Cottus specus Adams and Burr,, 2013

Adams, Ginny L., Burr, Brooks M., Day, Julie L. & Starkey, David E., 2013, Cottus specus, a new troglomorphic species of sculpin (Cottidae) from southeastern Missouri, Zootaxa 3609 (5), pp. 484-494 : 488-493

Cottus specus Adams and Burr, new species

Grotto Sculpin

Figure 4

Holotype. SIUC 88001, male, 80.2 mm SL, Mystery Cave, Perry County, Missouri 18 January 2012.

Paratypes. Missouri. Perry County. SIUC 88002 (2, 58.0– 60.5 mm SL), USNM 409781 (2, 65.3–86.7 mm SL) taken with holotype.

Additional materials (nontypes).

Missouri: Perry County: SIUC 19279 (20, 66– 103 mm SL) Cinque Hommes Creek, 1992. SIUC 18916 (3) Sculpin Stream, Mystery Cave, 21 April 1991. SIUC 19904 (3) Mystery Cave, 7 March 1992. SIUC 18923 (20, 52– 80 mm SL), Mystery Cave, 1 October 1991. SIUC 21258 (4, 57– 88 mm SL) Hot Caverns, 4 October 1992. SIUC 19839 (23, 51– 95 mm SL) Flaming River Cave, 3 July 1992. SIUC 21260 (8, 34– 56 mm SL) Running Bull Cave, 25 October 1992. SIUC 20916 (9, 31– 80 mm SL) Tom Moore Cave, 25 October 1992.

GenBank accession numbers for haplotypes.

Haplotype GR1 ( KC172892 ), Haplotype GR2 ( KC172893 ), Haplotype MID1 ( KC172894 ), Haplotype MID2 ( KC172895 ), Haplotype BR1 ( KC172896 ), Haplotype BR2 ( KC172897 ).

Diagnosis. Cottus specus is diagnosed from all other described members of the genus Cottus , except C. carolinae , Cottus chattahoochee , Cottus confusus , Cottus hubbsi , and some populations of Cottus beldingii by the complete lateral line ending near the base of the caudal fin and dorsal fins not usually connected. Cottus specus only occurs geographically adjacent to C. carolinae and can be distinguished by a reduction in eye size: 1–5% SL in 98% of specimens (1–4% in 85% of specimens) versus eye size 5–9% of SL in 100% of specimens ( Table 3 ). Using ANCOVA, only two individuals (<1%) overlapped in eye size between C. specus and C. carolinae when standard length was accounted for in the regression. Cottus specus exhibited a significant increase in cephalic lateralis pore size: 92% above 500 mm compared to 100% of C. carolinae between 200–500 mm; ANCOVA, P <0.001; Table 4 .

Description. Cottus specus is a moderate-sized species of the genus Cottus ; the largest specimen examined is 104 mm SL. Typical body shape is illustrated in Figure 4 . Frequency distribution of percent eye length as a function of standard length, pelvic fins and lateral-line pore sizes are given in Tables 3–5 . Additional information on morphology can be found in Burr et al. (2001).

Anal-fin rays 13, occasionally 12 or 14, dorsal-fin spines 7–8; dorsal-fin rays 16–18, usually 17–18; pectoralfin rays 14–17, usually 16; pelvic-fin rays 3–4, with a high degree of asymmetry; branched caudal-fin rays 9; lateral-line pores 32–36, modally 35; infraorbital pores 8–9, modally 9; preoperculomandibular pores 10–12, modally 11, post-maxillary pore present; median chin pores 2, rarely 1; enlarged mandibular pores 3, 4 and 6 ( Burr et al. 2001).

Several studies have found evidence of asymmetry in eye size in slightly to moderately microthalmic cave species ( Wilkens 2001; Pouilly & Miranda 2003); however, we found no evidence of asymmetry in the eyes of C. specus . Eye volume, eye lens and dermal cornea of the eye were also significantly reduced in C. specus when compared to C. carolinae . Along with a decrease in eye size, mean lens diameter in C. specus was 50 to 70% smaller than mean lens diameter in C. carolinae samples. Twelve individual C. specus (of 31) were missing the lens in either one or both eyes.

