Surveys Population Structure and Habitat Use of the Endangered Watercress Darter

R. Scot Duncan,* Bernard R. Kuhajda, Caitlin A. Hodges, Ashley L. Messenger

R.S. Duncan Birmingham-Southern College, 900 Arkadelphia Road, Birmingham, Alabama 35254

B.R. Kuhajda Tennessee Aquarium Conservation Institute, 1 Broad Street, Chattanooga, Tennessee 37402 Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021

C.A. Hodges, A.L. Messenger Birmingham-Southern College, 900 Arkadelphia Road, Birmingham, Alabama 35254

Abstract Despite Alabama’s exceptionally diverse freshwater fish fauna, many of its fish species face extinction. Some of the state’s most imperiled species dwell within coldwater springs, but a deficit of knowledge about their ecology hampers protection efforts. The watercress darter Etheostoma nuchale is a species confined to five springs in the greater Birmingham metropolitan area. Roebuck Spring likely harbors the largest population. Its pool has been surveyed occasionally, but there had been no survey of its run, a shallow stream flowing from the pool. We investigated the darter’s use of the run, its habitat preferences, and characteristics of the habitats where it is most abundant. We quantified the abundance of stream microhabitats, then estimated darter density in the stream’s five most common habitats using a throw trap, a high-walled metal frame dropped in the habitat. We found darters at densities vastly exceeding typical estimates derived using seine nets. We estimated the run harbored 116,932 (79,358–155,965) darters, two-thirds of which were juveniles. The most preferred habitat was coontail Ceratophyllum demersum, a submergent plant not previously known to provide darter habitat. Coontail grew prolifically in swift currents, which was surprising given that darter habitats described previously had little to no current. Coontail provided a more structurally complex habitat than the plants of the other microhabitats studied. Our results suggest that spring runs can support substantial densities of the watercress darter if dense submergent vegetation is present.

Keywords: habitat preference; geomorphology; Etheostoma nuchale; coldwater spring; Alabama Received: July 15, 2015; Accepted: July 13, 2016; Published Online Early: July 2016; Published: December 2016 Citation: Duncan RS, Kuhajda BR, Hodges CA, Messenger AL. 2016. Population structure and habitat use of the endangered watercress darter. Journal of Fish and Wildlife Management 7(2):499–508; e1944-687X. doi: 10.3996/ 072015-JFWM-062 Copyright: All material appearing in the Journal of Fish and Wildlife Management is in the public domain and may be reproduced or copied without permission unless specifically noted with the copyright symbol &. Citation of the source, as given above, is requested. The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service. * Corresponding author: [email protected]

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Initial surveys consistently found watercress darters associated with dense aquatic vegetation in deeper portions of spring pools and their run, which we define as the stream connecting a spring to the nearest tributary (USFWS 1992; Boschung and Mayden 2004; Stiles 2004). The darter has also been found in shallow- water, vegetated habitats with a moderate current (Duncan et al. 2010). The preference for vegetation seems related in part to its diet, which is believed to consist of small snails, aquatic insects, and crustaceans that abound within submerged vegetation (Howell and Caldwell 1965). Aquatic plants also provide shelter from predators and a substrate on which female darters lay eggs during the reproductive season, which peaks in March–July (Stiles 2004) but can occur year-round (Fluker Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 et al. 2009b). Darters are thought to survive no more than 3 y based on discernible size classes present in most seasons across all five populations (Fluker et al. 2009b). Relatively little else is known about the darter’s ecology, yet more detailed knowledge of its life history could inform protection and recovery efforts. The watercress darter population at Roebuck Spring is believed to be the largest population (Fluker et al. 2008, 2009b; Duncan and Kuhajda 2012); is genetically distinct from all other natural populations (Fluker et al. 2010); and is the most accessible for study because of the spring’s public ownership (City of Birmingham and State of Alabama), shallow waters, and relatively stable hydrology. The other springs are difficult to sample Figure 1. Examples of male watercress darters Etheostoma because of their depth, dense aquatic vegetation, and silt nuchale, a species endemic to a handful of coldwater springs in the Birmingham metropolitan area, Alabama. accumulation (Thomas); private ownership (Glenn); or the presence of North American beavers Castor cana- densis and the frequent hydrologic changes they create Introduction (Seven and Tapawingo). Roebuck Spring has also been the subject of legal action by the U.S. Fish and Wildlife Alabama has more fish species than any other state Service against the City of Birmingham on account of (Stein 2002), and is host to 20 endemic species two dewatering events in recent years, one in the spring (Boschung and Mayden 2004; Baker et al. 2013). pool in 2008 (Fluker et al. 2009a) and another in the However, 124 Alabama fish species are considered uppermost portion of the spring run in 2013 (G. imperiled (Boschung and Mayden 2004), 16 are listed as Thornton, U.S. Department of the Interior, personal endangered or threatened under the U.S. Endangered communication). Species Act (ESA 1973, as amended; USFWS 2014), and 2 Given the importance of Roebuck Spring to the are extinct. Many of the state’s most rare and endan- survival of the species and the spring’s accessibility, we gered fishes are endemics associated with coldwater undertook a study to better understand the population springs, habitats that have often been highly altered demographics and habitat use by the watercress darter. through hydrological alteration and water extraction Although most previous work had sampled Roebuck (Fluker et al. 2010). One of these coldwater spring Spring pool (Fluker et al. 2008, 2009a, 2009b), the spring endemics is the watercress darter, Etheostoma nuchale, a run was suspected to support a large darter population small and colorful member of the clade Astatichthys because of its length, diversity of habitat, abundance of aquatic vegetation, and relatively good water quality. within the subgenus Oligocephalus, which was not Thus, we examined three main questions about the discovered until 1964 (Figure 1; Howell and Caldwell spring run: 1) To what extent, if any, does the watercress 1965; Near et al. 2011). The species is restricted to four darter inhabit the run? 2) What habitats do the darters springs (Roebuck, Glenn, Seven, Thomas) within the most prefer in the run? and 3) What characterizes the greater Birmingham metropolitan area of Jefferson most preferred habitats? Answers to these questions will County, AL (Figure 2). A fifth population was established help in determining the importance of the run to the at Tapawingo Spring in 1988 as an ark population overall population at Roebuck Spring, and will guide outside its natural range (USFWS 2009). Some of these conservation efforts on effective habitat restoration and populations are believed to be stable, while others are in creation throughout the darter’s range. decline or their status is unknown (Fluker et al. 2008, A secondary focus of our study was the use of a throw 2009b; Duncan and Kuhajda 2012). trap, which was a novel sampling methodology for this

