Transactions of the American Society 129:811±826, 2000 ᭧ Copyright by the American Fisheries Society 2000

Gulf Spawning Migration and Habitat in the Choctawhatchee River System, ±

DEWAYNE A. FOX North Carolina Cooperative Fish and Wildlife Research Unit, Department of Zoology, North Carolina State University, Raleigh, North Carolina, 27695-7617, USA

JOSEPH E. HIGHTOWER* North Carolina Cooperative Fish and Wildlife Research Unit, U.S. Geological Survey, Biological Resources Division, Department of Zoology, North Carolina State University, Raleigh, North Carolina, 27695-7617, USA

FRANK M. PARAUKA U.S. Fish and Wildlife Service, Field Of®ce, 1612 June Avenue, Panama City, Florida 32405, USA

Abstract.ÐInformation about spawning migration and spawning habitat is essential to maintain and ultimately restore populations of endangered and threatened species of anadromous ®sh. We used ultrasonic and radiotelemetry to monitor the movements of 35 adult oxyrinchus desotoi (a subspecies of the A. oxyrinchus) as they moved between and the Choctawhatchee River system during the spring of 1996 and 1997. Histological analysis of gonadal biopsies was used to determine the sex and reproductive status of individuals. Telemetry results and egg sampling were used to identify Gulf sturgeon spawning sites and to examine the roles that sex and reproductive status play in migratory behavior. Fertilized Gulf sturgeon eggs were collected in six locations in both the upper Choctawhatchee and Pea rivers. Hard bottom substrate, steep banks, and relatively high ¯ows characterized collection sites. Ripe Gulf sturgeon occupied these spawning areas from late March through early May, which included the interval when Gulf sturgeon eggs were collected. For both sexes, ripe ®sh entered the Choctawhatchee River signi®cantly earlier and at a lower water temperature and migrated further upstream than did nonripe ®sh. Males entered the Choctawhatchee River at a lower water temperature than females. Results from histology and telemetry support the hypothesis that male Gulf sturgeon may annually, whereas females require more than 1 year between spawning events. Upper river hard bottom areas appear important for the successful spawning of Gulf sturgeon, and care should be taken to protect against habitat loss or degradation of known spawning habitat.

The Atlantic sturgeon the Gulf States Marine Fisheries Commission comprises two disjunct subspecies along the At- 1995). lantic and Gulf coasts: the form, Historically, Gulf sturgeon supported substan- A. o. desotoi (hereafter referred to as Gulf stur- tial commercial and limited sport ®sheries in Flor- geon) and the allopatric East Coast form, A. o. ida (U.S. Commission of Fish and Fisheries 1902; oxyrinchus (hereafter referred to as Atlantic stur- Burgess 1963; Smith and Clugston 1997). Overall, geon). Gulf sturgeon have one of the southernmost commercial ®sheries showed many signs of over- distributions of sturgeon worldwide (Bemis and exploitation. Catches declined rapidly in most ar- Kynard 1997). Historically, Gulf sturgeon ranged eas, and in 1984 the state of Florida ended harvest throughout the Gulf of Mexico from Louisiana to in all state waters. This was followed in 1991 by Charlotte Harbor, Florida. However, populations Federal designation of Gulf sturgeon as a threat- have been severely reduced or extirpated through- ened species. In an effort to prevent future declines out much of their range and present distribution is and to bolster the current Gulf sturgeon population from east of the Mississippi River to the Suwannee levels, the U. S. Fish and Wildlife Service and the River, Florida (U.S. Fish and Wildlife Service and Gulf States Marine Fisheries Commission com- pleted a Recovery/ Management Plan for the subspecies. The plan identi®ed a need to collect * Corresponding author: [email protected] information on Gulf sturgeon habitat requirements Received December 22, 1998; accepted December 27, 1999 (U.S. Fish and Wildlife Service and the Gulf States

811 812 FOX ET AL.

