph taken during a 2015 host-fish trial showing conglutinates of narrow pigtoe Fusconaia escambia containing pink eggs, developing glochidia, and cream-colored mature glochidia.

Figure 2.

Photograph taken during a 2015 host-fish trial showing conglutinates of narrow pigtoe Fusconaia escambia containing pink eggs, developing glochidia, and cream-colored mature glochidia.

Peak months of gravidity were May–July; we observed the greatest percentage of gravid individuals (40%) in May (Table 3). However, we observed individuals with pink, inflated gills as early as 9 March and as late as 25 October (Table 3; Table S2, Supplemental Material). High river stages prevented surveyors from verifying whether any narrow pigtoe were gravid in December and February.

Table 3.

Number of narrow pigtoe Fusconaia escambia examined for gravidity along with the number and percentage of those individuals that were gravid each month during surveys conducted 2013–2018 in the Escambia River in Florida. We did not examine mussels for gravidity in February, September, November, or December.

Number of narrow pigtoe Fusconaia escambia examined for gravidity along with the number and percentage of those individuals that were gravid each month during surveys conducted 2013–2018 in the Escambia River in Florida. We did not examine mussels for gravidity in February, September, November, or December.
Number of narrow pigtoe Fusconaia escambia examined for gravidity along with the number and percentage of those individuals that were gravid each month during surveys conducted 2013–2018 in the Escambia River in Florida. We did not examine mussels for gravidity in February, September, November, or December.

Host identification

We conducted two host-fish trials in July 2014, and four trials in July 2015 (Table 4). Each trial ran for approximately 1 mo. Glochidia concentrations in three of the six host trials met the 2,000–4,000 glochidia/L target concentration; in the other trials concentrations were only slightly less than 2,000 glochidia/L (Table 4). Mean water temperature during the trials was 23.6°C in 2014 and 24.1°C in 2015.

Table 4.

Start and end dates for narrow pigtoe Fusconaia escambia host trials in 2014 and 2015, and glochidia concentration (number of viable glochidia/L water) used in each trial. We used four narrow pigtoe for the host trials: one individual for the 2014 trials (a total of 3,524 glochidia split between two trials), one individual for trials 1 and 2 in 2015, one individual for trial 3 in 2015, and one individual for trial 4 in 2015.

Start and end dates for narrow pigtoe Fusconaia escambia host trials in 2014 and 2015, and glochidia concentration (number of viable glochidia/L water) used in each trial. We used four narrow pigtoe for the host trials: one individual for the 2014 trials (a total of 3,524 glochidia split between two trials), one individual for trials 1 and 2 in 2015, one individual for trial 3 in 2015, and one individual for trial 4 in 2015.
Start and end dates for narrow pigtoe Fusconaia escambia host trials in 2014 and 2015, and glochidia concentration (number of viable glochidia/L water) used in each trial. We used four narrow pigtoe for the host trials: one individual for the 2014 trials (a total of 3,524 glochidia split between two trials), one individual for trials 1 and 2 in 2015, one individual for trial 3 in 2015, and one individual for trial 4 in 2015.

We identified nine fish species from five genera as hosts for narrow pigtoe, and considered nine fish species from seven genera not to be hosts (Table 5). Of the fishes tested Blacktail Shiner Cyprinella venusta appeared to be the most suitable host, because it produced the greatest number of juvenile mussels (83 total), 100% of the fish tested (n = 4) produced viable juveniles, and the glochidia on these fish generally had high metamorphosis success (> 95% from three fish and 50% from the other fish; Table 5). Weed Shiner Notropis texanus appeared to be the second most suitable host. The other seven host species appeared to be less suitable hosts since they produced fewer juvenile mussels and produced juveniles less consistently (Table 5). All fish survived the host-fish trials in 2014, but both Longnose Shiner Notropis longirostris and one Ironcolor Shiner Notropis chalybaeus died during the 2015 trials (Table 5). We have provided our data sheets for the both years of host trials as supplemental material (Tables S3 and S4, Supplemental Material).

Table 5.

