Endangered and Threatened Wildlife and Plants: Notice of 12-Month Finding on a Petition To List Alabama Shad as Threatened or Endangered Under the Endangered Species Act

DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

[Docket No. 130626570-6999-02]

RIN 0648-XC742

Endangered and Threatened Wildlife and Plants: Notice of 12-Month Finding on a Petition To List Alabama Shad as Threatened or Endangered Under the Endangered Species Act

AGENCY:

National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.

ACTION:

Notice of 12-month finding.

SUMMARY:

We, NMFS, announce a 12-month finding and listing determination on a petition to list Alabama shad (

Alosa alabamae

) as threatened or endangered under the Endangered Species Act (ESA). We have completed a comprehensive review of the status of Alabama shad in response to the petition submitted by the Center for Biological Diversity (CBD), Alabama Rivers Alliance, Clinch Coalition, Dogwood Alliance, Gulf Restoration Network, Tennessee Forests Council, and the West Virginia Highlands Conservancy (petitioners). Based on the best scientific and commercial information available on the status of Alabama shad, we have determined that the species does not warrant listing at this time. We conclude that the Alabama shad is not currently in danger of extinction throughout all or a significant portion of its range and is not likely to become so within the foreseeable future.

DATES:

This finding was made on January 12, 2017.

ADDRESSES:

The reference list associated with this determination is available by submitting a request to the Species Conservation Branch Chief, Protected Resources Division, NMFS Southeast Regional Office, 263 13th Avenue South, St. Petersburg, FL 33701-5505, Attn: Alabama shad 12-month finding. The reference list is also available electronically at:

http://sero.nmfs.noaa.gov/protected_resources/listing_petitions/species_esa_consideration/index.html

FOR FURTHER INFORMATION CONTACT:

Kelly Shotts, NMFS, Southeast Regional Office (727) 824-5312; or Marta Nammack, NMFS, Office of Protected Resources (301) 427-8469.

SUPPLEMENTARY INFORMATION:

Background

In 1997, we added Alabama shad to our Candidate Species List (62 FR 37562; July 14, 1997). At that time, a candidate species was defined as any species being considered by the Secretary of Commerce (Secretary) for listing as an endangered or a threatened species, but not yet the subject of a proposed rule (49 FR 38900; October 1, 1984). In 2004, we created the Species of Concern list (69 FR 19975; April 15, 2004) to encompass species for which we have some concerns regarding their status and threats, but for which insufficient information is available to indicate a need to list the species under the Endangered Species Act (ESA). Twenty-five candidate species, including the Alabama shad, were transferred to the Species of Concern list at that time because they were not being considered for ESA listing and were better suited for Species of Concern status due to some concerns and uncertainty regarding their biological status and threats. The Species of Concern status does not carry any procedural or substantive protections under the ESA.

On April 20, 2010, the Center for Biological Diversity (CBD), Alabama Rivers Alliance, Clinch Coalition, Dogwood Alliance, Gulf Restoration Network, Tennessee Forests Council, and the West Virginia Highlands Conservancy (petitioners) submitted a petition to the Secretaries of Interior and Commerce, as well as to the Regional Director of the Southeast Region of the U.S. Fish and Wildlife Service (USFWS), to list 404 aquatic, riparian, and wetland species from the southeastern United States as threatened or endangered under the ESA. The petitioners also requested that critical habitat be designated for all petitioned species. We notified the USFWS' Southeast Region by letter dated May 3, 2010, that the Alabama shad, one of the 404 petitioned species, would fall under NMFS' jurisdiction based on the August 1974 Memorandum of Understanding regarding jurisdictional responsibilities and listing procedures between the two agencies. We proposed to USFWS that we would evaluate the petition, for Alabama shad only, for the purpose of the 90-day finding and any required subsequent listing action. On May 14, 2010, we sent the petitioners confirmation we would be evaluating the petition for Alabama shad. On February 17, 2011, we published a negative 90-day finding in the

Federal Register

(76 FR 9320) stating that the petition did not present substantial scientific or commercial information indicating that the requested listing of Alabama shad may be warranted.

On April 28, 2011, in response to the negative 90-day finding, CBD filed a notice of intent to sue the Department of Commerce (DOC) and NMFS for alleged violations of the ESA in making its finding. CBD filed the lawsuit in the U.S. District Court for the District of Columbia on January 18, 2012. On June 21, 2013, CBD and DOC/NMFS settled the lawsuit. We agreed to reevaluate the original listing petition, as well as information in our files, including some additional information we acquired after the original 90-day finding published on February 17, 2011, and publish a new 90-day finding. On September 19, 2013, we published a 90-day finding with our determination that the petition presented substantial scientific and commercial information indicating that the petitioned action may be warranted (78 FR 57611).

Our 90-day finding requested scientific and commercial information from the public to inform a review of the status of the species. We requested information on the status of Alabama shad, including: (1) Historical and current distribution and abundance of this species throughout its range, including data addressing presence or absence at a riverine scale; (2) historical and current population sizes and trends; (3) biological information (life history, genetics, population connectivity, etc.); (4) landings and trade data; (5) management, regulatory, and enforcement information; (6) any current or planned activities that may adversely impact the species; and (7) ongoing or planned efforts to protect and restore the species and its habitat. We received information from the public in response to the 90-day finding, and we incorporated all relevant information into our review of the status of Alabama shad.

Listing Species Under the ESA

We are responsible for determining whether Alabama shad warrants listing as threatened or endangered under the ESA (16 U.S.C. 1531

et seq.

