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Modern occurrence of and size data for Quadrula aurea (Mollusca: Unionidae) from the Medina River of Texas.

North America's freshwater mussels of the family Unionidae are extremely diverse, with approximately 300 species found throughout its waters (Williams et al., 1993; Haag, 2012). They are often the dominant filter-feeders in an aquatic environment, and perform important ecological functions including biodeposition, nutrient cycling, and serving as refuges, habitat, and food for various other organisms (Vaughn and Hakenkamp, 2001; Vaughn et al., 2004; Howard and Cuffey, 2006; Allen and Vaughn, 2011). However, because of their complex life histories typically involving an aquatic host species for reproduction and dispersal, the blockage and elimination of their host organisms, the destruction of aquatic habitats, the impoundment and alteration of waterways, the release of environmental toxins, and the introduction of invasive species, unionid populations have been and are continuing to decline throughout much of North America (Lydeard et al., 2004; Strayer et al., 2004; Bogan, 2008; Grabarkiewicz and Davis, 2008; Brown et al., 2010). Currently it is estimated that more than 70% of North America's unionid species are imperiled to some degree (Williams et al., 1993; Ricciardi and Rasmussen, 1999; Lydeard et al., 2004; Strayer et al., 2004).

In Texas, many of the approximately 50 described mussel species have declined in both range and abundance, with numerous locations now unable to support historical mussel populations (Neck, 1984; Howells et al., 1996; Howells, 2010). As a consequence the United States Fish and Wildlife Service (USFWS) currently has one species listed federally as "Endangered", and an additional 15 species are currently listed as Threatened" at the state level by the Texas Parks and Wildlife Department (2010). Of these 15 state-listed threatened species, six have been petitioned for federal protections and are considered Candidate" species by the USFWS (United States Fish and Wildlife Service, 2009, 2011). These six candidate species consist of several endemic and rare Texas species, including the golden orb, Quadrula aurea (United States Fish and Wildlife Service, 2009, 2011).

Quadrula aurea is a freshwater mussel (Mollusca: Unionidae) species endemic to the waters of central Texas with a subrectangular to broadly elliptical or oblong, moderately thick shell (Howells et al., 1996; Howells, 2014). The species attains lengths of up to approximately 80 mm, but individuals are typically smaller. The species is usually moderately compressed and solid, and is often less inflated than other Quadrula species (Howells, 2010, 2014). Internal coloration is typically white, and external colors can range from yellow, brown, gold, or orange-brown, to dark brown or black (Howells, 2014). Quadrula aurea populations are located almost exclusively in flowing waters in moderate-sized streams and rivers, with the exception of a population located within Lake Corpus Christi (Howells, 2010). Typically Q. aurea habitat consists of firm mud, sand, gravel or mixtures of these substrates at depths ranging from 15 cm-3 m. Currently there is little life history information available for Q. aurea, including host data; however, preliminary data indicate that Q. aurea likely utilizes ictaluridae species (Howells, 2014; Ford and Oliver, 2015), and host studies are currently ongoing.

Historically the range of Q. aurea included the Guadalupe, Nueces, Frio, and San Antonio River Basins of central Texas (Strecker, 1931; Howells et al., 1996; Howells, 2006, 2010, 2014). However, Q. aurea populations have been declining throughout the state and its range has become highly restricted, with only a few known populations remaining (Howells, 2006, 2010; Howells, 2014). Several areas throughout its historic range have not been surveyed within the last few decades, and in many locations it's unknown if populations of Q. aurea still survive. Modern records, from 1990 and onward, for Q. aurea include Cibolo Creek, and the Guadalupe (Howells, 2006, 2010), San Marcos (Howells, 2006; Burlakova and Karatayev, in litt.; and retrieved in 2016 from the Texas Natural Diversity Database, wildlife_diversity/txndd/), Nueces (Burlakova and Karatayev, 2012), and Frio Rivers (Burlakova and Karatayev, 2012). In addition, a population is surviving within Lake Corpus Christi (Howells, 2010), which is the only known impoundment with a population of Q. aurea.

Though Q. aurea is historically known from the San Antonio River Basin (Strecker, 1931; Howells et al., 1996; Howells, 2010, 2014), few records of this species exist within the basin prior to the early 2000s and late 1990s (Global Biodiversity Information Facility, Non-Vertebrate Paleontology, especially within the upper portions of the basin (Fig. 1). Neck (1989) conducted a survey within Medina Lake (Fig. 1), a reservoir within the San Antonio River Basin, along with some portions of the upper Medina River, and recovered three unionid species; however, he did not locate Q. aurea. Neck (1989) indicated that because the upper San Antonio River Basin tended to have a rocky substrate, there was likely not a robust mussel population within the upper portions of the basin.