A high degree of variability was seen in the general structure of the retina within cave populations. The overall size of the eye was markedly reduced in the cave populations along with a corresponding decrease in the size of the lens. Eye volume varied significantly among habitats (ANOVA, F5,71, P <0.001) with C. specus in caves exhibiting a significantly reduced eye size compared to C. specus in resurgence streams and C. carolinae . Cottus specus in resurgence streams had an intermediate eye volume that was significantly different from C. carolinae . No asymmetry was detected in eye length within any habitat type. Greatest length of the dermal cornea was also significantly reduced in C. specus compared to resurgence and surface sculpins (ANOVA, F2,71 = 14.82, P <0.0001).

There is a high degree of variability in pigmentation in C. specus with some individuals lacking all apparent pigmentation in both the fins and on the body and others approaching the banding pattern of the dorsal saddles found in C. carolinae . Individuals with darker pigmentation are primarily found in the surface resurgence stream; however, high variability exists at every site examined.

Etymology. The specific epithet specus refers to a cave or cavern in reference to the primary habitat in caves. The common name, Grotto Sculpin, also refers to the cave habitat.

Distribution. Cottus specus is distributed in tributaries of the Bois Brule River drainage including Cinque Hommes Creek and Blue Spring (which is the resurgence stream for the Moore Cave system) and has never been collected in the Bois Brule mainstem ( Fig. 2 ). The caves and the surface streams are direct tributaries of the Mississippi River through the Bois Brule River. Cottus specus can be found in cave streams as well as their resurgences, primarily over gravel, cobble, or bedrock bottom. Cottus specus is the only Cottus present throughout its distribution. It is not found in caves in nearby drainages ( Burr et al. 2001).

Reproduction. We have found nests of C. specus in Perry County caves during December, but reproduction is thought to occur as late as February-March for sculpins residing in Cinque Hommes Creek as judged from the presence of yolk-sac larvae and a single nest (pers. obs.). In some years, there may be two nesting periods separated by one to two months within the cave systems. Nests, guarded by a single male, are found under cobble or pebble substrate. Eggs are adhesive, in a clump, and are attached to the underside of a rock. Males guarding rocks may have enlarged knobs on the dorsal fins (similar to those described for Cottus by Kinziger & Wood 2010) and have darker pigmentation on the lips and head ( Fig 5 ).

Conservation status. We consider Cinque Hommes Creek sculpins (surface and resurgence) to be C. specus because they share similar morphological characteristics and haplotypes with both the northern and southern cave systems. High gene flow, possibly due to migration of nesting individuals upstream, between Cinque Hommes Creek and surrounding cave streams may have resulted in an intermediate population. It is also possible that sculpins colonized Cinque Hommes Creek from the northern caves after extirpation of the surface population (secondary colonization) or due to a lack of sculpins in Cinque Hommes Creek prior to colonization by C. specus (indicating initial colonization of the caves north of Cinque Hommes occurred through another route).

Presence of a troglomorphic species distinct from C. carolinae in Perry County may be the result of the extensive cave systems and relative isolation of related drainages due to the Mississippi River barrier, similar to Gammarus minus populations discussed in Culver and Wilkens (2000). Intermediate Cinque Hommes Creek sculpin may reflect the historical tendency of sculpin in Cinque Hommes Creek to move upstream into caves and springs to spawn, thus creating a high degree of interconnectedness of the respective populations.

Cottus specus is restricted to five cave systems and their corresponding resurgence streams in the Bois Brule drainage. Over the past fifteen years, two of the cave locations (Running Bull Cave and Mystery Cave) have experienced mass mortalities of unknown origin. Although both populations appear to have recovered from the perturbations, recent research provides evidence of pervasive and widespread contamination of C. specus habitat by a mixture of bioaccumulative organic contaminants ( Fox et al. 2010). The presence of karst terrain throughout the range of C. specus exacerbates the concern. Direct pathways for contaminants into the cave systems through sinkholes could lead to future extirpations ( Burr et al. 2001). Given the unique habitat requirements and morphological distinctiveness of C. specus , it is imperative that future studies further delineate drainage basins and potential sources of contaminants.