The number of juvenile narrow pigtoe Fusconaia escambia produced and percentage of metamorphosis (in parentheses) per fish are reported for fish species tested during two trials in 2014 (T1 2014 and T2 2014) and four trials in 2015 (T1 2015–T4 2015). Each trial tested a maximum of 10 fish species. Each species was represented by one individual (n = 1) with the exception that two Coastal Shiners Netropis petersoni were tested in Trial 4 in 2015, for which the total number of juveniles and mean percentage of metamorphosis are reported. Fish mortalities are indicated by X and a dash (—) indicates that the species was not included in the trial.

The number of juvenile narrow pigtoe Fusconaia escambia produced and percentage of metamorphosis (in parentheses) per fish are reported for fish species tested during two trials in 2014 (T1 2014 and T2 2014) and four trials in 2015 (T1 2015–T4 2015). Each trial tested a maximum of 10 fish species. Each species was represented by one individual (n = 1) with the exception that two Coastal Shiners Netropis petersoni were tested in Trial 4 in 2015, for which the total number of juveniles and mean percentage of metamorphosis are reported. Fish mortalities are indicated by X and a dash (—) indicates that the species was not included in the trial.
The number of juvenile narrow pigtoe Fusconaia escambia produced and percentage of metamorphosis (in parentheses) per fish are reported for fish species tested during two trials in 2014 (T1 2014 and T2 2014) and four trials in 2015 (T1 2015–T4 2015). Each trial tested a maximum of 10 fish species. Each species was represented by one individual (n = 1) with the exception that two Coastal Shiners Netropis petersoni were tested in Trial 4 in 2015, for which the total number of juveniles and mean percentage of metamorphosis are reported. Fish mortalities are indicated by X and a dash (—) indicates that the species was not included in the trial.

Discussion

Distribution in the Escambia River basin

The narrow pigtoe's status in the Escambia River basin in Florida appears to remain stable, as the species occupies most known historical localities. The Florida subbasins were among the most thoroughly surveyed subbasins throughout the narrow pigtoe's range; therefore, our inferences about the status of narrow pigtoe in Florida's portion of the Escambia River basin should be reliable. In contrast, the narrow pigtoe's status in the Alabama portion of the Escambia River basin is less clear. Overall, survey effort is lacking in Alabama, even for subbasins in which surveys have detected the narrow pigtoe in the past 10 y. The Alabama subbasins need more surveys where researchers have not detected narrow pigtoe to improve our understanding of the species' distribution and status in that state. Additionally, researchers need more surveys to confirm that the narrow pigtoe has not been extirpated in subbasins where surveyors have not detected it in more than 10 y. Future survey efforts should give highest priority to these subbasins. Subbasin 406-E in Alabama is of particular concern; since 2008, resurveys of five of six historical sites in this subbasin have not detected the species. Anthropogenic activity (discussed later) in and around this subbasin may be a cause of the lack of detections. Additionally, four subbasins (105-E, 305-E, 306-E, 503-E) in the Escambia River basin in Alabama lack records of narrow pigtoe and have little survey effort, but the species may occur in these subbasins because neighboring subbasins upstream and downstream have contemporary positive detections.

Distribution in the Yellow River basin

The narrow pigtoe's status in the Yellow River appears to remain stable in historically occupied subbasins. To date, all narrow pigtoe detections have been in Florida subbasins that contain the mainstem Yellow River, and surveys have never detected them in the upper subbasins of the Yellow River and Shoal River. It is unclear why researchers have not collected narrow pigtoe in those subbasins, but it may be related to swifter flow and a greater amount of unstable substrate in the upper Yellow River basins. Williams et al. (2014) noted that they found narrow pigtoe in slow to moderate flows. We have noticed during surveys in this watershed that the main river is narrow and shallow and flows more swiftly in the upper reaches, becoming wider and deeper, flowing more slowly through bottomland habitat in the lower reaches. Researchers have collected fourteen mussel species, including threatened and endangered mussels such as southern sandshell Hamiota australis, Choctaw bean Obovaria choctawensis, fuzzy pigtoe Pleurobema strodeanum, and southern kidneyshell Ptychobranchus jonesi in the upper subbasins, although in small numbers (Williams et al. 2014; McLeod et al. 2017). Water chemistry (i.e., low pH and low concentrations of nutrients and calcium) in the upper Shoal River subbasins may explain the absence of narrow pigtoe and other freshwater mussels (Williams et al. 2014). The nondetection subbasins that researchers have not consistently surveyed need additional surveys to better determine if narrow pigtoe is present in those areas of the Yellow River basin.

