2007 SOUTHEASTERN NATURALIST 6(3):479–490 Life -history Aspects of Hypentelium etowanum (Alabama Hog Sucker) (Actinopterygii: Catostomidae) in Northern Georgia Christopher T. O’Kelley1 and Steven L. Powers1,* Abstract - Life-history aspects of Hypentelium etowanum (Alabama Hog Sucker) were investigated from 12 monthly collections in Shoal and Moore creeks (Etowah River Drainage) in Cherokee County, GA. Specimens were collected primarily from riffles, runs, and flowing pools, and examined for age, growth, food habits, and reproductive cycle. Chironomidae composed the bulk of the diet, with consumption lowest in winter and peaking in spring. Spawning appeared to occur in spring with 493–2717 ripe eggs ranging from 1.5 to 2.8 mm in diameter present in specimens collected in March, April, and May. Sexual maturity appeared to occur by 3 years of age, with a maximum lifespan of greater than 4 years. The largest specimen collected was a female 190 mm standard length and 132 g total weight. Introduction Hypentelium etowanum (Alabama Hog Sucker) was described by David Starr Jordan in 1877 from specimens collected in the Etowah River near Rome, GA (Gilbert 1998) and is sister to the widespread H. nigricans (LeSueur) (Northern Hog Sucker) (Berendzen et al. 2003, Harris et al. 2002). Hypentelium etowanum is relatively common in small to large streams throughout the Mobile and upper Chattahoochee River drainages of northern Georgia, Alabama, and eastern Mississippi. It is distinguished from other catostomids within most of its range by dark oblique bars across the dorsum; bright orange pectoral, pelvic, and anal fins; horizontal pale stripes along the scale rows; flattened interorbital region; and highly protrusible mouth with papillose lips (Boschung and Mayden 2004). In spite of the wide range and conspicuous nature of H. etowanum, little is known of its biology. Information regarding reproduction is restricted to the collection of a nuptial female by Burr (1979) during late spring in a fast-flowing trough of the Chattahoochee River at 19 ºC water temperature. Etnier and Starnes (1993) reported that lengthfrequency data suggested H. etowanum have a maximum age of at least 5 years. The primary purpose of this study is to elucidate some of the aspects of the life history of H. etowanum. Study Area The study area encompassed Shoal and Moore creeks upstream of their confluence (34.3240°N, 84.5636°W), near Waleska in Cherokee County, 1Department of Biology, Reinhardt College, Waleska, GA 30183-2981. *Corresponding author - SLP@reinhardt.edu. 480 Southeastern Naturalist Vol. 6, No. 3 GA (Fig. 1). Shoal Creek is a typical upland fourth-order tributary of the Etowah River. Near the mouth of Moore Creek, Shoal Creek is between 5.3 and 9.8 m wide and less than 1.5 m deep at normal flows. Substrate is primarily gravel to cobble with sporadic bedrock in riffles, gravel to sand in runs, and sand and silt in pools. At its mouth, Moore Creek is a second-order stream between 3.1 and 6.4 m wide and less than 1.0 m deep at normal flows. Substrate is similar to that of Shoal Creek. Most H. etowanum collected during this study were taken from run and flowing-pool habitats. Upstream of their confluence, both watersheds are mostly forested with moderate agricultural use and sparse residential development. Water temperatures during collections ranged from 5 °C in December and January to 26 °C in July. Species richness of fishes within the study reach is relatively high, with 34 species representing nine different families collected during this study (Table 1). Of these, only Lepomis auritus and Perca flavescens appear to be nonindigenous (Boschung and Mayden 2004). Figure 1. Map of Hypentelium etowanum (Alabama Hog Sucker) study area in Shoal and Moore creeks upstream of their confluence (34.3240°N, 84.5636°W), near Waleska in Cherokee County, GA. 2007 C.T. O'Kelley and S.L. Powers 481 Methods Hypentelium etowanum and associated species were collected over a one-year period spanning from August 2004 to July 2005 by monthly sampling during daylight hours near the end of each month using a 3.3 m x 1.3 m Table 1. Fishes collected from Moore and Shoal creeks within study area between August 2004 and July 2005. Scientific name Common name Petromyzontidae Ichthyomyzon gagei Hubbs and Trautman Southern Brook