Marine Fisheries Commission 1995). This plan collection of fertilized eggs (Kempinger 1988; speci®cally the need for information regard- LaHaye et al. 1992). Sturgeon eggs in benthic ®sh ing the location, timing, and characteristics of es- intestines have been used to identify spawning sential spawning habitat. Recently, genetically dis- sites for the Chinese sturgeon A. sinensis (Zhong- tinct subunits of Gulf sturgeon were identi®ed Ling and Yan 1991). Atlantic sturgeon spawning throughout the Gulf of Mexico (Stabile et al. sites have been identi®ed by use of telemetry, cap- 1996); therefore, efforts must be taken to examine ture of larvae, collection of ripe individuals, and spawning habitat and life history characteristics analysis of reproductive hormones and metabolites within individual river systems. (Dovel and Berggren 1983; Van Eenennaam et al. Early efforts to delineate Gulf sturgeon spawn- 1996). ing locations were largely unsuccessful. Sampling Our primary objective was to delineate probable for eggs and larvae of Gulf sturgeon in the Su- spawning sites for Gulf sturgeon in the Choctaw- wannee River with 1-m plankton nets stationed hatchee River system of Alabama and Florida. This near the bottom produced neither, in spite of con- objective was to be addressed by tracking radio- siderable sampling (Huff 1975). In the Apalachi- tagged ®sh during the spawning season and by cola River, Florida, some incidental information deploying egg collectors in areas where telemetry on the location of spawning sites was derived by evidence indicated that adult ®sh were present. A the capture of three Gulf sturgeon larvae (Wooley secondary objective was to examine the role of et al. 1982). Recent efforts to delineate Gulf stur- sex and reproductive status on movement patterns geon spawning habitat have relied primarily on and habitat selection. arti®cial substrates to collect eggs (Marchant and Shutters 1996; Sulak and Clugston 1998). Over a Study Area 2-year period, collection of fertilized Gulf stur- The Choctawhatchee River originates in south- geon eggs at four discrete locations in the Suwan- eastern Alabama and ¯ows southward approxi- nee River provided the ®rst information regarding mately 280 km through Florida, eventually emp- the speci®c location and timing of spawning for tying into Choctawhatchee Bay (Figure 1). The this species (Marchant and Shutters 1996). These Choctawhatchee River drains a watershed in ex- ®rst insights provided a necessary starting point cess of 12,000 km2 and has an average discharge for more detailed studies. Recently, the collection of 198 m3/s, which makes it the third largest river of large numbers of eggs and detailed habitat char- in Florida (Bass et al. 1980). The watershed is acteristics of three Gulf sturgeon spawning loca- mostly agricultural or forested and has relatively tions has provided substantial new detail regarding low levels of urbanization, especially in the head- habitat characteristics within the waters. The Choctawhatchee River lacks a main- (Sulak and Clugston 1998; K. Sulak, U.S. Geo- stem impoundment, which makes it unique com- logical Survey-Biological Resources Division, pared with most other historical Gulf sturgeon riv- personal communication). ers. Two major tributaries contribute to the Choc- A combination of approaches have been used to tawhatchee River, the in the northern identify spawning sites for other sturgeon. Col- portion of the watershed and Holmes Creek, which lections of eggs and larvae with arti®cial sub- is the major tributary in Florida. The Pea River is strates, plankton nets, and beam trawls, combined located almost entirely within Alabama, and there with observations of spawning activity, have pro- is a run-of-the-river dam on the Pea River at river vided information regarding the spawning habitat kilometer (rkm) 191. requirements of white sturgeon A. transmontanus (McCabe 1990; Parsley et al. 1993; McCabe and Tracy 1994; Schaffter 1997). For shortnose stur- Methods geon A. brevirostrum, movement to and from Netting operations using multiple multi-®lament spawning sites has been characterized with telem- anchored gill nets (91.4±121.9 m long, 20±36 cm etry; the reproductive status of ®sh at hypothesized stretch mesh) were conducted within Choctaw- spawning sites was determined by visual inspec- hatchee Bay during late winter and early spring of tion, release of milt in males and movement pat- 1996 and 1997 (Figure 1). Nets were deployed terns (Buckley and Kynard 1985; Hall et al. 1991; perpendicular to the shoreline to maximize the in- Kieffer and Kynard 1993). Lake sturgeon A. ful- tercept area for migrating ®sh and were checked vescens spawning sites have been identi®ed by di- at 4-h intervals to minimize mortality risk. Sam- rect observation of spawning behavior and by pling was concluded when all transmitters had GULF STURGEON SPAWNING AND HABITAT 813

FIGURE 1.ÐLocation of Choctawhatchee River system and plotted maximum upstream relocation (in river ki- lometers or rkm from the mouth of the river) and reproductive status for individual female Gulf sturgeon for the 1996 and 1997 ®eld seasons. For ®sh captured in 1996 that returned in 1997, reproductive status in 1997 is unknown.