) To be considered for listing under the ESA, a group of organisms must constitute a “species,” which is defined in section 3 of the ESA to include taxonomic species and “any subspecies of fish, or wildlife, or plants, and any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature.” Section 3 of the ESA defines an endangered species as “any species which is in danger of extinction throughout all or a significant portion of its range” and a threatened species as one “which is likely to become an

endangered species within the foreseeable future throughout all or a significant portion of its range.” Thus, we interpret an “endangered species” to be one that is presently in danger of extinction. A “threatened species,” on the other hand, is not presently in danger of extinction, but is likely to become so in the foreseeable future (that is, at a later time). In other words, the primary statutory difference between a threatened and endangered species is the timing of when a species may be in danger of extinction, either presently (endangered) or in the foreseeable future (threatened).

Section 4(b)(1)(A) of the ESA requires us to make listing determinations based solely on the best scientific and commercial data available after conducting a review of the status of the species and after taking into account efforts being made by any state or foreign nation to protect the species. Under section 4(a) of the ESA, we must determine whether any species is endangered or threatened due to any one or a combination of the following five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence (Sections 4(a)(1)(A) through (E)).

We followed a stepwise approach in making this listing determination for Alabama shad. First we conducted a biological review of the species' taxonomy, distribution, abundance, life history, and biology. Next, using the best available information, we completed an extinction risk assessment using the general procedure of Wainwright and Kope (1999). Then, we assessed the threats affecting the status of each species using the five factors identified in section 4(a)(1) of the ESA.

In the next step, we evaluated the available information to determine whether there is a portion of the species' range that is “significant” in light of the use of the term in the definitions of threatened and endangered. We followed the final policy interpreting the phrase “significant portion of its range” (79 FR 37578; July 1, 2014). A portion of the range of a species is “significant” if the species is not currently endangered or threatened throughout all of its range, but the portion's contribution to the viability of the species is so important that, without the members in that portion, the species would be in danger of extinction, or likely to become so in the foreseeable future, throughout all of its range.

We describe each of the steps listed above in detail in the following sections of this finding.

Review of the Status of Alabama Shad

We have identified the best available scientific and commercial information in order to conduct a comprehensive review of the status of Alabama shad. Unlike many of our other 12-month findings, we have not developed a separate status review report. Instead we present all available relevant information for Alabama shad in this

Federal Register

notice.

Taxonomy

Alabama shad (

Alosa alabamae

) was first described by David Starr Jordan and Barton Warren Evermann in 1896 in the Black Warrior River near Tuscaloosa, Alabama (Jordan and Evermann 1896). Alabama shad was depicted earlier as “white shad” in documents from the U.S. Commission on Fish and Fisheries circa 1860 and was often confused with other shad even after it had been described (Daniels 1860, Barkuloo

et al.

1993). Alabama shad belong to the family Clupeidae and are closely related to, as well as similar in appearance and life history to, the American shad (

A. sapidissima

). They also resemble the skipjack herring (

A. chrysochloris

), which occurs in the same areas as Alabama shad. Defining characteristics of the Alabama shad are an upper jaw with a distinct median notch, and the number of gill rakers (41 to 48) on the lower limb of the anterior gill arch. Alabama shad differ morphologically from other

Alosa

species that occur in the same area by a lower jaw that does not protrude beyond the upper jaw, black spots along the length of the lower jaw, and a dorsal fin that lacks an elongated filament.

Alabama shad are considered a separate species from the closely related American shad based on mitochondrial DNA molecular data (Bowen 2005, 2008, Kreiser and Schaefer 2009), in addition to the physical differences. There is limited genetic difference and it is theorized that the two species have only recently diverged from a common ancestor. Alabama shad is its own monophyletic group (a group of organisms descended from a single ancestor) due to limited genetic differences among the Clupeidae family and allopatric speciation (speciation by geographic isolation, Bowen 2008). There has been no significant genetic differentiation among different stocks of Alabama shad geographically and there is no evidence of hybridization between any of the other

Alosa

species and Alabama shad (Kreiser and Schaefer 2009).

Diet

Alabama shad are likely generalist insect feeders. Mickle

et al.

(2013) conducted stomach content analyses on individuals collected from the Pascagoula and Apalachicola Rivers. The stomach contents of the smallest juvenile Alabama shad (those less than 50 millimeters), collected exclusively from the Pascagoula River, were made up primarily of semi-decomposed algae and other unidentifiable organics, suggesting filter feeding or particulate feeding of smaller prey. As the size of Alabama shad taken from the Pascagoula River increased, the percentage of terrestrial and aquatic insects in the stomach contents increased. Mickle

et al.

(2013) found that terrestrial insects dominated the stomach contents of all size classes of Alabama shad taken from the Apalachicola River. Diet of Alabama shad from both the Apalachicola and Pascagoula Rivers changed as the size of the fish increased, with insects replacing unidentifiable organic matter. Ephemeroptera nymphs, an order of aquatic insects, dominated the diets of larger Alabama shad from both rivers. These nymphs produce aquatic juvenile larvae that emerge in open water in the same habitats where Mickle

et al.

(2013) collected the Alabama shad for their study. Mickle

et al.

(2013) noted that these observed ontogenetic dietary shifts seemed to coincide with habitat shifts and are consistent with a generalist strategy.

Age and Growth

Like many clupeids (the family of fish that include shad, herring, sardines, and menhaden), egg hatching period and growth of subsequent larvae varies by location and environmental factors. Mickle

et al.

(2010) found those Alabama shad that hatched in the Apalachicola River had a longer successful hatch window (mean of 58 days) compared to those in the Pascagoula River (mean of 33.8 days).