Lamprey Clupeidae Dorosoma cepedianum (Lesueur) Gizzard Shad Cyprinidae Campostoma oligolepis Hubbs and Green Largescale Stoneroller Cyprinella callistia (Jordan) Alabama Shiner Cyprinella trichroistia (Jordan and Gilbert) Tricolor Shiner Cyprinella venusta Girard Blacktail Shiner Luxilus chrysocephalus Rafinesque Striped Shiner Notemigonus crysoleucas (Mitchill) Golden Shiner Notropis chrosomus (Jordan) Rainbow Shiner Notropis stilbius (Jordan) Silverstripe Shiner Notropis xaenocephalus (Jordan) Coosa Shiner Phenacobius catostomus Jordan Riffle Minnow Semotilus atromaculatus (Mitchill) Creek Chub Catostomidae Hypentelium etowanum (Jordan) Alabama Hog Sucker Moxostoma duquesnei (Lesueur) Black Redhorse Moxostoma erythrurum (Rafinesque) Golden Redhorse Ictaluridae Ameiurus melas (Rafinesque) Black Bullhead Noturus leptacanthus Jordan Speckled Madtom Fundulidae Fundulus stellifer (Jordan) Southern Studfish Cottidae Cottus bairdii Girard Mottled Sculpin Cottus carolinae (Gill) Banded Sculpin Centrarchidae Lepomis auritus (Linnaeus) Redbreast Sunfish Lepomis cyanellus Rafinesque Green Sunfish Lepomis macrochirus Rafinesque Bluegill Micropterus coosae Hubbs and Bailey Redeye Bass Micropterus punctulatus (Rafinesque) Spotted Bass Pomoxis annularis Rafinesque White Crappie Pomoxis nigromaculatus (Lesueur) Black Crappie Percidae Etheostoma scotti Bauer, Etnier, and Burkhead Cherokee Darter Etheostoma stigmaeum (Jordan) Speckled Darter Perca flavescens (Mitchill) Yellow Perch Percina kathae Thompson Mobile Logperch Percina nigrofasciata (Agassiz) Blackbanded Darter Percina palmaris (Bailey) Bronze Darter 482 Southeastern Naturalist Vol. 6, No. 3 seine and a Smith-Root Model 24 backpack electrofisher. A total of 184 H. etowanum was collected, preserved in 10% formalin, rinsed with water, and transferred into 70% EtOH for long-term storage. Specimens were accessioned into the University of Alabama Ichthyological Collection (UAIC 14729-14740). Observations for spawning behavior of H. etowanum were attempted by snorkeling and bank observation during March, April, May, and June, but no spawning activity was observed. Standard length (SL) of each specimen was measured using digital calipers and recorded in mm. Specimens were blotted dry, and total weight (TW), eviscerated weight (EW), and gonad weight (GW) were measured using a digital analytical balance and recorded to the nearest 0.001 g. Standard length and EW were plotted against month to provide length- and weight-frequency distributions to illuminate age and growth information. Pearson product moment correlation coefficients were calculated, and regressions by least sum of squares were performed for SL with EW and SL with the natural log of EW. Sexual size dimorphism was tested using a two-sample t-test. According to Raney and Lachner (1946), H. nigricans from New York form annuli on scales in the spring. Generally following Raney and Lachner (1946), scales (n = 3) were removed from the dorsolateral region of specimens collected in April and the two largest specimens collected during this study (185 and 190 mm SL) and examined for corroboration of length- and weight-frequency distributions. While aging fishes using scales may be imperfect, it provides another line of evidence in age and growth studies and in conjunction with length- and weight-frequency distributions, provides a clearer picture of fish biology (see Summerfelt and Hall 1987). Specimens less than 12 months of age were counted as age 0+, specimens 12–23 months were counted as age 1+, specimens, 24–35 months were counted as age 2+, specimens 36–47 months were counted as 3+, specimens greater than 47 months were counted as 4+. Proportion of total specimens collected represented by each age class was calculated to approximate the age-class makeup of the population studied. Gonadosomatic index (GSI) was calculated for all specimens by dividing GW by EW. One-way analysis of variance was performed to detect differences in mean GSI from different months. In gravid females, ova were enumerated, and diameters of five representative ova were measured to the nearest 0.01 mm. The anterior third of the gastrointestinal track was dissected, and its contents were removed and weighed using a digital analytical balance and recorded to the nearest 0.001 g. One-way analysis of variance