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Figure 2. Distribution of the endangered watercress darter Etheostoma nuchale, which is restricted to Jefferson County, Alabama, in the Black Warrior River drainage. All five populations are within the Birmingham Metropolitan Area. Populations include 1) Glenn Spring, 2) Thomas Spring, 3) Seven Springs, 4) Roebuck Spring, site of this 2011 study, and 5) Tapawingo Spring (introduced population). species. Our previous experience suggested that seine measures roughly 150 m long and 50 m wide and is nets were very poor at catching watercress darters, impounded by a small dam. The first 54 m of the 807-m which led to inaccurate estimates of darter density in run are piped belowground under tennis courts. The run these heavily vegetated spring habitats. The most vexing flows freely for 63 m, and is then piped for another 64 m problem was that seine nets were difficult to pull under a drive. Immediately adjacent to this section of the through dense aquatic vegetation, and the net bottom run is a parking lot for Birmingham’s Don A. Hawkins lifted off the substrate, which gave darters ample Recreation Center. After the parking area, the run flows opportunity to escape. To sample darters in this study, through a public golf course before joining Village Creek, we dropped a 1 3 1 m metal throw trap with tall sides on a tributary to the Locust Fork of the Black Warrior River a distinct spring habitat, and then sampled the interior of drainage. The floodplain of the run is presently in an the trap until no more darters were captured. We will early phase of secondary succession that began in 2009 present a summarized quantitative analysis of the and now serves as a buffer between the golf course and effectiveness of this technique in a different paper. spring run. Two low top-flowing dams are located along the run; these are the result of channel modifications Methods during the past century.

Study site Habitat surveys 0 0 Roebuck Spring (33835.089 N, 86842.583 W) is located We surveyed the habitats and their abundance within within the Ridge and Valley ecoregion, which is defined the spring run in March–April 2011 using 17 belt by elongated mountains and intervening valleys (Griffith transects placed across the run at 40-m intervals. We et al. 2001). The spring is located in Jones Valley, whose measured stream width (between the wetted margins) carbonate rocks are punctured by numerous springs and thalweg depth along each transect. We divided the (Osborne et al. 1989; Duncan 2013). The spring is within area within each 1-m-wide transect into 0.25-m2 square the eastern part of the City of Birmingham, and is blocks. We classified the habitat for each block based on surrounded by busy city streets, large shopping centers, the dominant vegetation type or substrate cover. Most and an interstate. A portion of the spring pool is owned aquatic plants in the spring run grow in single-species by the State of Alabama as part of a juvenile detention patches, which made habitat classification relatively facility. The remainder of the pool and the entire spring simple. run are owned by the City of Birmingham and managed We measured the biomass of common vegetated by the Parks and Recreation Board. The spring pool habitats as an estimate of habitat quality for darters.