Juvenile Alabama shad exhibit rapid growth, although the size of juveniles varies across the range of the species. Typical juvenile Alabama shad increase in size from about 4.7 centimeters total length (cm TL, the length of the fish measured from the tip of the snout to tip of the tail fin) to about 10.1 cm TL over the summer but variation can occur depending on the river drainage. For example, juvenile Alabama shad from the Apalachicola River grew faster than those in the Pascagoula River despite

similar environmental conditions (Laurence and Yerger 1967, Mickle 2010). In the Chipola River, Florida, juveniles move downstream at an average size of 6.5 cm TL, while those moving down the nearby Apalachicola River averaged 11.5 cm TL (Laurence and Yerger 1967).

In both the Apalachicola and Choctawhatchee Rivers, Florida, adult female shad were typically longer and heavier than the adult males (Laurence and Yerger 1967, Mills 1972, Mettee and O'Neil 2003). Age 1-3 males on average weigh 250 grams and age 1-4 females weigh around 650 grams before spawning (Mettee and O'Neil 2003, Ingram 2007).

Two studies have aged otoliths of Alabama shad but only one study has fit growth models to observed age data. In the Pascagoula River, maximum observed age was 6 years based on otoliths (Mettee and O'Neil 2003), while Ingram (2007) aged shad from the Apalachicola River to 4 years.

Reproductive Biology

Alabama shad is a euryhaline (adapted to a wide range of salinities), anadromous fish species that migrates between the ocean and medium to large flowing rivers to spawn (reproduce) from the Mississippi River basin to the Suwannee River, Florida. Alabama shad spawn in February to April at lower latitudes in the south and May to June in more northern latitudes, usually over sandy bottoms, gravel shoals, or limestone outcrops (Laurence and Yerger 1967, Mills 1972, Barkuloo 1993, Kreiser and Schaefer 2009, Mickle

et al.

2010). Water temperatures between 18 and 22 °C and moderate current velocities (0.5-1.0 meters (m) per second) promote successful spawning (Laurence and Yerger 1967, Mills 1972). If environmental circumstances are unfavorable, mature Alabama shad will sometimes abandon their upstream spawning movement (Young 2010).

Spawning males range in age from 1 to 5 years and females from 2 to 6 years (Mickle

et al.

2010). Some age-1 male Alabama shad move into fresh water for their first spawning, but the primary spawning age classes tend to be 2-3 years for males and 2-4 years for females; any age-4 Alabama shad present in rivers are almost always female (Laurence and Yerger 1967, Mettee and O'Neil 2003, Ingram 2007). Males arrive at spawning sites first and increase in abundance as the spawning season continues, while females appear in large groups slightly later in the spawning season (Mills 1972, Mettee and O'Neil 2003). It is unknown whether females arrive with ripened eggs, as suggested by Mills (1972), or if their gonads ripen as river temperatures increase (Laurence and Yerger 1967). Females tend to release their eggs in late April and early May when the water temperatures are 20-21 °C (Mettee and O'Neil 2003, Ingram 2007). Fecundity (reproductive capacity) is related to size, with larger females producing more eggs (Ingram 2007, Young 2010). Alabama shad produced 26,000-250,000 eggs per female in the Apalachicola River and between 36,000-357,000 eggs per female in the Choctawhatchee River (Mettee and O'Neil 2003, Ingram 2007). After spawning, the younger (age 2 and 3) Alabama shad migrate back to marine waters. The older spawners (age-4 and older) either die or are preyed upon by other piscivorous fish (Laurence and Yerger 1967).

Because of the age range among the spawning fish, it is believed that individuals may spawn more than once in a lifetime (Laurence and Yerger 1967, Mettee and O'Neil 2003, Ingram 2007, Mickle

et al.

2010). Laurence and Yerger (1967) indicated that 35 percent of Alabama shad were likely repeat spawners and noted that 2-4 year old males from the Apalachicola River had spawning marks on their scales. Mills (1972) also observed 35-38 percent repeat spawners (mostly age-3) as well as discernable spawning marks on scales from the Apalachicola River population. In addition, Mettee and O'Neil (2003) noted that many Alabama shad collected from the Choctawhatchee River were repeat spawners, with age-3 and age-4 females comprising the majority of repeat spawners in 1994-1995, and age-2 and age-3 females the majority in 1999-2000. In contrast, Ingram (2007) has not observed spawning marks on the scales of Apalachicola River shad and most fish in the Apalachicola may die after spawning (Smith

et al.

2011). Alabama shad appear to be philopatric and return to the same rivers to spawn, resulting in slight genetic differences among river drainages (Meadows 2008, Mickle 2010). These genetic differences may result in characteristics (

e.g.,

faster growth rates, higher temperature tolerance, etc.) that lead to variable spawning strategies among river drainages. Kreiser and Schaefer (2009) found slight genetic distinctions between populations from the Mississippi River basin and coastal Gulf of Mexico drainages due to Alabama shad straying from their natal rivers, at an estimated rate of about 10 migrants per generation.

Life History Strategy

On the spectrum of life history strategies, Alabama shad tend to be “r strategists”, species that are typically short-lived, have small body size, reach sexual maturity at an early age, and have high natural mortality that is balanced by a high growth rate (Adams 1980). Species that are r strategists adapt to unstable, unpredictable environments by producing higher numbers of offspring as compared to k strategist species living in stable, predictable environments. Elliott and Quintino (2007) found that species living in unpredictable, variable, and even stressed environments are well-adapted to cope with these conditions without or with reduced adverse effects. Adapting to highly variable environments also produces high natural variability in r strategist populations. Adams (1980) noted that fisheries for r strategists can have very large catches some years, but are characterized by erratic, highly variable production levels overall. Most clupeoids (an order of soft-finned fishes that includes Alabama shad, other clupeids, and anchovies in the family engraulidae) have a short life span and show striking inter-annual or decadal variation in productivity and abundance (Mace

et al.

2002). Fisheries for clupeoids can vanish for 50-100 years then undergo a remarkable recovery with the population growing as fast as 40 percent per year (Mace

et al.