been implanted within ®sh large enough to be sex- taining buffered 10% formalin for histological ually mature (fork length Ͼ1.3 m; Huff 1975). analysis. Captured ®sh were measured (both total length Thirty ®sh received internal radio transmitters and fork length) to the nearest 1 mm and weighed (Advanced Telemetry Systems model 5A) that op- to the nearest 0.5 kg. Fish were placed into an erated at 40 MHz, measured 2.0 ϫ 8.1 cm and anesthetic bath consisting of a 50±100 mg/L mix- weighed 40 g (in air). Transmitters were pro- ture of tricaine methane sulfonate (tradename: MS- grammed with different duty cycles in the 2 years 222) and bay water (Harms and Bakal 1994). To (12-h on±off in 1996 and 24-h in 1997), so all determine the sex and reproductive status of in- transmitters were guaranteed to last throughout the dividual ®sh (Huff 1975; Chapman et al. 1996), a 1997 ®eld season. To decrease signal attenuation, 40-mm incision was made using a surgical scalpel radio transmitter antennas (35.6 cm) exited the on the mid ventral line about 40±60 mm anterior body cavity through a puncture of the lateral body to the insertion of the pelvic ®ns. Upon reaching wall, posterior to the primary incision site, made the peritoneum, a retractor was placed into the by a sterilized large-gauge (8/0) aspiration biopsy surgical area to spread the musculature and enable needle. During 1997, ultrasonic transmitters (Son- a clear view of the area. Gonadal tissue was located otronics model CHP-87-XL, 10.0 ϫ 3.5 cm and with use of a blunt probe. External appearance of 110 g in air, expected battery life 30 months) were the gonad was noted and then a biopsy (1 cm3 also implanted in all ®sh (N ϭ 20) ®tted with radio fragment) was taken using surgical forceps and a transmitters. The ultrasonic tags were used in a scalpel. Each sample was preserved in a vial con- research project to examine Gulf sturgeon estua- 814 FOX ET AL. rine and marine habitat use. In 1997, both radio tempted to locate all tagged ®sh once biweekly and ultrasonic transmitters were coated with Si- until early July. lastic (Dow Corning Products) to reduce the prob- Habitat characterization.ÐOnce the general lo- ability of tag extrusion. cation of a ®sh was determined, a more precise The primary incision was closed using sterile position was estimated based on changes in signal resorbtive suture material. To ensure proper clo- strength using a paper clip, which served as a weak sure, a single interrupted suturing technique was antenna. At each ®sh location, we recorded latitude applied. Surgical glue was placed over the incision and longitude using a hand-held GPS unit. Tem- sites to aid in wound closure and to help secure perature, dissolved oxygen, conductivity, and sa- the tag in place until the wound began to heal. linity were measured at both the surface and bot- Following the application of surgical glue, a thin tom using a YSI multi-meter. A substrate sample layer of petroleum jelly mixed with Betadine was was obtained using a Petite PONAR sampler. Sub- placed over the incision areas to protect against strate samples were qualitatively categorized in the infection. ®eld as either silt, clay, sand, cobble, rock, or de- Five externally mounted radio transmitters also tritus. We also recorded water temperatures once were used to tag additional ®sh during this study. every 2.4 h using a temperature logger at rkm 117 These transmitters (Advanced Telemetry Systems (Figure 1). model 5A, 40 mHz) were programmed with a duty River ¯ow rates were obtained from the U. S. cycle of 9 months on and 3 months off and had a Geological Survey gaging station (02361000) lo- guaranteed tag life exceeding 2 years. External cated at rkm 167 on the upper Choctawhatchee transmitters were attached at the base of the dorsal River near Newton, Alabama (Figure 1). Daily ®n (Carr et al. 1996) using a sterilized large-gauge ¯ow rates were used to examine the interaction (8/0) aspiration biopsy needle. Te¯on-coated at- between ¯ow rates and movement patterns. Egg collection.ÐBecause the primary objective tachment wires were ®tted through the holes and of this project was to identify Gulf sturgeon af®xed in place with a backing plate and crimps. spawning sites, egg samplers were deployed in ar- Gonadal biopsies were collected as described eas where telemetry evidence suggested that ®sh above for all ®sh ®tted with external transmitters. might be spawning (i.e., ripe ®sh maintaining po- To determine reproductive stage, gonadal tissue sition over or moving between hard bottom areas was stained with hematoxylin and eosin. Each in the upper river). Egg samplers (modi®ed from sample was sectioned (3␮), mounted on a glass the design of Marchant and Shutters 1996) con- slide, and then examined using light microscopy. sisted of a red circular ¯oor buf®ng pad (55.9 cm Following Chapman et al. (1996), ®sh were clas- or 68.6 cm in diameter) anchored to the bottom si®ed as either immature, maturing, or ripe. Ac- with welded rebar. Previous results regarding cording to this classi®cation scheme, maturing ®sh spawning locations of Gulf sturgeon (substrate had spawned in a previous year and were between type of rock±cobble and ¯ow patterns of Ͼ1 m/s) spawning events at the time of collection. and other sturgeon species were considered when Telemetry.ÐDuring 1996, searches within the selecting sites for deploying egg samplers (Buck- Choctawhatchee River began 2 d following the ley and Kynard 1985; Marchant and Shutters 1996; release of the ®rst radio-tagged ®sh. During 1997, Bemis et al. 1997; Wei et al. 1997; Sulak and searches in the Choctawhatchee River began in Clugston 1998). Samplers were also positioned in early February in an attempt to document dates of areas where current patterns (i.e., eddies) possibly river entry for returning telemetered ®sh. Because accumulated eggs (Sulak and Clugston 1998). Be- ®sh captured in 1997 were implanted with both cause Gulf sturgeon eggs probably adhere to the radio and ultrasonic transmitters, searches were substrate almost immediately after spawning (Su- conducted biweekly in Choctawhatchee Bay until lak and Clugston 1998), it seems probable that all ®sh had left the bay and entered the Choctaw- eggs collected on the samplers were spawned in hatchee River. All navigable portions of the Choc- close proximity to the collection area. tawhatchee River were searched at least once each Sampling for eggs began when telemetered ripe week in 1996 and biweekly in 1997, until move- ®sh began approaching areas where spawning was ment patterns indicated a probable end to the thought to occur (i.e., upstream hard bottom areas). spawning season (i.e., ripe ®sh moving down to Between 70 and 100 samplers were deployed in the lower portions of the river). In both years, both the Choctawhatchee and Pea rivers and ex- following the end of the spawning season, we at- amined every 24±72 h for the presence of Gulf GULF STURGEON SPAWNING AND HABITAT 815 sturgeon eggs. Hard-bottom areas in the Choctaw- signed as the last day of each weekly interval. hatchee and Pea rivers are discrete in their distri- Individual ®sh were treated as sampling units in bution and tend to be associated with bends or all analyses to avoid the problems associated with turns in the river. In most cases, hard-bottom areas serial correlation and individual variation in be- could be located by the presence of limestone havior (Kenward 1992). Excluded from the anal- bluffs along the riverbank that were visible at low yses were 1997 relocations of ®sh tagged in 1996 ¯ows. Additional qualitative information about because the reproductive state of these ®sh was substrate hardness was determined through the use unknown during 1997. of a 5-m ®berglass pole, which was pressed against the substrate. Sampling with this method was more Results rapid but less informative than with the PONAR Sex Ratios and Reproductive Status unit and was employed when searching for hard- Netting operations began February 21, 1996 in bottom areas to be used for deploying egg sam- Choctawhatchee Bay. Gulf sturgeon were gener- plers. The number of sampling pads deployed at ally encountered along sand ¯ats at depths of 2± a given site ranged between about 15 and 50, de- 6 m. Of 17 Gulf sturgeon collected in 1996, 15 pending on the availability of samplers, apparent individuals (6 males and 9 females) were ®tted size of potential spawning area, and number of ®sh with radio transmitters. In 1997, 35 Gulf sturgeon located by telemetry in the immediate area. We were captured, and a subsample of 20 ®sh (7 males measured depth, substrate type, surface turbidity, and 13 females), chosen on the basis of size, gen- conductivity, temperature, and dissolved oxygen eral condition upon capture, and a combination of at each location a Gulf sturgeon egg was collected. sex and reproductive status, received transmitters. Sampling for eggs continued throughout the Three ®sh died as a result of capture during the spawning season until temperatures approached two ®eld seasons. One was a telemetered male the upper limit for larval survival (25ЊC; Chapman tagged in 1996 and recaptured in 1997; its incision and Carr 1995) and when it had appeared that most site had completely healed and very little scaring telemetered ®sh had left potential spawning sites was apparent. Upon examination, we determined and moved downriver towards areas typically oc- that the antenna had previously broken away from cupied during the summer. the main tag body and was lost. Because this ®sh Data analyses.