was performed to detect differences in mean weight of stomach contents from different months. Pearson product moment correlation coefficients (r) were calculated, and regressions by least sum of squares were performed for EW and weight of stomach contents, EW and variety of stomach contents, and EW and proportion of stomach contents as Chironomidae larvae to investigate influence of size on feeding. Food items were identified to the lowest practical taxon following Thorp and Covich (1991) and Merritt and Cummins (1996) and enumerated. Due to mastication by pharyngeal teeth, most stomach contents were not identifiable below 2007 C.T. O'Kelley and S.L. Powers 483 family, order, or sometimes class. All statistical analyses were executed using Data Desk 6.0 (Data Description, Inc., Ithaca, NY) with alpha for all tests equal to 0.05. Standard deviation is abbreviated as SD. Results Age and growth The smallest specimen collected was a female 34.58 mm SL and 0.942 g TW taken in December. The largest specimen collected was a female 190 mm SL and 132 g TW taken in September. The August collection was the earliest capture of young-of the-year specimens, which ranged from 42.03 to 58.95 mm SL (mean = 44.1, SD = 2.75). Scales from the largest specimens (185–190 mm SL) examined contained four annuli each, while the smallest specimens examined (43.08–59.23 mm SL) each contained a single annulus located at the edge of the scale. The ratio of females to males collected was 1.75:1, and no sexual size dimorphism was detected, with mean SL for females and males 74.6 and 74.9 mm respectively (p = 0.94). Standard length increased with age in months (R2 = 90.6%, p < 0.001). The natural log of EW and SL had a higher correlation (r = 0.974) than EW and SL (r = 0.924) indicating a curvilinear relationship with the natural log of EW increasing with SL (R2 = 95.8%, p < 0.001). Mean SL and EW by month are presented in Table 2 and Figures 1 and 2. Of the 184 specimens collected, 48.4% were age 0+, 33.2% were age 1+, 13.0% were age 2+, 4.4% were age 3+, and 1.1% were age 4+. Figure 2. Standard length in mm ± one standard deviation by age in months for Hypentelium etowanum (Alabama Hog Sucker) collected from Moore and Shoal creeks between August 2004 and July 2005. 484 Southeastern Naturalist Vol. 6, No. 3 Diet Diptera were most prevalent within H. etowanum stomachs, making up 90.6% of all food items. Chironomidae larvae made up 88.8% of all food items and were contained in stomachs from every month. The remainder of the Diptera were unidentifiable pupae or adults. Other food items are listed in Table 3. Of all stomachs examined, 35.9% were empty. Weight of stomach contents was not uniform across all months (F = 3.29, p < 0.001), with overall feeding peaking in April. The greatest variety of food items (n = 14) and mean weight (0.032 g, SD = 0.061) of stomach contents was also highest in April. Feeding appeared to be lowest during the winter months of December– February, as indicated by small numbers of items per stomach and high frequency of empty stomachs (Table 3). All stomachs from individuals Table 2. Age in months, standard lengths (SL) in mm and eviscerated weights (EW) in g of Hypentelium etowanum from Moore and Shoal creeks by age in months from August 2004 to July 2005. Age N Mean SL SD Mean EW SD 3 4 44.10 2.75 1.35 0.26 4 8 47.75 4.90 1.83 0.48 5 9 48.57 6.70 2.09 0.90 6 9 42.96 3.95 1.53 0.40 7 12 43.50 7.40 1.46 0.80 8 10 48.45 7.33 1.95 0.86 9 10 45.47 7.53 1.71 0.82 10 14 46.92 5.58 1.80 0.59 11 13 51.66 6.93 2.38 0.94 12 8 71.48 6.24 6.09 1.40 13 24 75.98 9.65 7.52 2.63 14 9 74.14 8.36 6.99 2.71 15 1 58.95 - 2.93 - 17 3 91.01 7.59 12.25 3.02 18 3 88.56 11.18 12.59 6.45 20 3 101.5 18.65 16.91 6.93 21 3 95.76 20.37 15.10 8.51 22 4 100.62 9.55 18.34 7.07 23 3 104.17 13.14 18.71 4.89 24 5 119.75 3.83 30.01 3.22 25 1 130.84 - 38.32 - 26 3 123.02 9.03 29.08 5.28 27 2 123.93 5.58 30.28 4.54 28 4 126.12 10.54 32.98 6.70 29 3 125.67 11.99 29.47 8.04 30 2 125.45 4.67 31.86 2.75 34 1 135.39 - 36.57 - 35 3 139.11 2.83 47.72 5.63 36 2 141.06 0.76 50.13 1.34 37 2 149.67 8.71 59.89 11.81 38 2 146.11 7.57 53.05 8.41 42 1 145.07 - 50.11 - 47 1 185 - 91.27 - 52 2 187.50 3.54 104.45 14.92 2007 C.T. O'Kelley and S.L. Powers 485 Table 3. Stomach contents of Hypentelium etowanum from Moore and Shoal creeks