2002).

Sammons and Young (2012) noted that the population sizes of species in the

Alosa

genus commonly fluctuate widely. An Alabama shad researcher with the Georgia Department of Natural Resources (DNR) noted that as an r strategist, Alabama shad are prone to “boom and bust” years, but they are also highly fecund (capable of producing an abundance of offspring) and can recover quickly from even a small number of fish (based on the results of stocking efforts; T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). In fact, the speciation (evolutionary process by which reproductively isolated biological populations evolve to become distinct species) of Alabama shad likely occurred from a very small number of fish that dispersed around the Florida peninsula and became separated from other

Alosa

species during the Pleistocene (Bowen

et al.

2008). Modeling conducted by Moyer (2012) indicated that the Pleistocene bottleneck for Alabama shad was intense. The effective population size for Alabama shad during the bottleneck was estimated to be between 76 and 398, meaning 76-398 individuals is the

population size during the Pleistocene estimated to have been necessary to result in the relatively low genetic diversity observed in members of the species today. Moyer (2012) also noted that the bottleneck event was prolonged (145-987 shad generations), indicating that the species persisted at very low numbers for an extended period of time.

Habitat Use and Migration

Alabama shad are found in the Gulf of Mexico, although there is very little information about their marine habitat use. Only six records of Alabama shad collected in marine waters exist. The Florida Museum of Natural History reports one specimen was captured in July 1957 approximately 80 miles (mi) or 129 kilometers (km) south of Choctawhatchee Bay, Florida, in about 100 meters of water (Fishnet2 2015, Catalogue #28671). The National Museum of Natural History, Smithsonian Institution, reports another Alabama shad was captured just off Dauphin Island, Alabama, in December 1960 in 15 meters of water (Fishnet2 2015, Catalogue #293755.5174309). Two Alabama shad were collected approximately 115 km southwest of Cape San Blas, Florida in November 2007 (Fishnet2 2015, Catalogue #20627). An Alabama shad was collected by the Texas A&M University Biodiversity Research and Teaching Collections in a trawl about 25 mi (40 km) offshore of Florida, between Tampa Bay and the Charlotte Harbor Estuary (Fishnet2 2016, Catalogue #14540.07). In March 2013, an adult female Alabama shad was collected during a fishery independent monitoring survey approximately 15 km south of the Pascagoula River just north of Petit Bois Island in Mississippi Sound and approximately 5 km east of Horn Island Pass, which leads to the open Gulf of Mexico (Mickle

et al.

2015). Microsatellite DNA analysis indicated that the fish was most genetically similar to Alabama shad originating from the Pascagoula River. She was observed to have well-developed ovaries, and Mickle

et al.

(2015) suggested she may have been preparing to make a spawning run. Stomach content analyses showed that the fish was full of small invertebrates. Previous studies (

e.g.,

Mills 1972) report few or no stomach contents in Alabama shad collected in riverine environments. The marine specimen with a full stomach collected by Mickle

et al.

(2015) supports that Alabama shad likely feed primarily in marine habitats, similar to other anadromous species.

As part of their anadromous life cycle, adult Alabama shad leave the Gulf of Mexico and move into rivers in the spring to spawn. First year (age-0) juveniles stay upriver in freshwater environments until late summer or fall and eventually migrate downstream to the Gulf of Mexico. Juveniles coming from natal rivers located at more northern latitudes (

e.g.,

Ouachita River in Arkansas) begin downstream movement throughout the summer, reaching the Gulf of Mexico by autumn. Juveniles located at more southern latitudes (

e.g.,

Pascagoula River in Florida) will remain in natal rivers as late as December before beginning their downstream movement to the Gulf of Mexico. Alabama shad do not overwinter in freshwater river systems (Mickle

et al.

2010).

Alabama shad prefer cooler river waters with high dissolved oxygen (DO) and pH levels (Mickle

et al.

2010). Although there have been no studies on the thermal tolerances of Alabama shad, other

Alosa

species cannot tolerate water temperatures greater than 32°C; it is likely that Alabama shad also cannot tolerate high water temperatures (Beitinger

et al.

1999). Mickle

et al.

(2010) found spawning adults in waters as cold as 10 °C, but juveniles have been collected in waters as warm as 32 °C (Mickle

et al.

2010, Young 2010).

Water velocity is also believed to be an important habitat feature, as this species is rarely found in the still or backwater portions of rivers. It is hypothesized that spring floods (increased river flows) are a vital environmental cue for spawning adults as well as an important aspect for successful hatching. Juveniles tend to occupy moderate to fast moving water (approximately 0.5-1.2 m per second) that is less than 1 m deep (Mickle 2010). Clear water with minimal benthic algal growth also appears to be preferred by this species (Buchanan

et al.

1999).

Smaller, younger shad tend to prefer the slightly shallower, more protected areas over sandbars, while the older, larger shad can be found in channel and bank habitats. Sandbars within the bends of rivers that are less than 2 m deep often support juveniles in the early summer (Mickle 2010). As the fish grow, they move to bank (greater than 2.5 m deep) and channel (1.5-2.5 m deep) habitats, although the shift is not always consistent (Mickle 2010). Presumably, this allows the juveniles to avoid predators, fulfill foraging needs, or access cooler temperatures that might be present in deeper waters (Bystrom 2003, Mickle

et al.

2010, Mickle 2010).

Distribution and Abundance

NMFS documented the current known distribution and abundance of Alabama shad in a technical memorandum published in August 2011 (Smith

et al.

2011). In addition to conducting an extensive search of all publications, technical reports, and theses available, NMFS staff surveyed scientists at universities, state and Federal facilities, and non-profit organizations throughout the historical range of Alabama shad for any recent recorded captures. Surveys were sent by email, and information was requested on capture dates, location, and number of Alabama shad captured, if available. Additionally, capture information and observations were provided by state and Federal agencies during the public comment period on our 90-day finding.