Cottus specus is typically found at abundances significantly lower than those reported for C. carolinae throughout their range and based on mark-recapture may be found at densities less than 0.06 individuals/m2, an order of magnitude lower than that of C. carolinae ( Greenberg and Holtzman 1987, Burr et al. 2001). Low densities may limit the ability of populations to recover from anthropogenic disturbances.

Discussion. The addition of C. specus brings the total number of recognized species of Cottus to 33 in North American fresh waters ( Kinziger & Wood 2010; Page & Burr 2011). The cave populations of the new species described here are more recognizable morphologically than most other species in the genus. Only two other reports of Cottus have been recorded to show troglomorphic traits in a cave environment ( Williams & Howell 1979; Espinasa & Jeffery 2003). Cottus specus eye size was smaller than that reported for the troglomorphic sculpin from Pennsylvania, which had a mean eye size of 5.7% SL ( Espinasa & Jeffery 2003). In addition, potential hybridization with a surface population may increase variation and asymmetry in the troglomorphic Sculpin from Pennsylvania compared to Cottus specus .

Species of Cottus are generally common to abundant in suitable habitat. Three species are protected in Canada as threatened, and the United States considers only one species, Cottus paulus (Pygmy Sculpin) , as threatened (restricted to Coldwater Spring, Alabama), none as endangered. Cottus echinatus (Utah Lake Sculpin) is an extinct species that occurred in Utah Lake, Utah. Cottus specus is known only from 5 caves and one stream in a single county in Missouri. Its tiny range and known threats (chemical pollution of groundwater) make it one of the rarest and most imperiled sculpins in North America ( Fox et al. 2010). On the basis of small geographic range, low population densities, and a multitude of threats to groundwater habitats, C. specus warrants formal protection at both state and federal levels.

Figures

FIGURE 2. Geographic distribution of sampling localities and drainage relationships in the Bois Brule drainage with caves overlaid. Abbreviations as in Table 1; HC (Hot Caverns) is part of Rimstone River Cave system, and ME (Mertz) is part of Crevice Cave system.

FIGURE 4. Cottus specus (A) 80.2 mm SL, holotype, SIUC 88001; (B) male, 66.8 mm SL; (C) 74.5 mm SL showing variation in eye size and pigmentation.

FIGURE 5. Increased pigmentation on the lips and head (A) and presence of fin-knobs (B) on a male Cottus specus (69.8 mm SL).

Tables

TABLE 3. Frequency distribution of percent eye length of standard length in Cottus carolinae and Cottus specus. Apple Creek specimens were taken from Perry and Cape Girardeau counties in Missouri, and Big Creek specimens were collected from Union County, Illinois.

Eye Length/SL
Species, System	1	2	3	4	5	6	7	8	9	N
Holotype, C. specus		1
Cottus carolinae
Apple Creek, MO					14	10				24
Big Creek, IL					5	35	15	6	1	62
Cottus specus
Cinque Hommes	14	34	55	82	38	2				225
Crevice Cave			2	4	10	2				18
Rimstone River Cave	3		8	24	1					36
Mystery Cave	20	63	64	36	26	6				215
Running Bull Cave	26	26	13	7	1					73
Moore Cave			4	11	1					16

TABLE 4. Frequency distribution of cephalic lateralis pore 3 lengths in Cottus carolinae and Cottus specus. Apple Creek specimens were taken from Perry and Cape Girardeau counties in Missouri, Bay Creek from Pope County, Illinois, Collier Spring in Monroe County, Illinois, and Big Creek in Union County, Illinois.

Pore Size
Species, System	200	300	400	500	600	700	800	> 900	N
Cottus carolinae
Apple Creek, MO	5								5
Bay Creek, IL	1	3	1						5
Collier Spring, IL		2	6						8
Big Creek, IL	1	2	3						6
Midlands	4	2	7						13
Cottus specus
Cinque Hommes		1	1	1	4	2	2	2	13
Crevice Cave			2		1	2	1	1	7
Rimstone River					1	2	3	4	10
Mystery Cave				1	1	1	2	4	9
Moore Cave			1		3	4	2		10