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Biomass may correspond to availability of foraging opportunities, egg-laying surfaces, and shelter from predators. However, it may not accurately reflect these and other measures of habitat quality, such as complex- ity. For any aquatic plant habitats that were 5% of all sample blocks, we took biomass samples within a 25 3 25 cm quadrat. We randomly chose 10 quadrats/species for sampling. We collected submergent vegetation in each quadrat and discarded emergent vegetation. We did not measure depth, so we scaled biomass measure- ments only to surface area. We removed debris and large macroinvertebrates from samples, but it was impractical to remove minute invertebrates and epiphytic algae. We allowed samples to drip dry, then weighed them (wet Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 weight). We measured dry weights after complete drying Figure 3. Aluminum-frame throw trap used to sample in an oven at 508C. Water can be a large proportion of watercress darters Etheostoma nuchale in the dense aquatic tissue mass in aquatic plants; therefore, wet weights may vegetation of a coldwater spring during May–June 2011 in better represent in situ habitat relative to dry weights, Birmingham, Alabama. but dry weights do not include the water film adherent to stems when wet weight is measured. We compared We captured darters by dropping a heavy-gauge, wet weights among species with an Analysis of Variance aluminum-frame throw trap (Kushlan 1981; Jordan et al. and conducted post hoc analyses using Tukey’s Honestly 1997) with solid siding on each sample locations (Figure Significant Difference test; we set alpha level at 0.05 for 3). The frame measured 1 m on each side and was 0.77 m all analyses tall. Immediately after we dropped the frame, we forced it into the sediment to prevent darters from escaping. Watercress darter survey We surrounded each sample location with a buffer of During May–June 2011, we conducted surveys of 0.5 m of the target habitat to help ensure that the watercress darters in the five most abundant habitats as sample was representative of that habitat. We extracted indicated by the habitat survey. This coincided with the darters using a seine net and dip nets as part of the breeding season so that we might understand how all separate comparative study of sampling methods. First, age classes of darters use these habitats. Cumulatively, we pulled through the frame a shortened 10 3 4 ft (3.05 these five major habitats accounted for 70% of the 3 1.22 m) seine, green dipped with 1/8-in (0.32-cm) Delta surveyed blocks and included watercress Nasturtium mesh (Memphis Net & Twine Co., Inc., Memphis, TN). This officinale, coontail Ceratophyllum demersum, silt, Ameri- involved three people—one for each brail and a third to can bur-reed Sparganium americanum, and alligator manually pull the lead-line along the substrate and weed Alternanthera philoxeroides. Both watercress and through the dense vegetation. We completed a single alligator weed are nonnative invasive species known to seine pass for each frame. Second, three workers then disrupt aquatic ecosystems (Spencer and Coulson 1976; sampled the contents of the frame using two dip nets Benson et al. 2004). As a result of concerns about habitat measuring 15 in (38 cm) wide and 11–15 in (28–38 cm) damage from repeated sampling in this relatively small, long, and having a mesh size of 1/16 in (1.6 mm). Three but potentially important, portion of the darter’s range, overlapping sweeps of the dip nets completed a single we conducted fish sampling only during this single ‘‘pass’’ through the frame. A pass began with two nets season. pushed simultaneously and unidirectionally along oppo- We distributed eight random samples of each of the site sides of the frame. One net would then be swept in five habitats across nine stream segments to provide the opposite direction through the center of the frame spatial representation. Segments averaged 74 m in to complete the pass. Nets were swept only across the length (range ¼ 31–127 m) and adjacent segments substrate because darters lack a swim bladder and usually differed in their average width, current speed, naturally rest along the bottom. Dip net contents were depth, and prevalent aquatic vegetation. We chose usually laden with organisms and silt, and the latter was sample locations within the segments at random from flushed out by gently shaking the net with its contents in patches of the appropriate habitats. We sampled each the stream’s current while keeping the frame of the net habitat type in eight locations maximally spread across above the surface. We continued passes through the segments. Not all habitats were present in each segment, frame until at least three passes were completed without so a uniform distribution of sampling locations was not catching a darter as detected during visual examination possible. Chosen sampling locations usually consisted of the flushed (rinsed) contents of the dip nets. entirely of the target habitat; however, in two cases we We immediately placed captured darters in a 5-gallon found another type of vegetation to be present during bucket with clear spring water, while we placed sampling, which totaled ,10% of the sampled area. vegetation and debris in large coolers with clear spring

Journal of Fish and Wildlife Management | www.fwspubs.org December 2016 | Volume 7 | Issue 2 | 502 Population Structure and Habitat Use of the Watercress Darter R.S. Duncan et al. water. We then brought buckets and coolers to shore for density in the silt habitat was very low, and other processing. We carefully examined vegetation for darters nonvegetated minor habitats in the spring run (e.g., by shaking small clumps over a water-filled bucket and woody debris, rocks) provide more cover than silt and then by floating handfuls of vegetation in a white likely have greater densities of darters. For instance, enameled pan to facilitate the visual detection of small Duncan et al. (2010) found that watercress darter darters. We found it useful to sort through the floated densities were the second highest in detritus (woody material with white plastic spoons, which we also used debris) among eight habitats sampled at Seven Springs. to gently scoop up darters. We passed remnant water in Finally, we summed these three estimates of darter the cooler and buckets through a fine-mesh aquarium numbers in the spring run (all major microhabitats, net to capture remaining darters. We positively identified vegetated minor microhabitats, and nonvegetated minor all watercress darters captured and recorded their length microhabitats) to yield the final estimate of the (mm, standard length), sex (if adults), and size categories watercress darter population size in the spring run (juvenile, 9-23 mm SL; medium, 24-31 mm SL; or large during May–June 2011. We determined confidence adult, 32–45 mm SL). Some samples with an abundance intervals of 95% by employing a parametric bootstrap Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 of vegetation required .1 h to process, with a team of (10,000 iterations) for our area-stratified abundance 4–6 workers. During processing we regularly replaced estimates, performed in R statistical language (version water in coolers and buckets with new clean spring 3.2.0; R Core Team 2015). water from the spring run to minimize risk to captured organisms. Results