ÐTwo-way analyses of variance was tracked throughout the 1996 ®eld season, it (ANOVA) were used to examine the in¯uence of seems probable that the antenna became detached sex and reproductive status on the migratory be- while the ®sh was in the bay. havior of Gulf sturgeon. The main factors in the Based on gonadal biopsies of male Gulf stur- model were the sex and reproductive status of each geon, we found similar numbers of ripe (N ϭ 6) ®sh. Year was included as a blocking effect to and immature (N ϭ 7) ®sh. No males were col- account for interannual variability in the maximum lected that were classi®ed as maturing during this upstream distance migrated and date of river entry. study. One male captured in 1996 and recaptured All interactions between factors were tested, and in 1997 was in ripe condition during both years. when interactions were deemed nonsigni®cant (␣ Based on gonadal biopsies of females, 14 were ϭ 0.05), they were excluded and the model was between spawning events (maturing state), 5 were re®tted. Maximum upstream distance was de®ned ripe, and 3 were classi®ed as immature. One fe- as the maximum distance upstream from the river male classi®ed as ripe during 1996 was classi®ed mouth that an individual ®sh was relocated during as maturing when recaptured during 1997. Because the course of sampling. Distances upriver were we did not collect any maturing males, we com- determined by using geographic information sys- bined immature and maturing females into a non- tems software (ArcView version 3.0a, Environ- ripe category for comparison with results for im- mental Systems Research Institute, Inc.). Date of mature males. river entry was de®ned as the date an individual ®sh was ®rst relocated upstream of the river mouth Telemetry (rkm 0). Temperature at time of river entry was During the spring spawning season in 1996, 14 recorded as the bottom temperature (ЊC) at the time of 15 tagged ®sh were relocated in the Choctaw- of ®rst relocation of a ®sh in the river. We at- hatchee River on at least one occasion. A total of tempted to correct for differences in the timing 193 relocations of telemetered ®sh, a mean of 14 between river searches by rounding the date of relocations per individual, were made during this entry to weekly intervals, which were then as- period. The ®rst tagged ®sh moved into the Choc- 816 FOX ET AL. tawhatchee River 7 d after tag implantation and due to sex (P ϭ 0.413) or year (P ϭ 0.173) and release in the bay. The ®sh that did not migrate no signi®cant interactions (P Ͼ 0.05). upriver during spring was relocated in the Choc- Water temperatures at time of river entry dif- tawhatchee River for the ®rst time on September fered signi®cantly by reproductive stage (cooler 4, or 188 d after release. Relocation of this ®sh for ripe versus nonripe ®sh; P Ͻ 0.001), sex (cool- established that postsurgery survival was 100% for er for males than for females; P ϭ 0.006), and year the 1996 season. (P ϭ 0.011; Figure 2). There was a signi®cant The ®rst relocations in the 1997 ®eld season interaction between reproductive stage and year (P were on March 26, when four ®sh were found in ϭ 0.001) that was due to greater difference in tem- the lower Choctawhatchee River. These ®sh were perature at river entry between ripe and nonripe relocated 4±13 d after tag implantation and re- ®sh in 1996 compared with 1997. Compared with lease. Subsequent tracking of the main-stem Choc- 1997, 1996 generally had cooler temperatures ear- tawhatchee River on March 31 and April 7, 1997 ly in the year and a much more rapid warming determined that two male ®sh tagged in 1996 were trend with the arrival of summer. Temperature at already in the upstream (upriver of rkm 120) hab- the time of river entry for individual ®sh ranged itat. A total of 230 relocations of ®sh radio-tagged from 11.2ЊC to 24.9ЊC and averaged 19.3ЊC for the in either 1996 or 1997 were made during the 1997 1996 ®eld season. In 1997, temperature at time of ®eld season, or an average of 9 relocations per river entry ranged from 18.3ЊC to 27.1ЊC and av- individual. All ®sh radio-tagged in 1997 were eraged 21.2ЊC. found within the Choctawhatchee River. The lo- There was a highly signi®cant difference in the cation of the last two ®sh on June 26 established maximum distance migrated upriver between ripe that, as in 1996, we achieved a postsurgery sur- and nonripe ®sh (Figure 2; P Ͻ 0.001). Most ripe vival rate of 100%. females were located above the con¯uence of the With the exception of one ®sh recaptured during Pea and Choctawhatchee rivers (rkm 117), where- gill-netting operations, none of the ®ve ®sh ®tted as nonripe females primarily occupied the lower with external transmitters in 1996 were relocated river (Figure 1). A similar pattern was apparent during 1997. For the one ®sh that was recaptured, for ripe versus nonripe males (Figure 3). Ripe the backing plate on the external transmitter had males and females moved downstream after the cracked and the tag was not securely attached. This spawning season to areas occupied by nonripe ®sh external transmitter was removed and replaced (Figures 4, 5). One exception to this pattern was with internal radio and ultrasonic transmitters. a ripe male ®sh that moved to the lower river after Six of 10 ®sh equipped with internal transmitters the spawning season, and then was alternately lo- during the 1996 season were relocated during cated in the lower river and Choctawhatchee Bay 1997. One ®sh tagged in 1996 died in our gill nets; during a 2-week period in May and June 1997. the remaining ®ve ®sh were tracked during the The spatial segregation between ripe and nonripe 1997 season. One of these ®ve either expelled its ®sh was compromised somewhat by one nonripe tag or died because the location of the transmitter male in each year, and two nonripe females in 1997 never changed. Because this ®sh was found at rkm (Figures 4, 5). We did not detect a signi®cant dif- 30 during mid-August 1996 and then near the ference between sexes in the maximum distance Choctawhatchee River mouth (rkm 0) during Sep- migrated upstream (P ϭ 0.065), although males tember 1996, it seems likely the ®sh either ex- did migrate further upstream than did females dur- pelled the tag or died on its return to the bay. The ing both years (Figures 4, 5). There was a signif- four remaining ®sh were relocated during regular icant interaction between reproductive status and searches during the 1997 ®eld season. year (P ϭ 0.011), which was due to the greater difference between ripe and nonripe ®sh observed in 1996. Migration Timing and Movement Patterns Although we did not quantify the relationships, Ripe Gulf sturgeon entered the Choctawhatchee no clear pattern was found between timing of river River signi®cantly earlier than did nonripe ®sh entrance and ¯ow patterns. Flow regimes varied (Figure 2; P ϭ 0.004). Ripe ®sh typically entered considerably between 1996 and 1997 (Figures 4, the river from March to mid-April, whereas non- 5). During 1996, ¯ows were characterized by sev- ripe ®sh entered the river over a much more pro- eral pulses of high water, from the middle of Feb- tracted period (March±September). There were no ruary though late April, that then tapered off with signi®cant differences in the timing of river entry the approach of summer. Flows in 1997 were high GULF STURGEON SPAWNING AND HABITAT 817

