2010 SOUTHEASTERN NATURALIST 9(3):507–520 Life-history Attributes of the Imperiled Frecklebelly Madtom, Noturus munitus (Siluriformes: Ictaluridae), in the Cahaba River System, Alabama Micah G. Bennett1,2,*, Bernard R. Kuhajda1, and Jenjit Khudamrongsawat1,3 Abstract - Noturus munitus (Frecklebelly Madtom) is a diminutive catfish with a disjunct distribution across the southeastern United States in large rivers and tributaries of the Mobile Basin and Pearl River drainage. Its distribution has contracted since extensive river modification began throughout its range in the 1960s, and it is likely extirpated from the Alabama River. We collected 242 specimens of N. munitus from a gravel island in the Cahaba River on the Coastal Plain in Alabama from May 2005 to March 2007 to examine life-history characteristics. Adults were associated with fast flow over large gravel at depths of 0.5–1.0 m. Young (<23 mm) were found at water depths of 0.4–0.5 m. Gonad development indicated a reproductive season from May to August, with collection of young-of-the-year in June and July supporting a mid- to late-summer spawn. Stomach content analysis revealed a diet similar to other Noturus species and dominated in volume by Baetidae nymphs (31.2%), Hydropsychidae larvae (20.3%), and Simuliidae larvae (19.7%). Some seasonal and sex differences in diet were apparent. Relative fecundity data indicate that N. munitus is one of the most fecund madtoms of the subgenus Rabida (mean of 30.6 mature oocytes) studied thus far. Few males were found in riffles during summer, and no young were found in riffles outside summer, indicating potential sex and size differences in seasonal habitat use. This knowledge is important for conservation of the species. Introduction Since Taylor’s (1969) revision of the genus Noturus, there has been a major effort to close gaps in our knowledge of madtom biology, and much information is known for the genus as a whole (reviewed in Burr and Stoeckel 1999). As a group, the North American genus is imperiled due to river modification and other human impacts to aquatic ecosystems (Burr and Stoeckel 1999, Jelks et al. 2008). However, several species still have no or only partial life-history data published. One of these imperiled species is Noturus munitus Suttkus and Taylor (Frecklebelly Madtom), a robust, boldly patterned member of the monophyletic saddled madtom subgenus Rabida (Hardman 2004, Near and Hardman 2006, Suttkus and Taylor 1965). Noturus munitus has a disjunct distribution across the southeastern United States in the Mobile Basin and 1University of Alabama Ichthyological Collection, Department of Biological Sciences, Box 870345, Tuscaloosa, AL 35487-0345. 2Current address - Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103-2010. 3Current address - Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand. *Corresponding author - micahgbennett@yahoo.com. 508 Southeastern Naturalist Vol. 9, No. 3 Pearl River drainage (Fig. 1). It occupies large and medium-sized rivers mostly on the Gulf Coastal Plain, with an additional population in upland areas in the upper Coosa River (Conasauga and Etowah systems) in Georgia and Tennessee, which is considered an undescribed form (Boschung and Mayden 2004, Butler and Mayden 2003, Jelks et al. 2008, Neely et al. 1998, Suttkus and Taylor 1965). Although once fairly abundant in appropriate habitat, N. munitus has declined rapidly since the mid-1960s, when river modification began throughout its range. The species is now reliably found in high numbers in only a few locations (Bennett et al. 2008, Boschung and Mayden 2004, Piller et al. 2004, Shepard 2004) and is considered threatened with extinction (Bennett et al. 2008, Jelks et al. 2008). Trauth et al. (1981) examined aspects of reproductive development and population structure in Mississippi, and Miller (1984) conducted a detailed study of the diet in a population of N. munitus from the Tombigbee River system; however, the species’ overall rarity, combined with its nocturnal habits and preference for difficult-to-sample large-river gravel shoals, has contributed to the lack of detailed life-history information for N. munitus. Figure 1. Current and historical distribution of N. munitus. Gray shading represents historic range. Hatching represents current distribution. 