More recently, portions of the basin have been surveyed by various individuals and organizations such as the San Antonio River Authority as part of their ongoing monitoring efforts, and live Q. aurea have been recovered from several locations along the main stem of the lower San Antonio River, and from various locations within Cibolo Creek (Burlakova et al., 2011; Burlakova and Karatayev, in litt.; retrieved in 2016 from the Texas Natural Diversity Database, huntwild/wild/wildlife_diversity/txndd/). However, these surveys have primarily occurred within portions of the lower and middle San Antonio River and Cibolo Creek, and did not include the Medina River (Fig. 1). To our knowledge there are currently no published modern (since 1990) records for Q. aurea for the upper San Antonio River Basin (though additional surveys are likely currently ongoing) and data remain lacking for many of the smaller tributaries and rivers of the upper San Antonio River Basin, including the Medina River. Here we present data from a unionid and fish survey conducted within the Medina River prior to its confluence with the San Antonio River.

MATERIALS AND METHODS--We conducted a mussel survey in 2014 within the Medina River of the San Antonio River Basin, in Bexar County, Texas, approximately 7 km south of the city of San Antonio. The Medina River is an approximately 187 km-long spring-fed river, which begins in Bandera County and flows southeast until it joins the San Antonio River downstream from Braunig Lake (Texas Parks and Wildlife Department, 1974; Fig. 1). Depth in this portion of the river during the survey ranged from less than 0.1 m to approximately 1 m. The adjacent land usage consisted of forested scrubland with moderately steep banks, and periodic flood events. Substrate within this portion of the river consisted of mixtures of cobble, gravel, clay, silt, sand, and organic debris.

The study area was chosen based upon a soon-to-be completed stream crossing which will include columns within the river. Due to impacts to the river bottom and potentially any unionid populations within this portion of the river, we surveyed the impact areas within the river. The study area consisted of two 100 m river sections extending both upstream and downstream from the location of the planned bridge crossing (29.259[degrees]N, 98.514[degrees]W; Fig. 1).

Mussels were surveyed via one m by one m ([1m.sup.2]). quadrats within the entire 200 m reach, extending across the entire width of the river for the length of the survey area. Mussels were collected from each quadrat, using timed tactile and visual searches to locate mussels on the surface, and extending approximately 8 cm into the substrate. This method is known to provide the most comprehensive and accurate results for mussel species richness and evenness and is considered effective at locating rare species (Hornbach and Deneka, 1996; Vaughn et al., 1997).

After all live and dead mussels were collected from the quadrat, the quadrat was flipped and the next area was surveyed. This formed a uniform grid throughout the entire reach, with quadrats extending one after another across the width of the stream and 100 m both upstream and downstream from the crossing. As a result, approximately 405 [m.sup.2] of the streambed were surveyed. The full complement of habitat types within the reach were surveyed, including completely dry areas, which might periodically be flooded, though only a visual survey was conducted of these locations, since they would only be functional mussel habitat during and shortly after flood events.

All live and dead mussels were collected per quadrat and identified following Howells et al. (1996) and Howells (2010, 2014). Individuals were counted to determine both the richness (the number of species), and abundances (the number of individuals of each species) within the reach. in addition, the richness and abundances within each individual quadrat were recorded to determine the densities per species per quadrat. All live individuals were returned to the river downstream of the project area to ensure that mussels were not sampled again, and could not potentially be washed back into the project area. Some dead individuals were retained as voucher specimens and were added to the Halff Associates, inc. mussel collection. All other dead individuals were returned to the river outside of the project area to avoid resampling. Length, height, and width data were recorded to the nearest millimeter via calipers for all live mussels, and no size data were taken on dead Q. aurea. Fish were collected from the area via electroshock methods utilizing an LR-24 backpack electrofisher made by Smith-Root, Vancouver, Washington. Live fish were collected, recorded and returned to the river outside of the project area. Dead fish were not recovered.

RESULTS/DISCUSSION--We recorded a total of 150 live and 66 dead mussels of six species during our survey within this reach of the Medina River. This included 124 live Q. aurea, which was the only species with more than 15 live individuals collected, and made up more than 80% of the total mussels collected (Table 1). other mussel species collected during the survey included Amblema plicata, Cyrtonaias tampicoensis, Lampsilis teres, Quadrula apiculata, and Quadrula verrucosa. Three species--A. plicata, C. tampicoensis, and Q. apiculata--were collected only as long-dead/subfossil shells (Table 1). interestingly, all L. teres and Q. verrucosa were small individuals <12 cm in length. Mussels were recovered from water depths ranging from 0.1 m to 0.9 m, though these depths likely change substantially during high flow events, and the survey occurred during a low flow period. Lengths of Q. aurea ranged from 10 to 40 mm (Fig. 2) with a mean length of 27 mm (Table 2), though researchers have found adults in other locations in Texas can reach lengths up to 80 mm (Howells, 2010). Several size classes of Q. aurea were recovered during the survey, including several small individuals which would seem to indicate that Q. aurea is reproducing and recruiting here.