FIGURE 2.ÐMean and SE for day of the year of river entry, water temperature at river entry (ЊC), and maximum upstream relocation (in river kilometers or rkm) for telemetered Gulf sturgeon in the Choctawhatchee River during 1996±1997. 818 FOX ET AL.

FIGURE 3.ÐPlotted maximum upstream relocation (in river kilometers, rkm, from the mouth of the river) and reproductive status for individual male Gulf sturgeon in the Choctawhatchee River system, 1996 and 1997 ®eld seasons. For ®sh captured in 1996 that returned in 1997, reproductive status in 1997 is unknown. in late February and early March and generally sturgeon eggs were collected from six discrete low during early summer, except for brief intervals (i.e., Ͼ1 km apart) sites in both the Choctawhatch- of high ¯ow. ee and Pea rivers (Figure 6). All egg collection sites were located in Alabama above rkm 110. Egg Collection Eggs were collected on six different dates between During 1996, telemetered ®sh moved over large April 18 and May 1. areas and failed to remain at speci®c sites for more Based on microscopic examination, egg devel- than a day or so on the upper Choctawhatchee and opmental stages ranged from the morula to the Pea rivers. Egg samplers were deployed from April advanced gastrulation stage (Conte et al. 1988). 25 to May 16, but no Gulf sturgeon eggs were Based upon temperatures at time of egg collection collected during the 1996 ®eld season (Figure 6). and information on hatching times for hatchery- In 1997 several telemetered Gulf sturgeon re- reared Gulf sturgeon (Parauka et al. 1991), we es- mained for 2±3 days in discrete areas in the upper timate that all eggs were no more than 48 h old at portion of the Choctawhatchee River. A steep lime- the time of collection. stone bank and hard bottom substrate characterized The sites where Gulf sturgeon eggs were col- each of these areas. Egg samplers were deployed lected had limestone or gravel substrates and water continuously from April 4 through May 13 in these depths ranging from 1.4 to 7.9 m. No difference areas. Except for a few periods of very high ¯ow in surface and bottom temperatures were observed, in late April and early May (when we were unable and water temperatures ranged from 18.4ЊCto to examine samplers), samplers were checked at 22.0ЊC on dates when eggs were collected. Con- 2±3 d intervals. During 1997, 42 fertilized Gulf ductivity values ranged from 32 to 70 ␮S and av- GULF STURGEON SPAWNING AND HABITAT 819 eraged 46 ␮S. Flow varied substantially during the tawhatchee River (Livingston et al. 1991). In ad- interval when eggs were collected (Figure 5). Tur- dition, spawning in upstream areas may prevent bidity values ¯uctuated greatly in response to the the newly hatched larvae from coming into contact timing of rainfall; values ranged from 12.3 to with saline water before they are ready to undergo 114.0 nephelometric turbidity units (NTU) and av- the necessary osmotic changes required for this eraged 52.5 NTU. transition to the marine environment (Van Eenen- naam et al. 1996; Altinok 1997). Discussion Our results support Chapman and Carr's (1995) The collection of fertilized Gulf sturgeon eggs hypothesis that reproductively mature individuals combined with telemetry results provides evidence time their migration and arrival at the spawning that upper river areas are important for successful grounds so that river conditions will optimize the reproduction of Gulf sturgeon within the Choc- survival of eggs and larval sturgeon (15±20ЊC). tawhatchee River basin. Fertilized eggs were col- All but one fertilized Gulf sturgeon egg collected lected on hard-bottom areas in the upper river that in this study were obtained at temperatures less were frequented by telemetered ripe Gulf sturgeon than 20ЊC, which corresponds closely to recent during the spawning season. Although Gulf stur- ®ndings in the Suwannee River (Sulak and Clugs- geon may spawn in other locations in the upper ton 1998). Choctawhatchee River, the spatial segregation of We obtained fertilized Gulf sturgeon eggs on six ®sh based on reproductive status indicates that lit- dates between April 18 and May 1, 1997, although tle or no spawning occurs in the lower portions of sampling was conducted both earlier and later in the river. Previous research on Gulf sturgeon (Mar- the season. Spawning in the Suwannee River is chant and Shutters 1996; Sulak and Clugston 1998) somewhat earlier (late March through early May), and other sturgeon species (Artyukhin et al. 1979; occurring shortly after the March and April new Kynard 1997; Schaffter 1997) has shown a com- moons and after water temperatures reach 17ЊC mon pattern of spawning in the upper portions of (Sulak and Clugston 1998). We found little evi- the river. dence for the coupling of spawning with lunar cy- Steep bluffs and an increased prevalence of cles within the Choctawhatchee River system. We limestone substrate characterize the upper river ar- obtained eggs on a semiregular basis from 11 d eas where ripe Gulf sturgeon were relocated and after the April new moon until just before the new fertilized eggs were collected, whereas the lower moon on May 6. Our results must be quali®ed, river sites are predominantly sand. This change in however, by the nonsystematic method of sampler substrate type occurs abruptly at around rkm 100. deployment and the limited number (N ϭ 11) of Information on Gulf sturgeon spawning in the Su- ripe ®sh tracked to the spawning grounds. Sam- wannee River also indicates that particular areas plers were deployed at a series of different sites of hard-bottom habitat are important for successful because we were more interested in identifying reproduction of Gulf sturgeon (Marchant and Sut- additional spawning locations than in quantifying ters 1996; Sulak and Clugston 1998). the periodicity of spawning at any one site. There are several reasons why spawning at up- We found that Gulf sturgeon migratory patterns stream hard-bottom areas would be expected. Gulf varied with respect to reproductive status and to sturgeon eggs are adhesive (Parauka et al. 1991), a lesser extent by sex of the individual. Ripe ®sh so eggs spawned in areas of soft-bottom substrate of both sexes entered the Choctawhatchee River (mud and sand) could become encapsulated with earlier and moved signi®cantly further upstream a layer of material that could possibly suffocate compared with nonripe ®sh. We did not detect a the developing egg. Upstream sites would be ex- difference between sexes in the date of river entry, pected to have higher water quality, i.e., lower but water temperatures at river entry were cooler temperatures and higher oxygen levels. Upstream for male Gulf sturgeon. Male Gulf sturgeon also sites probably provide lowered risk of . tended to remain at spawning sites for longer pe- Other sturgeon researchers have noted that devel- riods compared with females. An earlier migration oping larvae occupy the interstitial spaces between of male ®sh has also been documented for several rocks and cobble, which may provide protection European and North American sturgeon species from predation (Kempinger 1988; LaHaye et al. (Dovel and Berggren 1983; Holcik 1989; 1992). Also, Choctawhatchee River survey results O'Herron et al. 1993). In addition, there is evi- indicate that predatory ®sh occur more frequently dence that this pattern may be exhibited by Gulf in the tributaries and lower portions of the Choc- sturgeon in the Suwannee River (Carr et al. 1996). 820 FOX ET AL. GULF STURGEON SPAWNING AND HABITAT 821