1. Pearl River drainage—a) Bogue Chitto River, b) lower Pearl River and tributaries; 2. upper Tombigbee River drainage—a) East Fork, b) Buttahatchie River, c) lower Luxapallila Creek, d) Sipsey River; 3. Alabama and Cahaba river drainages—a) lower Cahaba River; 4. Etowah River system—a) upper Etowah River; 5. Conasauga River system—a) middle Conasauaga River. Black dot is study site on Cahaba River. 2010 M.G. Bennett, B.R. Kuhajda, and J. Khudamrongsawat 509 One of the few drainages in which N. munitus persists in abundance is the Cahaba River in central Alabama, which has escaped large-scale damming and other anthropogenic modifications. The Cahaba River flows approximately 307 km (191 mi) through north-central Alabama, beginning in the Valley and Ridge physiographic region near Birmingham and flowing through the Coastal Plain into the Alabama River near Selma (Boschung and Mayden 2004). The river has escaped major channelization and maintains numerous gravel islands and shoals throughout its lower Coastal Plain section, which provide habitat for N. munitus and other large-river specialists. Here, we provide information on the age, diet, habitat, and reproduction of N. munitus from the Cahaba River to add to the growing body of knowledge of madtom ecology and to aid in our understanding and ability to protect this imperiled species. Methods Two hundred forty-two specimens of N. munitus were collected and formalin-fixed during nighttime sampling from May 2005 to March 2007 from a gravel island on the Cahaba River (32.66500°N, -87.24083°W) using a 4.6- x 1.2-m mesh seine and a backpack electrofisher. Measurements of habitat included flow rate (estimated by timing a floating object for a distance of 10 m), depth (measured using meter stick), and substrate. No collections were made from January–March 2006 and August–January 2006–07 due to high water or because adequate samples were collected the previous year. After transfer to 70% ethanol, standard length (SL) was measured to the nearest 0.1 mm using dial calipers, and specimens were blotted dry to determine wet body mass to the nearest 0.01 g. Sex of individuals was determined by internal examination of gonads: testes were white and lobed (cf., Mayden and Burr 1981, Sneed and Clemens 1963), and ovaries consisted of spherical white, orange or amber oocytes (cf., Mayden and Burr 1981). Gonads were weighed to the nearest 0.001 g and a gonadosomatic index (GSI) was calculated using the formula ([gonad weight x 1000] / somatic body weight [i.e., after removal of abdominal organs except the air bladder]) following Mayden and Burr (1981). Oocyte maturity stage was determined using classification systems of both Baker and Heins (1994) and Mayden and Burr (1981). Oocytes from mature, ripening, and ripe ovaries (Baker and Heins 1994) and mature or potentially mature ovaries (Mayden and Burr 1981) were counted, and the diameters of three oocytes from each ripening and ripe individual were measured to the nearest 0.01 mm. A sub-sample of individuals, which included the two largest males, the two largest females, and the two smallest individuals, was selected for diet analysis from each season (spring = April–May; summer = June–August; 510 Southeastern Naturalist Vol. 9, No. 3 fall = September–November; winter = December–February). This subsample was supplemented with intermediate-sized fish to increase sample sizes for seasonal and other comparisons for a total of 91 stomachs. Stomach contents were identified to family when possible, the proportion of each type of food item was determined, and the volume of each type of food item was approximated following Winemiller (1990). Percent of total volume of diet items was compared between sexes and two size classes (large [>42 mm SL] and small [23–40 mm SL]), and among seasons. We tested for significant