Estimated watercress darter population size in the Habitat surveys run The width of the run averaged 10.5 m (SD ¼ 3.1) and We used the data from the habitat and watercress ranged from 7.3 to 19.2 m, while maximal depth darter survey to provide a simple estimate of the averaged 40.3 cm (SD ¼ 23.3) and ranged from 11.8 to population size of the darter in Roebuck Spring’s run. 95.0 cm. Across all transects, we surveyed 684 0.25-m2 In short, we multiplied the estimated density of darters blocks (Table S1, Supplemental Material). Twelve of the for habitats by an estimate of area occupied by each of 17 habitat categories were dominated by plants, and these habitats in the run, and then summed the values. these categories comprised 74.7% of the surveyed area. We used average stream width from the habitat surveys The five most abundant habitats (hereafter, major to represent stream width in our calculations. We habitats) were watercress (21% of surveyed blocks) estimated the length of the run to be 807 m using followed by silt (16%), coontail (16%), bur-reed (8%), Google Earth and the ruler tool’s path function. We and alligator weed (7%). The other habitats included subtracted the length of the run flowing through mixed species (7%), creeping primrose-willow Ludwigia culverts and across the secondary dam, yielding 671 m repens (6%), rock (6%), cattail Typha sp. (5%), woody of potentially inhabitable stream. We multiplied this and debris and leaf fragments (2%), terrestrial plant species the stream width to estimate the total inhabitable area (2%), fontinalis moss Fontinalis sp. (1%), green arrow (7,046 m2) of the run. For each of the five major habitats, arum Peltandra virginica (1%), sand (1%), green algae we multiplied its proportional coverage as estimated in (1%), emergent sediment deposits (1%), and pondweed the habitat survey by the total inhabitable area of the Potamogeton sp. (,1%). run to yield an estimate of each habitat’s total area. Then, Creeping primrose-willow had the greatest wet and for each major habitat, we multiplied the average density dry weights, while cattail had the least wet and dry of watercress darters (and its subcategories of sex and weights (Table S2, Supplemental Material; Figure 4). The size) by the area occupied by that habitat, and then relative rank order of mean weights was the same for summed these values. wet and dry weights with the exception of watercress We next factored in darters in the remaining minor and alligator weed, which swapped position in rank habitats that comprise 31.4% of the spring run. For minor order. We found significant differences between many of habitats that were vegetated, we used the average the plants when either wet or dry weights were darter density from the four major vegetated habitats compared. In general, creeping primrose-willow and sampled for darters. We then multiplied this density by cattail differed from more species than any others when the estimated area of all minor vegetated habitats in the comparing wet or dry weights. run to approximate the total darters in all minor vegetated microhabitats. For nonvegetated minor hab- Watercress darter survey itats, we used a similar approach by multiplying the Altogether, we captured 629 watercress darters across density of darters in the one nonvegetated major habitat the five major habitats (Table S3, Supplemental Material). (silt) by the estimated area of all minor nonvegetated The majority were captured in coontail (53%), followed habitats in the run. This yielded an estimate of the total by watercress (23%), alligator weed (15%), bur-reed (5%), darters in all minor nonvegetated microhabitats. We and silt (4%) habitats (Table 1). Average darter density in expect this is a conservative estimate because darter coontail was 10-fold higher than in bur-reed and silt

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reed and silt habitats; juvenile densities were intermedi- ate in watercress and alligator weed habitats. Females and males were significantly denser in coontail relative to alligator weed, bur-reed, and silt habitats, while water- cress had an intermediate density for each sex. Medium- sized darters were significantly denser in coontail than in the other habitats, but the few large darters collected in this study were distributed similarly across habitats. Though silt and bur-reed habitats generally had very low densities across all categories, they were not found to be statistically different from most other habitats apart from coontail. The reason for this was that in each of these two habitats, one of the eight samples yielded darters at

a density 4–6 times the mean of the seven other samples Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 of each habitat.