Determination of recruitment in mussel populations is typically done via several different methods, with either the age or the size of the individual usually utilized to determine a juvenile individual. When age is used, the mussel's annual growth rings (annuli) are counted, and a juvenile mussel is considered to be a specimen of 3-4 years of age or less (Neves and Widlak, 1987; Balfour and Smock, 1995; Haag and Commens-Carson, 2008). However, some studies have utilized size criteria to define a recent recruit instead of age and annuli. For example, Margaritifera margaritifera populations undergoing recruitment are considered to be those with individuals 50 mm or less in length (Hastie et al., 2000; Arvidsson et al., 2012). Within the Mississippi River, mussel size has been utilized to evaluate recent recruitment for numerous mussel species recovered from various mussel beds, and individuals 30 mm or less in length are considered to be juveniles (Whitney et al., 1996). Though size classification would be dependent upon the adult length of the species, when size is utilized to evaluate evidence of recent recruitment, mussels 30 mm or less are typically considered juveniles (Whitney et al., 1996; Nichols et al., 2001; Haag and Warren, 2007; Ford et al., 2009).

Though currently there are no data available on the exact age or size at maturity for Q. aurea (Howells, 2010), we collected a number of small specimens during our survey, including 34 Q. aurea that were 25 mm or less in length, an additional 61 individuals with lengths between 26-30 mm, and 29 with lengths greater than 30 mm. Since Q. aurea is typically a small species, and the majority of individuals were between 26-30 mm in length, the authors' considered those individuals 25 mm or less to be juveniles, though this is less than the typical length utilized to determine a juvenile mussel in other species (Whitney et al., 1997; Nichols et al., 2001; Haag and Warren, 2007; Ford et al., 2009). These young individuals constituted approximately 27% of the total Q. aurea recovered from the survey, and would indicate that recruitment of this species appears to be occurring here. Older individuals often dominate many mussel populations and evidence of recent recruitment is especially rare in uncommon and/or endangered species such as Q. aurea (Warren and Haag, 2005; Haag and Warren, 2007). Given the rarity of Q. aurea throughout Texas, and its potential listing by the USFWS (United States Fish and Wildlife Service 2009, 2011) this could be an important population of Q. aurea worth preserving given that it contains a reproducing population.

Densities of Q. aurea were relatively low throughout the study area, and Q. aurea were recovered from only 96 of the 405 quadrats. The majority of individuals, 74, were found individually within a single quadrat each. Of the remaining quadrats, 16 had two Q. aurea within them, 6 quadrats had three Q. aurea, and 309 quadrats had no Q. aurea. No quadrats had Q. aurea in densities greater than three individuals. Substrate throughout the survey area consisted of cobble (26.06%), gravel (26.05%), clay (26.26%), silt (16.58%), sand (1.56%), and organic debris (3.41%). Q uadrula aurea were recovered across the study area, and from all substrate types, though most rarely from the clay substrate. Our habitat information corroborates known habitat preferences for this species by Howells (2002), which indicated that Q. aurea is typically found in sand, gravel, or mixtures of these substrates within flowing waters. Substrate at the site followed this trend, and consisted primarily of gravel with sand and other substrates underneath with a low but constant flow. The substrate data recovered in this survey represent a broad range of substrate types utilized by Q. aurea, and additional information and research is necessary to quantify the environmental niche of the species as a habitat generalist or specialist. The authors recommend in future surveys and studies of Q. aurea that researchers focus on the exact habitat variables in which Q. aurea are located to determine the precise habitat requirements of the species.

A total of 257 live fish of 17 species were recovered from the survey area. This included six species of Centrarchidae, one species of Cichlidae, four species of Cyprinidae, three species of Ictaluridae, one species of Percidae, and two species of Poeciliidae (Table 1). However, fish were obtained only via electroshocking methods during a single collection event and no other methodology were utilized, and it is highly likely that additional fish species reside within this portion of the Medina River. The glochidia (larvae) of freshwater mussels are obligate parasites on the gills or fins of fish, and identification of natural host species is critical to successful conservation of freshwater mussels, especially for threatened and endangered species such as Q. aurea (Burlakova et al., 2011; Daniel and Brown, 2012; Johnson et al., 2012; Levine et al., 2012). Though additional fish species can occur and/or migrate through the study area (Hendrickson and Cohen, 2012) at various times of the year, we did not conduct host trials or investigate recovered fish for glochidia. It is possible that one of these fish species is a viable host for Q. aurea given the ongoing recruitment, and the presence of these fish species within this habitat removes one of the physiological barriers that prevent some potential species from serving as natural hosts (i.e., the fish species are present where reproducing mussel species are present; Rauque et al., 2003; Koehler and Poulin, 2010; Levine et al., 2012). However, these fish species should not be considered valid hosts for Q. aurea without additional laboratory and field trials, and should only be viewed as potential options for future host species testing.