deviations from equal sex ratio using a chi square test in Excel (Microsoft Corp., Seattle, WA). Age classes were visually estimated by examining length-frequency data for various time periods of the study. Results Habitat and associated species Several large-river specialists were frequently collected with N. munitus, including Macrhybopsis sp. cf. aestivalis, an undescribed Speckled Chub, Macrhybopsis storeriana (Kirtland) (Silver Chub), Notropis uranoscopus Suttkus (Skygazing Shiner), Crystallaria asprella (Jordan) (Crystal Darter), Percina lenticula Richards and Knapp (Freckled Darter), and Percina vigil (Hay) (Saddleback Darter) (Boschung and Mayden 2004, Shepard 2004). Adult madtoms were collected in swift current (mean = 1 m/sec) over large gravel, sometimes with sticks and leaf detritus, at depths of 0.5–1.0 m. Young-of-the-year madtoms (<23 mm) collected in June and July were associated with slower current in shallower water (0.4–0.5 m). Noturus munitus was not collected over sand or associated with aquatic vegetation. On two occasions, adult madtoms were collected within partially buried mussel shells. Reproduction Reproductive development based on GSI values increased rapidly in March for females, showing sustained high gonad-to-body weight ratios during the spring. Their GSI values (range = 1.6–271.1) peaked in June, followed by a substantial drop in July (Fig. 2). Male GSI values (range = 0.0– 8.8) peaked in May (Fig. 3). For all females, SL was significantly correlated with gonad weight based on linear regression (R² = 0.64 for log-transformed values, P < 0.001). Of the 123 females examined for reproductive development, 15 were early-maturing, 64 were late-maturing, 34 were mature, 8 were ripening, and 2 were ripe based on the classifications of Baker and Heins (1994). According to the classifications of Mayden and Burr (1981), all earlymaturing and late-maturing individuals were immature, and there were 32 potentially mature and 12 mature individuals. Mature oocytes were usually smaller and cream, opaque-yellow, or yellow. Ripening and ripe oocytes 2010 M.G. Bennett, B.R. Kuhajda, and J. Khudamrongsawat 511 were large (range = 1.6–2.5 mm, mean = 2.9 mm, n = 30) in diameter and amber or orange in color; ripe ovaries were darker towards the urogenital opening (cf., Heins et al. 1992). All fish with ripening and ripe oocytes also contained a second distinct size class of latent white oocytes less than Figure 3. Mean gonadosomatic index by capture date for male N. munitus (Frecklebelly Madtom). Note gaps in sequence from June–August 2005, December 2005–April 2006, and July 2006–February 2007 due to no samples or absence of mature individuals. Error bars represent ± 1 standard error. Figure 2. Mean gonadosomatic index by capture date for female N. munitus (Frecklebelly Madtom). Note gaps in sequence from June–August 2005, December 2005–April 2006, and July 2006–February 2007 due to no samples or absence of mature females. Error bars represent ± 1 standard error. 512 Southeastern Naturalist Vol. 9, No. 3 0.1 mm in diameter (cf., Baker and Heins 1994, Mayden and Burr 1981). One individual with mature oocytes was found in November; however, most mature individuals were found from March through June. Individuals with ripening oocytes were found from April through June and, along with ripe individuals, had the highest GSI values. The only two ripe individuals were found in June. All 10 ripening and ripe individuals and nine of the larger mature individuals from April through June were used to calculate fecundity (Baker and Heins 1994). Total number of oocytes from both ovaries (absolute ovarian fecundity, Burr and Stoeckel 1999) ranged from 70–171 in the 19 females examined (mean = 119). Relative fecundity (mature oocytes per g body weight) ranged from 21–39 (mean = 31). Even though the mature stage encompassed a broad range of oocyte sizes (Baker and Heins 1994), restricting fecundity measurements to ripening and ripe females (the mature of Mayden and Burr 1981) did not produce a significantly different mean value or