Estimated watercress darter population size in the run Our estimate of the watercress darter population size in the five major habitats, comprising an estimated 68.6% of the spring run, was 85,114 darters (95% CI ¼ 55,995–115,818). Using the average darter density from the four vegetated major habitats (18.9 darters/m2), we calculated there was an additional 29,711 watercress darters (95% CI ¼ 20,269–40,066) in the remaining 22.4% of the run that was vegetated. We calculated the number of darters in the 9% of the run that was nonvegetated to be 2,107 (95% CI ¼ 124–4,250). In sum, we estimated there were 116,932 (95% CI ¼ 79,358–155,965) watercress Figure 4. Average (þSD) wet (A) and dry (B) weights of 10 darters present in the spring run during May–June 2011. samples/species of most abundant plants March–April 2011 in Roebuck Spring, Alabama (note differences in scale), home to a population of the endangered watercress darter Etheostoma Discussion nuchale. Significant differences were detected among species in both data sets. Within each chart, species not sharing the same Our survey of watercress darters in the five most letter differ significantly from one another according to Analysis common habitats of Roebuck Spring yielded new of Variance post hoc analysis (P , 0.05). insights into the ecology of this federally endangered darter. Our novel technique for sampling this species yielded densities far surpassing those of any previous habitats and roughly double that in watercress (the survey of the species. For example, the maximum namesake plant for the darter’s common name). Two- density of darters from a survey of Seven Springs thirds (67%) of captures were juveniles, while 18% and yielded 18/m2 (Duncan et al. 2010), whereas the present 16% were adult females and males, respectively. There study’s maximum was 87/m2. However, inferences were significantly more juveniles in coontail than in bur- about habitat use by watercress darters must take into

Table 1. Mean (SD) number of watercress darters Etheostoma nuchale captured per m2 in eight samples in each of the five dominant habitat types in Roebuck Spring run, Birmingham, Alabama that were sampled in March–April 2011. Range of number of darters per sample in each habitat type is given to the right of the mean, after the semicolon. Statistical values are from One-way Analysis of Variances comparing numbers of captured darters among the habitats. Lower-case letters to the right of the mean and the range indicate the results of post hoc analyses (Tukey’s Honestly Significant Difference) comparing habitats pairwise; habitats sharing the same letter were not significantly different from one another (P . 0.05). SL is standard length.

Habitat type Size category Coontail Watercress Alligator weed Bur-reed Silt FP-value All sizes 41 (23); (16-87) a 18 (22); (3-69) b 12 (6); (2-21) b 4 (4); (0-12) b 3 (4); (0-13) b 8.8 ,0.001 Juvenile (9–23 mm SL) 28 (26) a 12 (21) a,b 8 (6) a,b 1 (2) b 3 (4) b 3.9 0.010 Female 7 (5) a 3 (3) a,b 2 (1) b 2 (2) b 0 (0) b 5.2 0.002 Male 7 (3) a 4 (4) a,b 2 (2) b 1 (1) b 0 (0) b 8.3 ,0.001 Medium (24–31 mm SL) 12 (7) a 5 (5) b 3 (2) b 1 (1) b 0 (0) b 11.9 ,0.001 Large (32–45 mm SL) 2 (1) a 2 (2) a 1 (1) a 2 (2) a 0 (0) a 2.8 0.043

Journal of Fish and Wildlife Management | www.fwspubs.org December 2016 | Volume 7 | Issue 2 | 504 Population Structure and Habitat Use of the Watercress Darter R.S. Duncan et al. consideration that our study provides only a snap-shot half the average number of darters found per sample in during the springtime, and although this is a critically coontail, but higher than the average densities in any important time for the species on account of peak of the other habitats studied. Both fontinalis moss and spawning, habitat use patterns may vary throughout coontail are submergent native species whose numer- the year. For example, as ambient temperatures rise in ous branching filaments form a structurally complex the summer, the distribution of watercress darters may habitat. The presence of both species further diversifies contract toward the spring pool. Furthermore, at our and expands the habitats available for watercress location watercress dies back from late summer to darters. Because fontinalis moss and coontail do not midspringtime, and alligator weed dies back during the develop roots and colonize new areas via stem winter, forcing some darters to find alternative habitats fragments (Crum and Anderson 1981; Godfrey and during these times (RSD, personal observation). Thus, Wooten 1981), both could be easy to introduce during further studies addressing habitat use in other seasons habitat expansion or restoration projects for watercress would likely reveal new insights into the needs of the darters. Creeping primrose-willow, while uncommon at species.