Information on the historical and current distribution and abundance of Alabama shad is largely lacking. Alabama shad was never an economically important species, therefore information from fisheries statistics, such as landings data, is rare. Hildebrand (1963) noted that Alabama shad were considered unfit for human consumption, and the lack of demand produced no incentive to capture the species or record its presence and abundance. Very few directed research studies on Alabama shad have occurred, with the exception of recent studies in the Apalachicola Chattahoochee Flint (ACF) and Pascagoula River systems. The recent studies in the ACF River system have produced the only abundance estimates, either historical or current, for Alabama shad in any river system. The historical and current distribution of Alabama shad in other systems is based on capture data from general multi-species surveys, project monitoring, captures incidental to other research studies, and anecdotal information. Information received from state resource agencies (

e.g.,

during the public comment period on the 90-day finding and during development of this determination, presented in the sections below) corroborates that long-term, strategic studies of the species in their states are lacking. For instance, the Arkansas Fish and Game Commission stated in their comments on the Alabama shad positive 90-day finding they could not assess the status of Alabama shad in their state because of the scarcity of information on the species, the lack of targeted surveys, and the unknown detectability of the species (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013).

Mettee and O'Neil (2003) note that low numbers of recorded Alabama shad individuals may be due, at least in part, to insufficient sampling effort during

appropriate times (

i.e.,

spawning migrations) and with the appropriate gear to target the species. Hildebrand (1963) noted the importance of proper gear, citing greatly increased catches of Alabama shad that occurred in Kentucky when surface-fishing seines were substituted for bottom-fishing seines. Short-term studies may also fail to accurately demonstrate the status of a given river population of Alabama shad since this r strategist species is prone to high natural variability and long-term studies would be necessary to reveal any population trajectory.

In reviewing data provided by the Florida Fish and Wildlife Conservation Commission (FFWCC) during the public comment period on the positive 90-day finding (J. Wilcox, FFWCC, pers. comm. to K. Shotts, NMFS, November 12, 2013), less than 50 Alabama shad were reported since 1999. The shad were collected during multispecies surveys not specifically targeting Alabama shad. The research with positive reports of Alabama shad was conducted using otter trawls, seines, and electrofishing during winter (December, January, February), spring (May), summer (June, July, August), and fall (September, October, November) months between 2002 and 2011. It is notable that none of the FFWCC surveys were conducted in March or April, when the largest catches of Alabama shad have occurred during targeted research in the ACF River system (Kern 2016, Sammons 2013, 2014). Further, although FFWCC caught less than 50 Alabama shad from 2002-2011, researchers targeting Alabama shad in the ACF River system captured 128-1,497 Alabama shad per year during an overlapping time period (2005-2011; Young 2010, 2011). This demonstrates the importance of the sampling gear and time of year in interpreting available data and why short-term and/or non-targeted research is not always a good indicator of distribution and abundance.

Even studies designed to target Alabama shad have yielded difficulties in detecting the species. Researchers studying Alabama shad in the ACF River system noted they had great difficulty finding Alabama shad in portions of the Flint River and expressed their surprise at the difficulty, given the small size of the river (Kern 2016; S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, Jim Woodruff Lock and Dam (JWLD) Fish Passage Year-End Summary Meeting, January 2014; S. Sammons, Auburn University, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2015). Large gaps in detections of Alabama shad were observed in the Flint River (Kern 2016; S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2014; S. Sammons, Auburn University, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2015). Alabama shad were detected at upstream and downstream locations on acoustic receivers, but were not detected by receivers in between. Multiple methods were used with limited success to improve the detectability of Alabama shad, including passive (anchored receivers), boat, and airplane tracking of acoustically and radio-tagged shad (S. Sammons, Auburn University, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2015). Kern (2016) believed a combination of behavioral and environmental factors reduced the detectability of Alabama shad. Kern (2016) notes there are many “blue hole” springs along the river's length that are substantially deeper than the surrounding river and it is possible that Alabama Shad may use these features as refugia during the spawning migration. High water conditions were also experienced during portions of the sampling period. Kern (2016) stated that increased water depth during periods of high river discharge, swimming depth of Alabama Shad, and the presence of significantly deeper habitats than what is available in the rest of the river could lead to decreased detection probability by exceeding the detection range of passive and manual receivers. Kern (2016) also noted that Alabama shad are capable of long, rapid migration runs and if those migration runs occur at night, Alabama shad will not be detected by manual tracking (from boats and airplanes) that occurs exclusively during the day. The same detection problems (gaps in Alabama shad detection at receivers between two positive detection points) were experienced during Alabama shad conservation locking studies in the Alabama River system (Kern 2016; S. Sammons, Auburn University, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2015).

It is unknown to what degree the lack or low numbers of Alabama shad reported for many river systems accurately reflects the abundance in those systems or whether it is indicative of the lack of targeted studies or the detectability of this species.

Distribution and abundance information is summarized below by rivers, starting with the Apalachicola River where we have the most information regarding Alabama shad, then information is presented by rivers from west to east.

Apalachicola River Drainage

The Apalachicola River drainage is made up of the Apalachicola, Chattahoochee, and Flint Rivers and drains water from parts of Florida, Alabama, and Georgia. Alabama shad were known to have migrated from the Apalachicola River up the Chattahoochee River to Walter F. George Reservoir in the early 1970s (Smith

et al.