Gulf sturgeon began migrating from Choctaw- Heard, Gulf Coast Research Laboratory, personnel hatchee Bay into the Choctawhatchee River in late communication). These prey items occur within March and continued through the spring and into Choctawhatchee Bay. the summer months. The initiation of migration Our results, and those of Foster and Clugston into the Choctawhatchee River was delayed com- (1997), support the hypothesis that Gulf sturgeon pared with the Suwannee River; in the Suwannee, have adapted to erratic winter±spring ¯ows and migration began in mid-February and concluded begin their migration when water temperatures ap- in early May (Carr et al. 1996; Foster and Clugston proach some thermal minimum (about 18ЊC). The 1997). This difference in the start of migration is average water temperatures when ripe ®sh began probably due to temperature differences because migrating into the Choctawhatchee River were the Suwannee River typically warms earlier than comparable to those reported for the Suwannee the Choctawhatchee River (Frank Parauka, River (Foster 1993; Chapman and Carr 1995). USFWS, personal communication). However, this Similar to Foster and Clugston (1997), we did not cannot fully explain the more protracted timing of detect evidence for a relationship between ¯ows river entrance that we documented for immature and the timing of river entrance. In contrast, Chap- and maturing individuals. A second explanation man and Carr (1995) reported that a strong positive for the difference in the timing of migration of ®sh correlation existed between high discharge levels between river systems may be the location of cap- and the initiation of migration for Gulf sturgeon ture sites. In previous studies on the Suwannee in the Suwannee River. River, Gulf sturgeon were collected at the river Only 6 of 10 Gulf sturgeon receiving internal mouth (Huff 1975; Carr et al. 1996; Foster and transmitters in 1996 were located in the Choctaw- Clugston 1997), whereas we collected them in the hatchee River during 1997. This low return rate is bay prior to river entrance. The delayed start of somewhat problematic, given that Gulf sturgeon, migration that we observed for immature and ma- unlike their Atlantic counterparts, are thought to turing individuals is noteworthy when coupled return to rivers each year regardless of reproduc- with our observations that Gulf sturgeon appeared tive condition (Carr et al. 1996). The low return to be actively feeding within Choctawhatchee Bay. rate may be due to straying to other river systems, We hypothesize that mature, nonspawning Gulf their remaining in the Gulf of Mexico or estuarine sturgeon may be utilizing estuarine habitat to a waters, transmitter failure, or expulsion of the greater degree than previously thought. Because transmitter. Transmitter failure cannot be ruled out, foraging ceases while adult Gulf sturgeon are in but it seems unlikely that such a large number of the river (Clugston et al. 1995), extended periods tags would fail prematurely. Straying to neigh- of estuarine and marine residency may be impor- boring river systems may account to some extent tant in rebuilding of energy reserves and gonadal for the low return rate. In July of 1998, Florida recrudescence during nonspawning years. Department of Environmental Protection research- Gulf sturgeon appeared to be foraging within ers relocated one of our 20 telemetered Gulf stur- Choctawhatchee Bay before initiating their up- geon in the Escambia River (Ͼ100 km from Choc- stream migrations. Upon capture, several ®sh ei- tawhatchee River). Despite this observation, a high ther regurgitated or passed fecal material contain- rate of straying seems inconsistent with recent ge- ing large numbers of decapod crustaceans, includ- netic evidence that Gulf sturgeon exhibit high ®- ing blue crabs Callinectes sapidus and Lepedo- delity to their natal rivers (Stabile et al. 1996). We phthalmus (ϭCallianassa) louisianensis (ghost hypothesize that some ®sh remain in marine or shrimp family: Callianassidae). Necropsy results estuarine waters for a year or more where they for a ®sh that died during capture in 1996 indicated undergo gonadal recrudescence. The late summer that the ®sh had been feeding exclusively on both return of immature and maturing individuals pro- ghost shrimps and Leptalpheus forceps a commen- vides evidence that a prolonged period of fresh- sal species in the family Alpheidae (Richard water residency may not be required for all Gulf