Roebuck Spring, has been found to support densities of Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 For the first time, we documented watercress darters watercressdartersashighas8.7/m2 in seining surveys inhabiting coontail, a plant that appears to provide elsewhere (RSD and BRK, personal observation) and important habitat in the spring run. The plant species is seems to have a comparatively high biomass. Given not known to occupy the spring pool or other springs that it is commonly propagated from cuttings by harboring watercress darters. Darter densities in coontail aquarists (Ozt¨ urk¨ et al. 2004), creeping primrose-willow were more than double those in alligator weed and may be another submergent native plant that could be watercress, the habitats with the next highest densities. easily established to create new watercress darter Alligator weed and watercress are nonnative invasives habitat. that may host fewer native, invertebrate prey species Our findings of moderate to high densities of darters relative to coontail. In addition, alligator weed and across a range of vegetated habitats in the Roebuck watercress die back seasonally and invest in emergent Spring system supports the assessment that watercress growth that does not augment habitat for darters, darters primarily associate with densely vegetated whereas coontail is a submergent plant providing year- habitats, but that otherwise, it is a versatile species. round cover. Though the biomass of these three species These habitats can be deep, with little to no current was comparable, coontail stems were thinner and (e.g., fontinalis moss); moderately deep with swift seemed to be more numerous, thus potentially provid- current (coontail); shallow with a moderate current ing disproportionately more darter habitat. In fact, (alligator weed and watercress); and vegetation can be though coontail was mainly found where the current native or nonnative, and submergent or emergent. The may be too swift for a small darter to occupy, coontail’s proportions of all size and sex classes of darters were thick growth slows the current speed down to half that of the thalweg (RSD, unpublished data). Despite their nearly identical across the coontail, alligator weed, and potential drawbacks as habitat, alligator weed and watercress habitats, suggesting the relative importance watercress seem to provide additional darter habitat of these habitats to the darter is independent of these along the shallow margins of the run where coontail population-structure categories. However, the darter’s does not grow. dependency on densely vegetated habitats may be its Bur-reed had the lowest biomass and lowest average greatest vulnerability at this time. Such habitats can no darter densities of any vegetated habitat. These plants longer be supported throughout most of its range have broad, unbranching, strap-like leaves that are because of channel modification and stormwater submergent or float when young, but become stiff and runoff from the surrounding urban landscape. At all emergent in late summer. Silt habitat had a very low five of the springs supporting watercress darters, average density of darters. Both the silt and, to a lesser aquatic vegetation is scarce to nonexistent in the degree, bur-reed seem to provide little cover for receiving stream (Fluker et al. 2008, 2009b; Duncan and watercress darters and probably support relatively low Kuhajda 2012). amounts of prey. Darters captured in both habitats may Similar studies of the relationship between the have been in transit to more suitable habitats. geomorphology and habitat use and availability of Surveys of the spring pool have found that fontinalis other springs harboring watercress darters would moss, which grows liberally there, shelters an abun- significantly advance the knowledge needed to help dance of darters (Fluker et al. 2008, 2009b; Duncan and the species recover. In the Roebuck Springs run, our Kuhajda 2012). As part of our separate and parallel findings suggest that geomorphological diversity helps study quantifying the effectiveness of the frame sustain a diversity of aquatic vegetation. This plant method for sampling darters, we completed a single diversity may be critical for sustaining the run’s robust sample of fontinalis moss habitat using the frame in population by ensuring there is appropriate habitat Roebuck Spring pool. This sample yielded 21 darters, of available over the seasons and during episodic disrup- which 5 were juveniles, 13 were medium-sized, and 3 tions such as drought and extreme freezes. Any were large; the adults included 6 males and 10 females. perturbation reducing the geomorphological diversity Though we caution against overinterpretation of this and, hence habitat diversity, is a threat to the single sample, we note that these values are roughly population, including high levels of stormwater runoff,