Our findings represent the first modern record of a reproducing population of Q. aurea from the Medina River, and this record is approximately 18 km upstream from the nearest location were Q. aurea had previously been recovered within the basin (Fig. 1). Currently few locations within Texas support populations of Q. aurea (Howells, 2010), and no modern populations were known to occur within the Medina River prior to our survey. The closest recent record of Q. aurea is within the mainstem of the San Antonio River (Fig. 1; Howells, 2010; Burlakova et al., 2011; Burlakova and Karatayev, in litt.; retrieved in 2016 from the Texas Natural Diversity Database, https:// Our finding is significant because Q. aurea is currently under review for federal protections under the Endangered Species Act (United States Fish and Wildlife Service, 2009, 2011), and it indicates that Q. aurea populations could be surviving within other small streams and rivers within its range that have yet to be investigated. Critical steps in species protection are the identification of areas with viable and reproducing populations of threatened species and protection of known breeding populations of those species. Here we have identified a reproducing population of Q. aurea, which potentially warrants additional protections. The authors advise more extensive studies of the upper reaches of the San Antonio River Basin (Leon Creek, Medina River, Salado Creek, etc.) be undertaken to determine the exact distribution and viability of any surviving Q. aurea populations within the basin, which could potentially impact a USFWS listing decision.

Submitted 1 April 2016. Accepted 15 February 2017.

Associate Editor was Frederic Robert Govedich.

The authors would like to thank Bio-West, the City of San Antonio, Capital Construction Division, Aecom, A. Garcia, B. Boe, and Dr. N. B. Ford for supporting various aspects of this research.


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* Correspondent:

Caption: FIG. 1--Locations where Quadrula aurea has been recovered from the San Antonio River Basin of Texas (expansion of shaded area on inset of Texas). Circles represent modern records from the 1990s and onward, the triangles represent pre-1990 records, and the square represents the survey effort conducted in 2014 during this project.
TABLE 1--The mussel and fish species recovered during the 2014 survey
within the Medina River in the San Antonio River Basin of Texas,
and the relative abundances of the mussel and fish species.
Only live individuals were utilized to calculate
the relative abundances.

Family                   Species            n Live   n Dead   Total

Unionidae       Amblema plicata               0        14      14
                Cyrtonaias tampicoensis       0        6        6
                Lampsilis teres               14       8       22
                Quadrula apiculata            0        7        7
                Quadrula aurea               124       28      152
                Quadrula verrucosa            12       3       15
                Total                        150       66      216
Centrarchidae   Lepomis cyanellus             1      -- (a)     1
                Lepomis gulosus               1        --       1
                Lepomis macrochirus           4        --       4
                Lepomis megalotis             78       --      78
                Micropterus salmoides         1        --       1
                Micropterus punctulatus       2        --       2
Cichlidae       Cichlasoma cyanoguttatum      10       --      10
Cyprinidae      Cyprinella lutrensis          19       --      19
                Cyprinella venusta            35       --      35
                Notropis volucellus           18       --      18
                Pimephales vigilax            42       --      42
Ictaluridae     Ameiurus natalis              1        --       1
                Ictalurus punctatus           11       --      11
                Noturus gyrinus               2        --       2
Percidae        Percina carbonaria            5        --       5
Poeciliidae     Gambusia affinis              21       --      21
                Poecilia latipinna            6        --       6
Total                                        257       --      257

Family          Relative
Unionidae          --
Centrarchidae      0.4
Cichlidae          3.9
Cyprinidae         7.4
Ictaluridae        0.4
Percidae           1.9
Poeciliidae        8.2
Total             100.0

(a) Dash indicates not recovered or not used in the calculations.

TABLE 2--The mean, standard deviation and range of the length,
height, and width recorded for the Quadrula aurea recovered
during a 2014 survey in the Medina River in the
San Antonio River Basin of Texas.

        Length   Height   Width
         (mm)     (mm)    (mm)

Mean     27.0     19.7     7.3
SD       5.9      4.9      2.8
Range   10-40     6-31    1-15

FIG. 2--Lengths of the 124 live Quadrula aurea collected and
measured during the authors' 2014 survey within the upper
Medina River in the San Antonio River Basin of Texas.

Length (mm)   Number of Mussels

10-15                 7
15-20                 7
21-25                20
26-30                61
31-35                25
36-40                 4

Note: Table made from bar graph.
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Date:Mar 1, 2017
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