range. The smallest mature female was 41.1 mm SL, which corresponds to the approximate 2+ age class. The total number of oocytes increased with SL for all females (R² = 0.39, P = 0.004), but the relationship was stronger for ripening and ripe females (R² = 0.55, P = 0.014). The sex ratio for the entire Table 1. Stomach contents for 91 specimens of N. munitus (Frecklebelly Madtom) by mean percent volume and mean percent total number. Food items Mean % volume Mean % composition by number Insecta Diptera Chironomidae 2.3 9.0 Simuliidae 19.7 40.8 Tipulidae 0.3 0.6 Ephemeroptera Baetidae 31.2 35.4 Heptageniidae 0.1 0.4 Isonychiidae 6.0 0.4 Tricorythidae 0.5 0.5 Unknown 3.5 0.8 Plecoptera Perlidae 2.4 0.3 Perlodidae 5.0 0.5 Trichoptera Polycentropodidae 1.3 1.1 Hydropsychidae 20.3 9.4 Hydroptilidae 0.3 0.2 Psychomyiidae 0.04 0.1 Coleoptera Elmidae 0.2 0.2 Hemiptera Coryxidae 0.5 0.2 Other 5.4 0.1 2010 M.G. Bennett, B.R. Kuhajda, and J. Khudamrongsawat 513 sample was not significantly different from 2 females:1 male based on a chi-square test (1.74 females/male, P = 0.74). This pattern was the same for individuals in late spring through summer (May–August) (2.8 females/male, P = 0.26), but in fall (September–December), the ratio was not significantly different from 1:1 (1.5 females/male, P = 0.09). Diet Diet analysis showed Baetidae nymphs (31%), Hydropsychidae larvae (20%), and Simuliidae larvae (20%) provided most of the food volume for N. munitus (Table 1). These three groups maintain top position by percent of total number (35, 9, and 41% respectively), although the order of relative importance changes. Chironomidae made up a higher proportion of diet by number than by volume (Table 1). An item of interest in a stomach (placed in the “other” category in Tables 1–3) was a larval ictalurid. Chironomidae made up a much larger portion of the diet in winter (21%) than in other seasons (≤3%) (Table 2). Baetidae nymphs made up 56% of the diet volume in spring, but only 14–22% in other seasons. Simuliidae larvae made up 38% of the diet volume in fall, but only 1–17% in Table 2. Stomach content analysis by season for 91 specimens of N. munitus (Frecklebelly Madtom). %V = percent volume, %N = percent by number Spring (n = 25) Summer (n = 22) Fall (n = 22) Winter (n = 22) Food items %V %N %V %N %V %N %V %N Insecta Diptera Chironomidae 3.3 10.5 1.5 10.6 1.1 2.7 21.2 63.3 Simuliidae 8.2 22.0 17.4 49.9 38.1 59.8 1.0 2.5 Tipulidae 0.0 0.0 0.53 1.3 0.45 0.54 0.17 1.3 Ephemeroptera Baetidae 55.9 60.1 13.8 18.1 20.2 21.0 21.7 13.9 Heptageniidae 0.92 0.39 0.40 0.25 0.0 0.0 15.2 5.1 Isonychiidae 10.3 0.58 0.0 0.0 8.9 0.54 0.0 0.0 Tricorythidae 0.92 0.78 0.67 0.76 0.0 0.0 0.0 0.0 Unknown 0.0 0.0 6.8 1.8 4.5 0.81 0.0 0.0 Plecoptera Perlidae 1.1 0.19 0.0 0.0 2.5 0.54 9.9 1.3 Perlodidae 0.0 0.0 15.4 1.8 0.0 0.0 0.0 0.0 Trichoptera Polycentropodidae 0.0 0.0 0.0 0.0 0.89 0.0 0.0 0.0 Hydropsychidae 14.3 4.5 25.3 12.7 21.7 12.4 21.2 11.4 Hydroptilidae 0.65 0.19 0.0 0.0 0.37 0.27 0.0 0.0 Psychomyiidae 0.0 0.0 0.13 0.25 0.0 0.0 0.0 0.0 Other 1.3 0.19 3.1 2.5 0.89 0.81 0.33 1.3 Coleoptera Elmidae 0.40 0.19 0.0 0.0 0.0 0.27 0.0 0.0 Hemiptera Coryxidae 1.4 0.39 0.0 0.0 0.0 0.0 0.0 0.0 Other 1.3 N/A 14.9 N/A 0.30 0.27 9.3 0.0 514 Southeastern Naturalist Vol. 9, No. 3 other seasons. Isonychiidae nymphs appeared in the diet only in spring and fall, and Perlodidae larvae were found only in summer. Percentage of empty stomachs was greatest in spring (24%) and winter (23%) and low in summer and fall (5%). Diet comparison between 17 large and 17 small individuals indicated a heavier reliance on Chironomidae by small madtoms (3% of diet volume versus 1% in large individuals) and a greater diversity of prey items consumed by large individuals. Small individuals consumed a total of 10 taxa compared to 14 taxa consumed by large individuals. Examination of male and female stomach contents (Table 3) revealed more utilization of Simuliidae (32%) and Isonychiidae (7%) by volume in males, but both sexes heavily utilized Baetidae (32%) and Hydropsychidae (males 17%; females 