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FIGURE 4.ÐChoctawhatchee River relocations (in river kilometers, rkm, upstream from the river mouth), by date, for (A) individual female and (B) male Gulf sturgeon tagged during the 1996 ®eld season. Symbols indicate reproductive status. Panel (C) represents averaged daily ¯ow rates (m3/s) and daily temperatures (ЊC) in the Choctawhatchee River by date. 822 FOX ET AL. GULF STURGEON SPAWNING AND HABITAT 823

FIGURE 6.Ð(A) Locations of sites where egg sampling pads were deployed during 1996 and 1997 and fertilized Gulf sturgeon eggs were collected compared with (B) sampling sites where no Gulf sturgeon eggs were collected. sturgeon. During our 1996 ®eld season, one ®sh er indicated that timing of river entrance of Gulf apparently remained in the estuary until early Sep- sturgeon varied according to sex (Carr et al. 1996). tember, after which it was relocated once in the Information about migration and the timing of lower Choctawhatchee River. During 1997, three reproductive cycles is needed to understand the ®sh were relocated in the bay (ultrasonic tags) impact of ®shing on Gulf sturgeon. Previous stud- through late June when migration upriver began. ies of both Gulf and Atlantic sturgeon indicate that One Gulf sturgeon moved between the lower river individuals require prolonged periods for the re- and Choctawhatchee Bay on two occasions in late building of gonadal material between spawning May and early June 1997. Such movements be- events. Females required 3±5 years between tween fresh and saltwater habitats could not be spawning events, whereas males required 1±5 detected in our previous telemetry studies because years (Smith 1985). The ®nding of maturing males only radio transmitters had been used. by Huff (1975) provided evidence that spawning Recent work on Atlantic sturgeon migration in- was not annual for male Gulf sturgeon. However, dicated that both the sex and reproductive status we found no maturing males among the 13 males of individual ®sh affects the migratory behavior that we examined surgically. Of the three males of adult Atlantic sturgeon (Van Eenennaam et al. that were ripe in 1996, one was ripe when recap- 1996). Prior evidence for differential habitat uti- tured in 1997. The remaining two males returned lization in Gulf sturgeon based on sex and repro- to the river in 1997 and exhibited movement pat- ductive status is largely circumstantial. Huff terns characteristic of ripe ®sh (i.e., early river (1975) noted that the low capture rate of spent entry and movement to spawning sites). These ob- females in surveys supported the hypothesis that servations suggest that male Gulf sturgeon may be migration routes differed by sex. Similarly, mul- capable of spawning on an annual basis. tiyear sampling at the mouth of the Suwannee Riv- Our evidence regarding spawning periodicity in