2011), even with the construction downstream of the Jim Woodruff Lock and Dam (JWLD) in the early 1950s and George W. Andrews Lock and Dam in the early 1960s. Alabama shad were able to pass upstream and downstream when the navigation locks were open. Located at the confluence of the Chattahoochee and Flint Rivers, JWLD is the first major obstacle on the Apalachicola River to the upstream migration of Alabama shad to their historical spawning grounds. River traffic on the Apalachicola River resulted in the lock being operated frequently, allowing passage and sustaining reproduction of the resident Alabama shad population. Historically, JWLD was operated continuously 24 hours per day for commercial barge traffic (Sammons 2013). With the elimination of commercial traffic in the late 1960s, lock operation was reduced to 8 hours per day for on-demand passage of recreational boats, reducing the number of lockages to less than 100 per year from a high of 1200. Barge traffic decreased and lock operation became less frequent when navigational dredging ceased in 2001 (J. Wilcox, FFWCC, pers. comm. to K. Shotts, NMFS, November 12, 2013). Researchers believe Alabama shad spawn in shoal habitat downstream of JWLD based on observations of the species congregating over the shoals during spawning season, as well as usage by other spawning anadromous species, such as Gulf sturgeon (

Acipenser oxyrinchus desotoi;

T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016).

During the public comment period, the FFWCC reported collecting fewer than 50 Alabama shad in the lower Apalachicola River since 1999 (J. Wilcox, FFWCC, pers. comm. to K. Shotts, NMFS, November 12, 2013). In reviewing the data provided by FFWCC during the public comment period on the positive 90-day finding, the fewer than 50 Alabama shad reported since 1999 were collected during multispecies surveys (

i.e.,

Alabama shad were not specifically targeted). The research with positive reports of Alabama shad was

conducted using otter trawls, seines, and electrofishing during winter (December, January, February), spring (May), summer (June, July, August), and fall (September, October, November) months between 2002 and 2011. It is notable that none of the surveys were conducted in March or April, when the largest catches of Alabama shad have occurred during research targeting Alabama shad in the ACF River system, which occurs annually between March and May to coincide with the spring spawning migration (Kern 2016, Sammons 2013, 2014). Further, although FFWCC caught less than 50 Alabama shad from 2002-2011, researchers targeting Alabama shad in the ACF River system captured 128-1,497 Alabama shad per year during an overlapping time period (2005-2011; Young 2010, 2011). This demonstrates the importance of the sampling gear and time of year in interpreting available data and why short-term and/or non-targeted research is not always a good indicator of distribution and abundance.

The ACF River system likely contains the largest spawning population of Alabama shad within its range, although the population may be several orders of magnitude smaller than historical levels (Schaffler

et al.

2015). Because this population has remained self-sustaining even with apparent declines, a project to restore passage to upstream spawning habitats was initiated (Schaffler

et al.

2015). Beginning in 2005, a cooperative study supported by multiple local, academic, state, and Federal conservation partners started tracking movements of Alabama shad and other fish species in the Apalachicola River (USFWS 2008, Ely

et al.

2008, TNC 2010). The study also evaluated the feasibility of moving fish upriver of JWLD during the spawning season. The results of this collaborative study showed that the existing lock at JWLD could be operated to allow fish to move upriver through the lock where they could access additional spawning habitat. Based on these results, U.S. Army Corps of Engineers (USACE) began “conservation locking” (operating the lock at JWLD to provide Alabama shad access to upstream habitat) in 2005.

In 2012, the “cooperator” organizations (USACE, USFWS, NMFS, Georgia DNR, FFWCC, and TNC) signed a Memorandum of Understanding (MOU) clarifying their commitments and responsibilities in the continued implementation of fish passage at JWLD. The contents of the MOU are described in more detail in the “Regulations on Dams” section in “

D. Inadequacy of Existing Regulatory Mechanisms.

” In fulfillment of the cooperation outlined in the MOU, an annual meeting to discuss the issues and outcomes from the previous spring conservation locking cycle is held, usually in the early part of the following year (

i.e.,

January or February). At the annual meetings, the cooperators and other interested parties (

e.g.,

universities that are not signatories to the MOU, but are heavily involved in research activities associated with the conservation locking in the ACF River system) discuss lessons learned from the previous year and participate in planning the next cycle of spring conservation locking, including whether the locking operation and schedule can be improved. For example, during the planned lock maintenance that occurred during the 2013-2014 season, the cooperators were able to upgrade the method of delivering the attractant flow (a stream of high velocity water used to attract spawning fish) from a manual system to an electric pump as a more efficient way to direct shad through the lock when conservation locking resumed (S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2014).

Population abundance estimates for Alabama shad in the ACF River system were determined through mark-recapture methods from 2005-2016. The estimated abundances for 2005-2016 are listed in the following table (the asterisks indicate years in which no conservation locking occurred due to maintenance and upgrades to the lock at JWLD). The table also shows the catch per unit effort (CPUE) of adult and juvenile Alabama shad during spring and fall sampling, respectively.

Table 1—Adult and Juvenile Alabama Shad Research Results in the ACF River System

Year

Adult

population

estimate

(spring)

Confidence interval

(spring)

Adult CPUE

(spring)

Juvenile CPUE

(fall)

2005

25,935

17,715-39,535

20.47

n/a.

2006

2,767

838-5,031

6.10

0.1.

2007

8,511

5,211-14,674

13.17

5.75.

2008

5,253

1,592-9,551

13.00

16.17.

2009

10,753

3,258-19,551

9.20

0.

2010

98,469

51,417-127,251

7.17

22.4.

2011

26,193

22,371-43,713

72.93

25.

2012

122,578

57,911-282,872

100.6

1.9.

2013 *

2,039

618-3,706

17.2

1.33.

2014 *

n/a

n/a [86 fish captured; no re-captures]

6.5

3.33.

2015

324

58-3,240

6.8

0.