24%). Females consumed a larger total volume (1416 μL) than an equal number of males (810 μL). Age Length-frequency histograms were somewhat difficult to interpret due to low sample size for some seasons and the absence of individuals <37 mm from October to December 2005 and should be taken as only preliminary Table 3. Stomach content analysis by sex for 91 specimens of N. munitus (Frecklebelly Madtom). Males Females Food items % volume % by number % volume % by number Insecta Diptera Chironomidae 2.8 12.3 2.1 10.9 Simuliidae 31.8 45.1 13.8 34.8 Tipulidae 0.25 0.51 0.39 0.65 Ephemeroptera Baetidae 32.2 31.3 32.3 37.0 Heptageniidae 1.6 0.51 0.71 0.52 Isonychiidae 7.4 0.34 0.21 0.39 Tricorythidae 0.74 0.68 0.42 0.39 Unknown 4.9 0.85 2.9 0.65 Plecoptera Perlidae 0.37 0.17 3.7 0.39 Perlodidae 0.0 0.0 8.2 0.91 Trichoptera Polycentropodidae 0.99 1.0 1.6 1.0 Hydropsychidae 16.5 6.8 23.6 11.4 Hydroptilidae 0.0 0.0 0.53 0.26 Psychomyiidae 0.12 0.17 0.0 0.0 Coleoptera Elmidae 0.0 0.0 0.25 0.26 Hemiptera Coryxidae 0.0 0.0 0.78 0.26 Other 0.25 0.17 8.6 0.12 2010 M.G. Bennett, B.R. Kuhajda, and J. Khudamrongsawat 515 hypotheses for age structure. In the April–June histogram (Fig. 4) and the July–September histogram (Fig. 5), the one with the largest sample size, there appear to be approximately three size classes. Most of the young-ofthe- year (0+) appear to have grown quickly, with a mode around 29 mm (17–31 mm), and a second mode of around 34 mm may correspond to age 1+ fish (31–43 mm), but the upper boundary of this class is difficult to define (Fig. 5). The 2+ is difficult to assign due to lack of specimens from 49–66 mm, but may be represented by the mode of 53 mm in the October to December 2005 histogram, with possible 3+ individuals greater than or equal to 58 mm (Fig. 6). The largest specimen collected was a 66.8 mm male. Figure 5. Length-frequency histogram for N. munitus (Frecklebelly Madtom) collected from July–September 2005 and 2006. Bars represent estimated age classes. Figure 4. Length-frequency histogram for N. munitus (Frecklebelly Madtom) collected from April–June 2005 and 2006. Bars represent estimated age classes. 516 Southeastern Naturalist Vol. 9, No. 3 Young-of-the-year individuals (13–23 mm SL) were first collected in late June of 2005 and 2006 and were collected through late July. Most individuals collected were in the 1+ age class. Discussion Our data rank N. munitus as highly fecund compared to other members of the subgenus Rabida. Based on data compiled in Burr and Stoeckel (1999) and adding data from Bulger et al. (2002), absolute fecundity in Rabida ranges from 14 to 340 (mean = 89.7) and relative fecundity, which is only available for 5 of the 18 extant Rabida species, ranges from 11.7 to 43.1 (mean = 20.5). The mean absolute fecundity of N. munitus (119.4) is about average for Rabida, but its mean relative fecundity (30.6), preferable for comparing species (Mayden and Walsh 1984), is among the highest known for the subgenus, with higher values reported only from a subspecies of the Least Madtom, N. hildebrandi lautus Taylor (Mayden and Walsh 1984). Noturus munitus is intermediate in mean absolute fecundity between two of its closest relatives, N. placidus Taylor (Neosho Madtom) (41.5; Bulger et al. 2002) and N. stigmosus Taylor (Northern Madtom) (191; Burr and Stoeckel 1999) (Hardman 2004, Near and Hardman 2006). Reproduction and diet are similar to those for other madtom species. Noturus munitus likely spawns in mid-late summer and appears to reach reproductive maturity during the second summer of life, as has been reported for most madtom species not attaining 100 mm SL (Burr and Stoeckel 1999). Based on current knowledge of diet (Miller 1984), N. munitus is an opportunistic insectivore feeding on a variety of aquatic insect larvae. Our Figure 6. Length-frequency histogram for N. munitus (Frecklebelly Madtom) collected from October–December 2005. Bars represent estimated age classes. 