Period of gravidity

Many Fusconaia spp. are short-term brooders that spawn in spring and release glochidia during the same summer (Williams et al. 2008, 2014). Williams et al. (2014) considered the narrow pigtoe to be a short-term brooder and reported observations of gravid females in the Escambia River in May and June. Our study corroborates this knowledge, since we observed most gravid narrow pigtoe from May through July, with peak gravidity in May. This period of gravidity is similar to that of the gulf pigtoe Fusconaia cerina (28 May–28 July; Haag and Warren 2003) and is slightly later than that for the tapered pigtoe Fusconaia burkei (16 March–27 May and possibly into June, with peak gravidity in late March; White et al. 2008).

Host identification

Blacktail Shiner Cyprinella venusta and the Weed Shiner Notropis texanus were the two most suitable hosts for narrow pigtoe, and similar studies support these findings. Many Fusconaia spp. produce pelagic conglutinates (Haag 2012) that mimic flatworms, oligochaetes, and terrestrial insects. Almost all mussels known to produce pelagic conglutinates are host specialists on minnows that feed on insects and other food items drifting down a stream (drift-feeding minnows, generally of the genera Cyprinella and Notropis; Haag 2012). Researchers consider Cyprinella spp. to be the primary host for many related Fusconaia spp., including tapered pigtoe, gulf pigtoe, Texas pigtoe Fusconaia chunii (previously Fusconaia askewi; Williams et al. 2017), shiny pigtoe Fusconaia cor, and finerayed pigtoe Fusconaia cuneolus (Brunderman and Neves 1993; Haag and Warren 2003; White et al. 2008; Williams et al. 2008; Bertram et al. 2017). Researchers have identified Notropis spp. as important hosts for finerayed pigtoe (Brunderman and Neves 1993) and gulf pigtoe (Haag and Warren 2003) but not for tapered pigtoe (White et al. 2008).

We identified several other Notropis and Pteronotropis minnows as hosts for the narrow pigtoe in this study, although they may be marginal hosts. We considered a marginal host to be a fish species with fewer viable juveniles produced, lower metamorphosis success, and a smaller percentage of individuals that successfully transformed viable juvenile mussels compared to the most suitable host (O'Brien and Brim Box 1999; Johnson et al. 2012; Harriger et al. 2015). Although labeling a host as marginal can suggest that it is less important, having more than one host could be advantageous to the narrow pigtoe if there were interspecific competition between the two primary hosts identified in this study (Brunderman and Neves 1993; Haag 2012). Further research with the marginal hosts identified in our trials could provide a better sense of the importance of these species as hosts for the narrow pigtoe.

The Blackspotted Topminnow Fundulus olivaceus and the Brown Darter Etheostoma edwini are likely poor hosts for the narrow pigtoe because each individual produced only one juvenile mussel during each trial. The Blackspotted Topminnow is a surface feeder, which probably makes the chance of natural infestation by narrow pigtoe glochidia slim for this fish species (Haag and Warren 1997; Boschung and Mayden 2004). The habitat of the narrow pigtoe and the Brown Darter may rarely overlap, because Brown Darters are often found among vegetation in sandy runs of creeks to medium-size rivers (Boschung and Mayden 2004; Robins et al. 2018). We used only one individual each of Blackspotted Topminnow and Brown Darter in our trial; future trials involving these species should provide more information on their role as hosts to the narrow pigtoe.