by month from August 2004 to July 2005. Month Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total % of total # of stomachs 13 13 19 20 15 27 14 8 14 15 14 12 184 Detritus 1 1 10 6 6 2 7 1 34 1.14 Nematoda 5 5 0.17 Mollusca Corbicula 1 1 0.03 Annelida Oligochaeta 2 2 0.07 Hirudinae 1 7 14 22 0.74 Arachnida Hydrachnida 4 1 6 3 3 15 32 1.07 Crustacea Branchiopoda 1 33 8 5 4 31 15 10 107 3.59 Insecta Unidentified parts 2 5 6 6 2 1 4 5 2 33 1.11 Ephemeroptera 3 3 1 1 1 1 10 0.34 Plecoptera 23 23 0.77 Coleoptera 1 1 1 3 0.10 Hymenoptera 1 1 0.03 Trichoptera 4 3 1 8 0.27 Diptera Chironomidae larvae 4 2 556 770 717 47 187 64 111 45 140 3 2646 88.79 Unidentified pupae 2 21 8 7 1 1 40 1.34 Unidentified adults 6 2 2 3 13 0.44 Number empty 7 12 1 2 2 16 5 2 8 11 66 Total items 6 4 615 858 744 79 211 70 164 69 157 3 2980 Items/stomach 0.462 0.308 32.37 42.9 49.6 2.926 15.07 8.75 11.71 4.6 11.21 0.25 % empty 53.85 92.31 5.263 10 13.33 59.26 35.71 0 0 13.3 57.14 91.7 486 Southeastern Naturalist Vol. 6, No. 3 collected during winter contained less than four food items, and the contents of only a single stomach were great enough to register on the balance (0.002 g). The correlation between EW and weight of stomach contents (r = 0.337) was significant (p < 0.001), but had a low R2 of 11.4%. The correlation between EW and variety of stomach contents was low (r = 0.114) and not significant (R2 = 1.3%, p = 0.229). The proportion of stomach contents as Chironomidae larvae was inversely correlated with EW (r = -0.276) and significant (p = 0.004), but had a low R2 of 7.6%. Reproduction Individual GSI peaked in spring, with values greater than 0.1 only in specimens from March and April. The highest GSI for a single individual was 0.1423 in a female 185 mm SL from April (Fig. 3). Mean GSI did not differ significantly among months (F = 1.69, p = 0.079). The two months with the highest mean GSI were April (0.0169, SD = 0.0320) and September (0.0174, SD = 0.0193). June, July, and August had low mean GSI values of 0.0047 (SD = 0.0029), 0.0039 (SD = 0.0022), and 0.0043 (SD = 0.0051), respectively. The lowest mean GSI for a month was from December (0.0015, SD = 0.0022). Mature eggs were present only in specimens collected in March, April, and May, and ranged from 1.5 to 2.8 mm in diameter. Ova ranged between 493 and 2717 (mean = 1475.5, SD = 932.28) in number in a single mature female. The smallest female examined with mature ova was 24 months in age (124.5 mm SL, 34.53 g EW) and the smallest male with mature testes was 22 months in age (114.4 mm SL, 28.45 g EW). Figure 3. Eviscerated weight in g ± one standard deviation by age in months for Hypentelium etowanum (Alabama Hog Sucker) collected from Moore and Shoal creeks between August 2004 and July 2005. 2007 C.T. O'Kelley and S.L. Powers 487 Discussion Age and growth Hypentelium etowanum appear to grow rapidly in April as indicated by length and weight increases at approximately 12, 24, and 36 months of age (Figs. 2 and 3). Scales examined for this study also suggest annuli form during spring, but due to the mild winters in Georgia, they may not be as well defined as those observed in H. nigricans by Raney and Lachner (1946). The largest H. etowanum examined (185–190 mm SL) all had four annuli indicating, along with length and weight frequencies, at least four or five different age classes in our samples. This is largely consistent with the hypothesis of Etnier and Starnes (1993) that Hypentelium etowanum live to five years or more as no specimens examined during this study approached the maximum recorded size of 254 mm SL for the species (Boschung and Mayden 2004). The low proportion of age 3+ and 4+ specimens suggests that very few individuals survive to the maximum age, as is typical of most fishes (Matthews 1998). However, the low number of older specimens collected may be due in part to the difficulty collecting larger specimens using a 3.3 m x 1.3 m seine and a backpack electrofisher. Diet Increased feeding during the spring also appears to coincide with increased energetic requirements associated with gamete production and Figure 4. Maximum Gonadosomatic Index of Hypentelium etowanum (Alabama Hog Sucker) from Moore and Shoal creeks by month from August 2004 to July 2005 (1 = January, 2 = February, etc.). 