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FIGURE 5.ÐChoctawhatchee River relocations (in river kilometers, rkm, upstream from the river mouth), by date, for (A) individual female and (B) male Gulf sturgeon tagged during the 1997 ®eld season. Symbols indicate reproductive status. Panel (C) represents average daily ¯ow rates (m3/s) and daily temperatures (ЊC) in the Choc- tawhatchee River by date. The shaded rectangles indicate the interval when fertilized Gulf sturgeon eggs were collected on egg sampling pads. 824 FOX ET AL. females supports the observation that spawning is study and also for giving comments on earlier ver- not annual (Huff 1975). Histological results from sions of this manuscript. This work would not have the female captured in 1996 and recaptured in 1997 been possible without the ®nancial support and showed that this female was not ripe in consecutive assistance provided by the Panama City, Florida, years. This ®nding is also supported by telemetry U.S. Fish and Wildlife Service of®ce. In particular, evidence for other female Gulf sturgeon. In ad- we thank Gail Carmody, Bob Jarvis, and Laura dition to the one recaptured female, two females Jenkins. We also express our gratitude to the U.S. that were ®tted with transmitters during the 1996 Geological Survey, Florida±Caribbean Science ®eld season returned in 1997. One ®sh was deter- Center, Gainesville, Florida, for their technical as- mined to be ripe in 1996 but during 1997 exhibited sistance and loan of egg samplers. In particular we movement patterns that appear to be characteristic thank Ken Sulak and Les Parker. For help with of a nonripe individual (i.e., delayed river entry both histological and egg staging techniques, we and reduced upstream movement). The second re- thank Frank Chapman and the University of Flor- turning female was classi®ed as immature in 1996 ida. We also recognize Mark Collins, Dave Eg- but exhibited movement patterns in 1997 more gleston, John Godwin, Mary Moser, Ted Smith, characteristic of a ripe female (i.e., early river en- Ken Sulak, and two anonymous reviewers for their try and movement to spawning sites). Our histo- comments and reviews of this manuscript. logical results also support a greater than annual interval between spawning events. Three of 9 fe- References males in 1996 and 10 of 13 in 1997 were classi®ed Altinok, I. 1997. Hydromineral regulation capabilities as maturing. Results of previous work on Gulf of juvenile Gulf of Mexico sturgeon (Acipenser ox- sturgeon (Huff 1975) showed a much lower abun- yrinchus desotoi). Master's thesis. University of dance of females in the maturing category. This Florida, Gainesville. discrepancy in ®ndings may be a result of differ- Artyukhin, Y. N., A. D. Sukhoparova, and L. G. Fi- ences in gear selectivity, classi®cation schemes, or mukhina. 1979. The gonads of the sturgeon, Aci- the failure of maturing females to return to the penser guÈldenstaÈdti, in the zone below the dam of rivers each year. Recent work on the closely related the volgograd water engineering station. Journal of Ichthyology 18:912±923. Atlantic sturgeon has shown that females with Bain, M. B. 1997. Atlantic and shortnose of midvitellogenic (i.e., maturing) gonads are absent the Hudson River: common and divergent life his- from collections on the Hudson River (Van Ee- tory attributes. Environmental Biology of Fishes 48: nennaam and Doroshov 1998). Because Atlantic 347±358. sturgeon reside in marine waters for 3±5 years be- Bass, G. D., D. M. Yeager, and V. G. Hitt. 1980. Ecology tween spawning events (Bain 1997), it seems prob- of the Choctawhatchee River system, Florida. Flor- able that the lack of maturing females is due to ida Game and Freshwater Fish Commission, North- west Streams Research Project, Tallahassee. their absence on the river sampling sites (Van Ee- Bemis, W. E., E. K. Findeis, and L. Grande. 1997. An nennaam and Doroshov 1998). overview of . Environmental Bi- In conclusion, this study provides the ®rst de- ology of Fishes 48:25±71. tailed information on the relationship between mi- Bemis, W. E., and B. Kynard. 1997. Sturgeon rivers: an gratory behavior and both the sex and reproductive introduction to acipenseriform biogeography and status of Gulf sturgeon. In addition, we provide life history. Environmental Biology of Fishes 48: 167±183. the ®rst descriptions of spawning sites for Gulf Buckley, J., and B. Kynard. 1985. Yearly movements sturgeon known outside of the Suwannee River. of shortnose sturgeons in the Connecticut River. Our results establish that hard-bottom areas in up- Transactions of the American Fisheries Society 114: per river areas are important for spawning. Al- 813±820. though it is probable that Gulf sturgeon spawn in Burgess, R. F. 1963. Florida sturgeon spree. Outdoor other locations in the upper river, our telemetry Life (March):44. results indicate that little or no spawning occurs Carr, S. H., F. Tatman, and F. A. Chapman. 1996. Ob- in the lower portions of the river. Thus, preser- servations on the natural history of the Gulf of Mex- ico sturgeon (Acipenser oxyrinchus desotoi, Vla- vation of upper river sites with suitable spawning dykov 1955). Ecology of Freshwater Fish 5:169± habitat will become increasingly important as Gulf 174. sturgeon populations rebuild. Chapman, F. A., and S. H. Carr. 1995. Implications of early life stages in the natural history of the Gulf Acknowledgments of Mexico sturgeon, Acipenser oxyrinchus desotoi. The authors are indebted to Michelle LaRue for Environmental Biology of Fishes 43:407±413. her assistance with the ®eld component of this Chapman, F. A., J. P. Van Eenennaam, and S. I. Doro- GULF STURGEON SPAWNING AND HABITAT 825

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