2016

n/a

[0 fish captured]

0

CPUE not yet calculated [20 juveniles captured].

In the period of conservation locking, Alabama shad have been successfully passed through the navigational lock at the most downstream dam on the ACF, JWLD, providing upstream migration to higher quality spawning and juvenile rearing habitat, which has potentially improved recruitment and lead to population increases (Ely

et al.

2008, Young

et al.

2012, Schaffler

et al.

2015). Since conservation locking began, Alabama shad have been reported above JWLD in both the Chattahoochee River and the Flint River (2008-2010) by the Georgia DNR (Smith

et al.

2011). The USACE reported Alabama shad in Lake George W. Andrews in the Chattahoochee River during recent sampling of the area (Smith

et al.

2011). Only a few Alabama shad have been found in the Chattahoochee River, with the vast majority being found in the Flint River (Young 2010). In years when conservation locking occurred, the locks were operated twice a day to correspond with the natural movement patterns of migrating fish during spawning seasons (February through May) each year. During conservation locking, acoustically tagged Alabama shad

released below the dam have been found to pass upstream of the lock with 45 percent efficiency (Young 2010). Alabama shad can more easily access over 150 mi (241.4 km) of historical habitat and spawning areas in the ACF River system for the first time in more than 50 years now that the lock is operated to correspond with their natural spawning cues (TNC 2010).

Schaffler

et al.

(2015) completed a study on shad collected in 2010 and 2011 to determine whether fish passage efforts at JWLD were contributing recruits to the adult Alabama shad population. They evaluated otolith (inner ear bone) chemistry from spawning adult Alabama shad to determine the river reach within the ACF basin the fish originated from. They first examined the otolith chemistry of known-origin juveniles captured in freshwater reaches both upstream and downstream of JWLD. Then, they compared the distinct chemical signatures of the juvenile otoliths to those from returning spawning adults of unknown origin captured below the dam to assign river-reach natal origins. The results showed that the Flint River, inaccessible to Alabama shad prior to conservation locking, is the dominant source of recruits returning to spawn in the ACF River system making up 86 percent of the individuals captured. Schaffler

et al.

(2015) found no evidence that collection year, sex, or age impacted the origin of returning Alabama shad in the ACF River system, meaning the Flint River produced the majority of recruits in the ACF River system for the 2008-2010 cohorts of both males and females. The results from this study indicate that conservation locking is making a tremendous contribution to Alabama shad in the ACF River system, the bulk of the Alabama shad population in the ACF River system is spawning in the Flint River, and juvenile Alabama shad are able to successfully move downstream to contribute to the adult stock.

In 2005, the population estimate in the ACF River system was about 26,000 individuals, but decreased to less than 10,000 in both 2006 and 2007 (Ely and Young 2008). In 2008 and 2009, mark-recapture methods yielded an Alabama shad population estimate of approximately 5,200-10,700. However, one of the researchers noted that the Alabama shad population estimates for 2008 and 2009 (5,253 and 10,753 shad, respectively) are likely underestimates of the actual population numbers based on the results of a companion electrofishing study by Clemson University (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, February 8, 2016). Based on a predictive model developed by Clemson, the 2008 and 2009 Alabama shad population estimates would be closer to 8,500 and 26,000 shad, respectively.

Young (2010) estimated the number of Alabama shad in the ACF River system at 98,469 in 2010, almost 4 times larger than the previous high estimate of 25,935 in 2005 (Ely

et al.

2008). Alabama shad were the most abundant species observed in the Apalachicola during spring sampling in 2010 (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016).

Within the ACF River system, the number of Alabama shad in 2011 was estimated at 26,193; this is lower than the 2010 value but slightly higher than the maximum abundance in the 2005-2009 period (Young 2011). The major difference between the 2010 and 2011 Alabama shad spawning runs was a lack of age-1 males in 2011. Ingram (2007) noted that fewer age classes and lower numbers of older, more mature, fish are indicative of a declining population. The 2011 run was dominated by older, larger adult females in excellent condition, a potential indicator of strong year classes in the future (Young 2011). Sammons and Young (2012) provided a report from the Apalachicola River, estimating the number of Alabama shad at 122,578 in 2012 (the largest since 2005). This spawning run was composed of many males presumed to be from the 2010 year class, as well as numerous older, larger adults of both sexes (presumably recruits from 2008 and 2009). In 2012, the abundance of 3- and 4-year-old fish made up the largest percentage of spawning Alabama shad, rather than 1- and 2-year-olds as in previous years (Ingram 2007), indicating a healthier population (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). Sammons and Young (2012) noted that a year of higher than average flows in 2009 may have contributed to spawning and recruitment successes in 2010 and 2012.

While conservation locking of Alabama shad at JWLD and monitoring of Alabama shad populations in the ACF River system continue to receive support and funding Alabama shad were not passed through the lock in 2013 and 2014 due to maintenance on the structure. However, 74 Alabama shad out of a total of 251 captured by researchers during 2013 were tagged and transported above JWLD and released (Kern 2016, Sammons 2013) in order to access habitat above the dam. Of the 74 tagged fish, 11 were verified as post-release mortalities, with another 3 suspected mortalities (Sammons 2013). It is unknown whether Alabama shad not captured by researchers successfully spawned at the shoal habitat below JWLD where they spawned prior to conservation locking (

Acipenser oxyrinchus desotoi;

T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). Also, during the maintenance period on the lock, the method of delivering the attractant flow (a stream of high velocity water used to attract spawning fish) was upgraded from a manual system to an electric pump as a more efficient way to direct shad through the lock when conservation locking resumed (S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2014).

Conservation locking appears to have enhanced spawning and recruitment of Alabama shad in the ACF River system (Young 2010, 2011, Sammons and Young 2012, Schaffler

et al.