Scientific literature corroborates the fish identified as the most suitable hosts in this study, but our methods slightly deviated from standard procedures and may have biased calculations of metamorphosis success and the number of juvenile mussels produced. During the host-fish infection process in 2014 and 2015 we combined multiple fish species in a bucket, whereas some studies keep fish species separate (Johnson et al. 2012) to prevent interspecific interactions from affecting glochidia attachment on the fish. If interspecific interactions between the fish cause stress, it may have biased the production of juvenile mussels in this study. Recent studies suggest that increased cortisol levels (a stress response hormone) in host fish may increase metamorphosis success and production of juvenile mussels (Dubansky et al. 2011; Douda et al. 2017; Nelson and Bringolf 2018). Additionally, we only rinsed fish after glochidia infection in 2015, which may have biased calculations of metamorphosis success in 2015, although this bias is likely minimal. Also note that our metamorphosis success may appear high because we calculated this parameter for individual fish, whereas many studies calculate the average for each fish species (Johnson et al. 2012; Johnson et al. 2016; McLeod et al. 2017).

It is unclear why trials 1 and 2 in 2015 appeared to perform poorly compared to the other trials in this study. Although it is difficult to isolate particular factors that may have caused the poor performance, mixing fish species in a bucket and rinsing fish only in 2015 probably did not affect these two trials differently than the others. Water temperature is known to affect the transformation of glochidia into juvenile mussels in laboratory experiments (Roberts and Barnhart 1999), and the mean water temperature in the aquarium system was slightly warmer in 2015 (24.1°C) compared to 2014 (23.6°C). However, it is not clear whether this small difference in temperature would have affected the 2015 results. Additionally, the dates of all four trials in 2015 overlapped, so it seems unlikely that water temperature would have impacted two trials and not the others.

Conservation Management Implications

Our study provides a better understanding of the period of gravidity and host fish requirements for narrow pigtoe, which will benefit propagation efforts. The variety of common and widespread fish species that the narrow pigtoe used as hosts in this study suggests that host-fish availability probably does not limit its populations. However, research has not well documented abundance and distribution data for each of the hosts and it is possible that reduction in host-fish abundance or diversity may impact narrow pigtoe populations. Additional fish species may be hosts for narrow pigtoe and future host-fish studies should test this. Some of these fish species include Clear Chub Hybopsis sp. cf. winchelli, Pugnose Minnow Opsopoeodus emiliae, and Longjaw Minnow Notropis amplamala.

Understanding the threats to narrow pigtoe and how researchers can mitigate them will also be important to the conservation of this species. Knowledge of threats to the narrow pigtoe in the Escambia and Yellow river basins is currently sparse; nevertheless, degraded instream habitat, water quality, and altered hydrologic regimes have the potential to negatively affect freshwater mussels in the Escambia and Yellow river basins (USFWS 2012). More specifically, streams in these basins have experienced increased siltation, sedimentation, nutrient loads, flashy flows, and water pollution (NWFWMD 1997; Cook and Moss 2009; Hinson et al. 2015). Researchers have attributed these problems to current and past land use practices, particularly row crop agriculture, timber harvest, and urban development, which have caused widespread alteration of terrestrial habitats (NWFWMD 1997). A recent study documented negative effects of freshly deposited sediments carrying excess manganese, ammonia, and organic carbon on the survival and biomass of freshwater mussels (Archambault et al. 2017). Flashy tributaries carrying and depositing pulses of contaminated sediments from agrarian areas may be harming mainstem mussel populations downstream, especially in the Escambia River basin.

Government agencies documented water quality problems caused by municipal and industrial point sources as early as the 1950s in the Escambia and Yellow river basins. Releases of industrial and untreated sewage effluent have occurred regularly (Olinger et al. 1975; FDEP 1994; NWFWMD 1997). Bouchard et al. (2009) showed that municipal effluent negatively affects survival and causes immune responses in freshwater mussels in Canada. Container Corporation, a paper mill plant near Brewton, Alabama, began discharging industrial wastewater into a tributary of the Conecuh River, Alabama, in 1957 (Olinger et al. 1975) and has been implicated as a source of dioxin contamination in Pensacola Bay, Florida (Mohrherr et al. 2009). The wastewater treatment plant for Crestview, Florida, also had a history of problems. The plant previously discharged into a tributary of the Yellow River and had numerous violations for releases of untreated sewage, including a spill in 1990 that resulted in a large fish kill (FDEP 1994).