488 Southeastern Naturalist Vol. 6, No. 3 spawning. The prevalence of Chironomidae in stomachs may indicate selective feeding by H. etowanum, but may also be explained by the extremely high density that chironomids (> 20,000 individuals/m2) often reach in the substrate of sandy runs and flowing pools (Benke et al. 1984), which appear to be among the more regularly inhabited microhabitats for H. etowanum. The inferior mouth placement in H. etowanum suggests that feeding would most likely occur at or near the substrate as is typical of most Catostomidae (Matthews 1998). The weak correlations between EW and weight of stomach contents, and EW and proportion of diet as Chironomidae may suggest that feeding of H. etowanum increases slightly and shifts away from Chironomidae as individuals get larger. However, these correlations do appear to be weak, and there is no evidence of a shift in variety of stomach contents throughout the life of H. etowanum. Thus, it would seem that any changes in diet associated with size are not dramatic. Reproduction The inability to detect differences in monthly mean GSI is likely due to the high proportion of juveniles collected during this study. Highest individual GSI values during spring months indicate spawning most likely occurs in late April to May (Fig. 4). While mean GSI for females was highest in September, no large (> 1.5 mm) mature ova were present in any specimens collected in the fall. All ova from summer, fall, and winter months were latent or maturing (see Heins and Machado 1993). The restriction of large (> 1.5 mm) mature ova to specimens collected in March, April, and May suggest a single spring spawning season despite the highest mean GSI from fall months. Tubercles also first appeared in age-two specimes from February, peaked in April, and were completely absent by July. This pattern of tubercle development is consistent with observations by Etnier and Starnes (1993) and Boschung and Mayden (2004). Burr (1979) observed spawning of H. etowanum in the upper Chattahoochee River on 10 and 11 June 1976 in water 19 °C. The water temperature of the April, May and June collections for this study were 15 °C, 16 °C, and 25 °C, respectively. This appears largely consistent with the findings of Burr (1979) suggesting spawning occurs mostly likely from late April to early June as water temperature approaches 20 °C. No spawning activity was observed, but most specimens collected for this study were from habitats similar to that described by Burr (1979). Examinations of gonads, length and mass frequency, and scale circuli indicated that sexual maturity occurs by three years of age, as mature gonads were observed only in specimens at two years of age or greater. Comparison to other species of Hypentelium The biology of H. etowanum is similar to that of the two other species of Hypentelium and appears to be intermediate between the others in many lifehistory aspects. Hypentelium etowanum shares a similar lifespan with H. 2007 C.T. O'Kelley and S.L. Powers 489 roanokense Raney and Lachner (Roanoke Hog Sucker) despite the much smaller maximum size (100 mm SL) of the latter (Jenkins and Burkhead 1994). The largest of the three species (􀂧 495 mm SL), H. nigricans appears to be much more long-lived than the others, reaching a maximum age of 11 years (Raney and Lachner 1946). Our data from H. etowanum are largely consistent with the findings of Raney and Lachner (1946) that rapid growth occurs in H. nigricans during spring as evidenced by the formation of annuli near the edge of scales from mid April to late May. The diet of Hy. etowanum appears similar to that of H. nigricans and H. roanokense, as all appear to feed mostly on Chironomidae larvae living in the substrata of streams. Jenkins and Burkhead (1994) also suggested that a slight dietary shift away from aquatic insect larvae may occur in older H. nigricans similar to that suggested by the weak negative correlation between EW and proportion of stomach contents as Chironomidae found in this study. All three Hypentelium species appear to reach sexual maturity at about three years of age with males sometimes maturing a year earlier in H. nigricans and two years earlier in H. roanokense. We did not detect a difference in age at maturity between males and females for H. etowanum. 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