2010 M.G. Bennett, B.R. Kuhajda, and J. Khudamrongsawat 517 data for N. munitus diet are similar to results from Miller’s (1984) study on a Tombigbee River population which found only slight changes in important prey taxa through time and between sexes. The few seasonal changes in diet probably reflect differences in prey availability, as has been previously found for N. munitus and several other madtom species (Burr and Stoeckel 1999, Miller 1984). Variations in sex ratio, presence of young-of-the-year, and a sharp drop in female GSI from June to July, provide important clues to seasonal habitat shifts in N. munitus at our sampling site. While no nests of N. munitus have been found, different sex ratios in summer (2 females to 1 male) versus fall (1:1), as well as lack of adults in summer, may result from males moving to pools (where wading sampling is not possible) to prepare nesting sites while females remain more evenly dispersed among different habitats (Burr and Stoeckel 1999, Clugston and Cooper 1960, Mayden and Burr 1981). Higher male mortality, which could also explain unequal sex ratios, is unlikely because males made up a greater portion of the larger size classes (Clugston and Cooper 1960, Mayden and Walsh 1984). Lack of small madtoms in fall collections (all were ≥34 mm) may indicate that young-ofthe- year spend several months in slow-moving, deep-water habitats after hatching. The sharp break in female GSI values from June to July could result from ripe females moving to male-guarded nesting sites in pools, out of the reach of our collecting gear. This explanation is further supported by the fact that all females collected in July 2006 were less than 31 mm SL, smaller than the youngest mature female collected during the study (41.1 mm SL). These data combined with the presence of young-of-the-year in late June may suggest spawning and nesting in pools in June and July. Brewer et al. (2008) found similar results with N. flavus Rafinesque (Stonecat), in a Missouri river, with adults becoming rare in May and June and returning in July, and suggested that histological techniques, rather than GSI, may be more useful in fishes that move to difficult-to-sample habitats for spawning because it would reveal internal morphological and physiological changes associated with spawning in individual fish and would thus require fewer samples. Of the 29 described Noturus species, more than 50% are considered vulnerable, imperiled, or extinct, and many of the undescribed forms are likely in need of conservation action due to small ranges and increasing anthropogenic threats (Burr and Stoeckel 1999, Jelks et al. 2008). We still lack a basic understanding of the biology of some of the most critically imperiled madtoms due to their rarity (e.g., N. crypticus Burr, Eisenhour, and Grady [Chucky Madtom]; N. fasciatus Burr, Eisenhour, and Grady [Saddled Madtom]; Noturus stanauli Etnier and Jenkins [Pygmy Madtom]; N. taylori Douglas [Caddo Madtom]). While phylogeny can be used to infer traits of closely related species, there are still gaps in our understanding of evolutionary relationships and important aspects of reproductive 518 Southeastern Naturalist Vol. 9, No. 3 biology. For example, nesting biology and habitat has yet to be determined for N. munitus, and although these data could potentially be inferred from close relatives N. placidus and N. stigmosus (Hardman 2004), there is also very little information for these species (Burr and Stoeckel 1999, Holm and Mandrak 2001, MacInnis 1998). Successful conservation of aquatic biodiversity in the future will depend on accurate knowledge of species’ habitat and life-history traits, the communities and ecosystems they occupy, recognition and description of evolutionary diversity within currently described species, and our ability as scientists to educate and involve more citizens in research and conservation efforts (Angermeier 2007, Mayden and Wood 1995). Acknowledgments We thank J.H. Howell, A. Waggoner, N. Putman, C. Fluker, B.L. Fluker, G. Hubbard, A. Rypel, T.B. Kennedy, L. Robinson, M. Sandel, P. Hegji, and R. Butler for much-needed field assistance. 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