Since the 1970s, regulatory actions have improved problems associated with point-source pollution, but the expansion of row crop agriculture and urban growth in these basins has increased nonpoint-source pollution. Agricultural runoff and urban stormwater now account for most water quality problems (FDEP 1994; NWFWMD 1997). Row crops (i.e., cotton, peanuts, corn, and soybeans) grown in the Escambia and Yellow river basins are associated with high levels of pesticides and fertilizers (Osteen and Szmedra 1989; NWFWMD 1997; Hinson et al. 2015). Despite the increase in nonpoint-source pollution, streams in the Yellow River basin have relatively good overall water quality, due to lower sediment and nutrient loads, compared to streams in adjacent basins, including the Escambia River basin (FDEP 1994; Cook et al. 2002; Cook and Moss 2009). This is likely due to larger holdings of federal (i.e., Conecuh National Forest, Eglin Air Force Base) and state-owned lands in the Yellow River watershed, which have minimal farming and urban development.

In addition to the problems previously mentioned, there are also numerous past and ongoing gravel mining operations located within the floodplains of Big Escambia Creek (503-E), Little Escambia Creek (406-E), Burnt Corn Creek (403-E), and Murder Creek (404-E) subbasins. The USFWS (2012) has associated channel instability, turbidity, and sedimentation with these mining operations. Also, two mainstem impoundments are located on the Conecuh River in Covington County, Alabama (104-E). Point A Lake and Gantt Lake dams were constructed in 1923 for hydroelectric power generation and together impound approximately 19 km of the Conecuh River. The relatively small size of the reservoirs and the operational regime of the dams support suitable narrow pigtoe habitat in some submerged areas, and reproducing populations of the narrow pigtoe occur in both reservoirs (USFWS 2012; Table S1, Supplemental Material). The dams, however, are barriers to fish movement and may prevent genetic exchange between upstream and downstream mussel populations (USFWS 2012). Further, researchers have widely implicated hydroelectric dams in downstream declines of freshwater mussels through altered hydrologic, sediment, temperature, and dissolved oxygen regimes (Haag and Williams 2014). Surveys have never detected the narrow pigtoe in subbasin105-E (the subbasin immediately downstream of the impoundments), but very little sampling has occurred there, so it is difficult to assess its presence or absence in this subbasin.

In summary, results of this study will benefit conservation efforts for the narrow pigtoe throughout its range. The narrow pigtoe's status appears to be stable in Florida, but its status in Alabama is less clear. Continued surveys to monitor the distribution and abundance of narrow pigtoe and its hosts will be important to understanding the status of this species over time. It will also be important to monitor and mitigate anthropogenic threats to ensure long-term survival of this species.

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.

Table S1. Narrow pigtoe Fusconaia escambia collection records and localities compiled from survey data, field notes, and museum specimens, 1917–2018. We compiled survey data and field notes from the Florida Fish and Wildlife Conservation Commission Freshwater Mussel Database (Gainesville, Florida) and two collections databases from the U.S. Fish and Wildlife Service.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S1 (72 KB XLSX).

Table S2. Gravidity data for narrow pigtoe Fusconaia escambia from Florida Fish and Wildlife Conservation Commission surveys in the Escambia River, Florida, 2014–2018. Information includes information about the mussels (size, sex, gravidity, gill color) and survey details (date, location, surveyors).

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S2 (76 KB XLSX).

Table S3. Results of the 2014 host-fish trials for narrow pigtoe Fusconaia escambia. The table documents the number of juvenile mussels collected throughout the course of the trials, number of fish mortalities, and the percentage of metamorphosis success for fish species that we considered to be hosts.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S3 (21 KB XLSX).

Table S4. Results of the 2015 host-fish trials for narrow pigtoe Fusconaia escambia. The table documents the number of juvenile mussels collected throughout the course of the trials, number of fish mortalities, and the percentage of metamorphosis success for fish species that we considered to be hosts.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S4 (25 KB XLSX).