Journal of Fish and Wildlife Management | www.fwspubs.org December 2016 | Volume 7 | Issue 2 | 505 Population Structure and Habitat Use of the Watercress Darter R.S. Duncan et al. anthropogenic channel modification, or even extensive Roebuck Spring run during May–June 2011. Each habitat hydrological alteration by beavers. was sampled in eight locations. Fish were trapped in a 1 To our knowledge, this study provides the most 3 1 3 0.77 m aluminum-frame throw trap, extracted with complete picture of the structure and habitat use of a the single pass of a seine net, then sampled to depletion watercress darter population to date. This population with dip nets. Fish were measured (standard length) and was probably near its annual maximum because peak classified by size and sex. spawning occurs in springtime. Males and females were Found at: DOI: http://dx.doi.org/10.3996/072015- found in similar proportions, and there were very few JFWM-062.S3 (219 KB DOCX). large adults, as could be expected for this short-lived species. Juveniles comprised two-thirds of the popula- Reference S1. Benson AJ, Jacono CC, Fuller PL, tion in the spring run, suggesting that prolific reproduc- McKercher ER, Richerson MM. 2004. Summary report of tion is occurring. Given that one-third of the population nonindigenous aquatic species in U.S. Fish and Wildlife was mature, we expect that approximately half the Service Region 5. Report to the U.S. Fish and Wildlife juveniles present in May–June 2011 would survive to Service, Arlington, Virginia. adulthood over the next year if conditions in the Found at: DOI: http://dx.doi.org/10.3996/072015- Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 population remain stable. Though Roebuck Spring’s run JFWM-062.S4 (4.6 MB PDF); also available at https://nas. harbors a large population of darters, this population er.usgs.gov/publications/R5finalreport.pdf (4.6 MB PDF). faces threats presented by urban stormwater; beavers and muskrats Ondatra zibethicus that destroy aquatic Reference S2. Duncan RS, Kuhajda BR. 2012. Status vegetation used by the darter; and the nonnative survey of the endangered watercress darter, Etheostoma invasive virile crayfish Orconectes virilis, which is a nuchale. Report to U.S. Fish and Wildlife Service, Jackson, probable predator of, and competitor with, the water- Mississippi. cress darter (Savino and Miller 1991; Bryan et al. 2002; Found at DOI: http://dx.doi.org/10.3996/072015- Dorn and Mittelbach 2004; Taylor and Soucek 2010). JFWM-062.S5 (4.2 MB PDF). However, this new knowledge about the darter’s habitat preferences may help managers restore darter habitat Reference S3. Fluker BL, Kuhajda BR, Harris PM. 2008. after disturbances and expand darter habitat when Status and distribution survey and genetics of the opportunities arise. endangered watercress darter, Etheostoma nuchale. Report to the Alabama Department of Conservation Supplemental Material and Natural Resources (Montgomery) and the U.S. States Fish and Wildlife Service, Jackson, Mississippi. Please note: The Journal of Fish and Wildlife Manage- Found at DOI: http://dx.doi.org/10.3996/072015- ment is not responsible for the content or functionality JFWM-062.S6 (7.4 MB PDF). of any supplemental material. Queries should be directed to the corresponding author for the article. Reference S4. Fluker BL, Kuhajda BR, Harris PM. 2009b. Status and distribution survey and genetics of Table S1. Data on vegetation cover and stream the endangered watercress darter, Etheostoma nuchale. geomorphology collected from Roebuck Spring run Report to the Alabama Department of Conservation and during March–April 2011 using 17 belt transects placed Natural Resources, Montgomery, and U.S. Fish and across the run at 40-m intervals. Located in Birmingham, Wildlife Service, Jackson, Mississippi. Alabama, the spring is one of five known locations Found at DOI: http://dx.doi.org/10.3996/072015- sheltering the endangered watercress darter Etheostoma JFWM-062.S7 (3.6 MB PDF). nuchale. Found at: DOI: http://dx.doi.org/10.3996/072015- Reference S5. Griffith GE, Omernik JM, Comstock JA, JFWM-062.S1 (48 KB XLSX). Lawrence S, Martin G, Goddard A, Hulcher VJ, Foster T. 2001. Ecoregions of Alabama and Georgia, (color poster Table S2. Dry weights (above) and wet weights with map, descriptive text, summary tables, and photo- (below) of common aquatic plants (and plant debris) graphs). Reston, Virginia: U.S. Geological Survey. collected during April 2011 from among 17 transects Found at DOI: http://dx.doi.org/10.3996/072015- spanning Roebuck Spring run, Birmingham, Alabama. JFWM-062.S8 (6.0 MB PDF); also available at https:// The spring is one of the five known locations for the archive.epa.gov/wed/ecoregions/web/html/alga_eco. endangered watercress darter Etheostoma nuchale.Dry html (6.0 MB, pdf). and wet weights were used as measures of habitat quality for the darter. Data linking dry and wet weights Reference S6. [USFWS] United States Fish and Wildlife for individual samples were lost, so each is reported here Service. 1992. Watercress darter (Etheostoma nuchale) in separate tables. recovery plan. Jackson, Mississippi: USFWS. Found at: DOI: http://dx.doi.org/10.3996/072015- Found at DOI: http://dx.doi.org/10.3996/072015- JFWM-062.S2 (18 KB DOCX). JFWM-062.S9 (1.0 MB PDF).

Table S3. Data on watercress darters Etheostoma Reference S7. [USFWS] United States Fish and Wildlife nuchale captured in surveys of five major habitat types in Service. 2009. Watercress darter (Etheostoma nuchale)5-

Journal of Fish and Wildlife Management | www.fwspubs.org December 2016 | Volume 7 | Issue 2 | 506 Population Structure and Habitat Use of the Watercress Darter R.S. Duncan et al. year review: summary and evaluation. Jackson, Missis- predators. Environmental Biology of Fishes 63:49–56. sippi: USFWS. doi: 10.1023/A:1013899125938 Found at DOI: http://dx.doi.org/10.3996/072015- Crum HA, Anderson LE. 1981. Mosses of eastern North JFWM-062.S10 (154 KB PDF). America. New York: Columbia University Press. Dorn NJ, Mittelbach GG. 2004. Effects of a native crayfish Reference S8. [USFWS] United States Fish and Wildlife (Orconectes virilis) on the reproductive success and Service. 2014. Listing and occurrences statewide for nesting behavior of sunfish (Lepomis spp.). Canadian Alabama. Daphne: Alabama Ecological Services Field Journal of Fisheries and Aquatic Sciences 61:2135– Office. 2143. doi: 10.1139/f04-158 Found at DOI: http://dx.doi.org/10.3996/072015- Duncan RS. 2013. Southern wonder: Alabama’s surprising JFWM-062.S11 (66 KB PDF); also available at: http:// biodiversity. Tuscaloosa: University of Alabama Press. ecos.fws.gov/tess_public/reports/species-listed-by-state- Duncan RS, Elliot C, Fluker BL, Kuhajda BR. 2010. Habitat report?state AL&status listed (66 KB, pdf). ¼ ¼ use of the watercress darter (Etheostoma nuchale): an