Reference S1.Cook MR, Moss NE. 2009. Analyses of water quality, sedimentation, and impacts of land use on the Conecuh and Blackwater river watersheds. Tuscaloosa, Alabama: Geological Survey of Alabama. Open File Report 0805.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S5 (3.80 MB PDF); also available at https://www.gsa.state.al.us/img/Groundwater/OFR/OFR0805.pdf

Reference S2.Cook MR, O'Neil P, Moss N, DeJarnette S. 2002. Assessment of water resources in the Yellow River watershed in south-central Alabama: surface water and biological resources. Tuscaloosa, Alabama: Geological Survey of Alabama. A report to the Choctawhatchee, Pea, and Yellow Rivers Watershed Management Authority.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S6 (36.49 MB PDF).

Reference S3.[FDEP] Florida Department of Environmental Protection. 1994. Water quality assessment for the State of Florida. Technical appendix. Tallahassee, Florida: Standards and Monitoring Section. Bureau of Surface Water Management. Division of Water Facilities. 305(b) Technical Report.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S7 (706 KB PDF); also available at https://www.govinfo.gov/content/pkg/CZIC-td224-f6-h36-1994-v-1/html/CZIC-td224-f6-h36-1994-v-1.htm

Reference S4.Hinson AS, Rogers AL, Cook MR. 2015. Choctawhatchee, Pea, and Yellow rivers comprehensive watershed management plan. Tuscaloosa, Alabama: Geological Survey of Alabama. Information Series 82.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S8 (19.76 MB PDF); also available at http://cpyrwma.alabama.gov/wp-content/uploads/sites/7/2017/07/00-CPYR-WMP_webready.compressed.pdf

Reference S5.Mohrherr CJ, Liebens J, Rao KR. 2009. Screening of selected contaminants in sediments of Escambia Bay, Pensacola Florida. Pensacola, Florida: University of West Florida.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S9 (5.38 MB PDF); also available at https://pages.uwf.edu/cedb/PERCH_Escambia_Bay_final_report.pdf

Reference S6.[NWFWMD] Northwest Florida Water Management District. 1997. Pensacola Bay system: surface water improvement and management plan update. Havana, Florida: Northwest Florida Water Management District. Program Development Series 97-2.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S10 (2.00 MB PDF); also available at https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&ved=2ahUKEwi94tKauaPkAhUtVt8KHQ8SBmIQFjAAegQIABAC&url=https%3A%2F%2Fwww.nwfwater.com%2Fcontent%2Fdownload%2F6344%2F45041%2FPensacola_SWIM_Plan_Update_1997.pdf&usg=AOvVaw3scM0LVnzz4W8UFMLWRYcR

Reference S7.Olinger LW, Rogers RG, Fore PL, Todd RL, Mullins BL, Bisterfeld FT, Wise LA. 1975. Environmental and recovery studies of Escambia Bay and the Pensacola Bay system, Florida. Atlanta, Georgia: EPA Report 904/9-76-016.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S11 (22.83 MB PDF); also available at https://nepis.epa.gov/Exe/ZyPDF.cgi/9101CISS.PDF?Dockey=9101CISS.PDF

Reference S8. Osteen CD, Szmedra PI. 1989. Agricultural pesticide use trends and policy issues. Washington, D.C.: Resources and Technology Division, Economic Research Service, U.S. Department Of Agriculture. Agricultural Economic Report No 622.

Found at DOI: https://doi.org/10.3996/092019-JFWM-074.S12 (4.76 MB PDF); also available at https://naldc.nal.usda.gov/download/CAT10407750/PDF

Acknowledgments

Amanda Mattair, Matt Wegener, Neil Branson, Matt Rowe, Cayla Morningstar, Sahale Casebolt, Susan Geda, Sarah Sharkey, and Jim Williams assisted with collecting mussels. Amanda Mattair's assistance with host-fish trials is greatly appreciated. Thanks to the Utah Division of Wildlife Resources for supporting the completion of this manuscript. We also thank Florida Fish and Wildlife Conservation Commission biologists and editors, two anonymous reviewers, and the Associate Editors for providing comments and edits that improved this manuscript.

Any use of trade, product, website, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Author notes

Citation: Holcomb KM, Holcomb JM, Pursifull SC, Knight JR. 2020. Distribution, period of gravidity, and host identification for the narrow pigtoe mussel. Journal of Fish and Wildlife Management 11(2):410–421; e1944-687X. https://doi.org/10.3996/092019-JFWM-074

Competing Interests

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.