endangered fish in an urban landscape. American Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/7/2/499/2362009/072015-jfwm-062.pdf by guest on 26 September 2021 Acknowledgments Midland Naturalist 164:9–21. doi: 10.1674/0003-0031- 164.1.9 This study was supported in part by a research contract Duncan RS, Kuhajda BR. 2012. Status survey of the from the U.S. Fish and Wildlife Service (USFWS contract endangered watercress darter, Etheostoma nuchale. 40181AM387). We would like to thank the City of Report to U.S. Fish and Wildlife Service, Jackson, Birmingham, the Alabama Department of Conservation Mississippi (see Supplemental Material, Reference S2, of Natural Resources, and USFWS for permission to http://dx.doi.org/10.3996/072015-JFWM-062.S5 (4.2 conduct this study. We are grateful for additional MB PDF). support from the University of Alabama and Birming- Fluker BL, Kuhajda BR, Duncan RS, Salter EL, Schulman M. ham-Southern College. We are very indebted to J. Heath 2009a. Impacts of a small dam removal on the Howell, Karen Marlowe, Zach Napier, Rebecca P. Parker, endangered watercress darter. Proceeding of the Matthew S. Piteo, Josh Rabbit, Marty Schulman, and Annual Conference of the Southeast Association of Nicole White for their assistance in conducting the fish Fish and Wildlife Agencies 63:188–195. sampling. Special thanks to Josh Ennen for assistance Fluker BL, Kuhajda BR, Harris PM. 2008. Status and with statistics and Sarah C. Hazzard for assistance with distribution survey and genetics of the endangered cartography (Figure 2). We extend our appreciation to watercress darter, Etheostoma nuchale. Report to the two anonymous reviewers and a Subject Editor, whose Alabama Department of Conservation and Natural feedback improved our manuscript. Permits to collect Resources (Montgomery) and the U.S. Fish and Wildlife the species were issued to coauthor B.K. Kuhajda (USFWS Service, Jackson, Mississippi (see Supplemental Mate- Permit TE137403-0 and State of Alabama Protected rial, Reference S3, http://dx.doi.org/10.3996/072015- Species Scientific Collecting Permit 2011000061868680). JFWM-062.S6 (7.4 MB PDF). Any use of trade, product, or firm names is for Fluker BL, Kuhajda BR, Harris PM. 2009b. Status and descriptive purposes only and does not imply endorse- distribution survey and genetics of the endangered ment by the U.S. Government. watercress darter, Etheostoma nuchale. Report to the Alabama Department of Conservation and Natural References Resources, Montgomery, and U.S. Fish and Wildlife Service, Jackson, Mississippi (see Supplemental Mate- Baker WH, Blanton RE, Johnston CE. 2013. Diversity rial, Reference S4, http://dx.doi.org/10.3996/072015- within the redeye bass, Micropterus coosae (Perci- JFWM-062.S7 (3.6 MB PDF). formes: Centrarchidae) species group, with description Fluker BL, Kuhajda BR, Lang NJ, Harris PM. 2010. Low of four new species. Zootaxa 3635:379–401. doi: 10. genetic diversity and small long-term population sizes 11646/zootaxa.3635.4.3 in the spring endemic watercress darter, Etheostoma Benson AJ, Jacono CC, Fuller PL, McKercher ER, Richerson nuchale. Conservation Genetics 11:2267–2279. doi: 10. MM. 2004. Summary report of nonindigenous aquatic 1007/s10592-010-0111-y species in U.S. Fish and Wildlife Service Region 5. Godfrey RK, Wooten JW. 1981. Aquatic and wetland Report to the U.S. Fish and Wildlife Service, Arlington, plants of Southeastern United States: Dichotyledons. Virginia (see Supplemental Material, Reference S1, DOI: Athens: University of Georgia Press. http://dx.doi.org/10.3996/072015-JFWM-062.S4 (4.6 Griffith GE, Omernik JM, Comstock JA, Lawrence S, Martin MB PDF); also available: https://nas.er.usgs.gov/ G, Goddard A, Hulcher VJ, Foster T. 2001. Ecoregions publications/R5finalreport.pdf (December 2015). Bo- of Alabama and Georgia, (color poster with map, schung HT, Mayden RL. 2004. Fishes of Alabama. descriptive text, summary tables, and photographs). Washington, D.C.: Smithsonian Books. Reston, Virginia: U.S. Geological Survey (see Supple- Bryan SD, Robinson AT, Sweetser MG. 2002. Behavioral mental Material, References S5, http://dx.doi.org/10. responses of a small native fish to multiple introduced 3996/072015-JFWM-062.S8 (6.0 MB PDF); also avail-

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