2015). Although the ACF population of Alabama shad has been the largest known population for decades (Laurence and Yerger 1967), the lack of conservation locking in 2013 and 2014, combined with environmental conditions (cold and flooding) and the poor condition of spawning fish (discussed below), likely produced the weakest year class since research began on Alabama shad in the ACF River System in 2005. However, environmental conditions (cold, flooding, and the presence of large debris) and funding levels also hampered researchers' ability to survey the Alabama shad population in the ACF River system in 2013-2015 to develop reliable population estimates.

The Alabama shad population sampled below JWLD during the 2013 spawning season was low compared to previous seasons (Sammons 2013). A total of 309 Alabama shad were captured below JWLD and of those fish, 87 fish were tagged and 1 was recaptured, resulting in a population estimate of 2,039 Alabama shad (Sammons 2013). Sammons (2013) noted that most Alabama shad collected below JWLD in 2013 were in poor physical condition, with visible wounds (this will be discussed further in “C. Disease and Predation”). The wounds were observed only on adult fish and not on younger fish, indicating the source may have occurred in the Gulf of Mexico (Sammons 2013). The wounds were also not observed on other anadromous species, indicating Alabama shad are either more susceptible to the source of the wounds or they are distributed in areas that the other species are not (Sammons 2013).

The wounds remain unexplained, but Sammons (2013) cited a news article reporting gash wounds on fish potentially associated with the Deepwater Horizon Oil Spill resembling the wounds found on Alabama shad. Sammons (2014) also cited Murawski

et al.

(2014) noting the anecdotal reports of skin lesions in offshore fish species in 2010 and 2011, but the symptoms declined by 2012. The sores have not been observed in any Alabama shad captured since 2013 (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016).

The Alabama shad captured below JWLD were tagged and/or released approximately 5 km above the dam (Sammons 2013). Most of the Alabama shad were relocated (detected again after release) in Lake Seminole just above the dam, but some fish were detected moving into the preferred spawning habitat in the Flint River (Sammons 2013). Although fewer fish were detected making a spawning run than in previous years, Alabama shad traveled greater distances from the area they were released in 2013 than in previous years (Sammons 2013).

Reasons for the lack of fish found below JWLD are unknown, but unusually cold water temperatures due to cooler weather patterns present throughout the Apalachicola River Basin in 2013 may have been a contributing factor (Sammons 2013). Water temperature serves as one of the main cues for Alabama shad to enter the ACF River system to spawn (Kern 2016, Sammons 2013). The researchers suspect that many Alabama shad had not yet entered the Apalachicola River to spawn during their sampling effort in the river, and this factored into the low numbers captured during 2013.

In 2014, 102 Alabama shad were captured below JWLD; 86 were tagged and released above JWLD (Sammons 2014). No fish were recaptured and a population estimate could not be calculated (Sammons 2014). Since conservation locking did not occur in 2013 or 2014 due to maintenance of the lock, Alabama shad likely did not pass upstream except for those transported by researchers. Sammons (2014) noted that the Alabama shad captured in 2014 were smaller than shad captured in the previous two years, but that the fish were in better condition and did not exhibit the wounds as the majority of the population did in 2013. Although few adult Alabama shad were captured in the spring 2014, juvenile Alabama shad were collected in the fall sampling above JWLD in 2014 (CPUE of 3.3 in the table above), indicating that adult Alabama shad had successfully passed upstream and spawned (P. Freeman, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, February 2016). Despite no abundance estimate being produced, juvenile CPUE in 2014 was higher than CPUEs in the 2 previous years.

Given the low numbers, Sammons (2014) believes that weak year classes were produced in 2013 and 2014. However, Sammons (2014) stated that water levels and temperature may have factored in to the low catches in 2014. Water levels and discharge were much higher during Alabama shad sampling in 2014 than in the previous 2 years and the mean catch rate of Alabama shad below JWLD was inversely correlated with mean daily discharge over the past 5 years (Sammons 2014). High water and discharge may have hindered catch rates, but spawning population size was also likely low (Sammons 2014). Reasons for the lack of fish found below JWLD are unknown, but may have also involved unusually cold water temperatures. As in 2013, water temperature was generally more than 2-4 °C cooler throughout the spawning season than in 2011 or 2012 (Sammons 2014). Abnormally low water temperatures in the Apalachicola River throughout the spring in 2013 and 2014 may have inhibited the usual spawning migration cues of this species, resulting in fewer fish migrating upstream (Sammons 2014). Sammons (2014) stated it is possible that a significant spawning population of this species persists in the Gulf of Mexico waiting for more normal spring conditions to return to the river before initiating their spawning run.

In 2015, conservation locking resumed, but the Alabama shad population estimate remained low (324 fish). Due to the lack of conservation locking in 2013 and 2014, and potentially the lack of successful spawning due to the poor condition of the Alabama shad observed in 2013 (Sammons 2013, 2014), it is probable that the actual number of returning adult Alabama shad in 2015 was low. Similar to the previous year, researchers noted factors that may have reduced their capture rates, such as high water levels and large amounts of debris in the river that hampered sampling, potentially leading to the low number of recaptures and the low population estimate (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, February 3, 2016).

In 2016, high water levels occurred early in the sampling season, but later returned to normal levels (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). No Alabama shad were captured in the Apalachicola River in 2016, and therefore an abundance estimate could not be produced for that year (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). However, Alabama shad were observed lower in the Apalachicola River by another researcher conducting striped bass surveys (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). The Alabama shad survey occurred about 2 km downstream of JWLD (Sammons 2014) and therefore would not have encountered Alabama shad occurring downstream of that location. The gill-netting survey conducted in Lake Seminole above JWLD to detect juvenile Alabama shad occurred in mid-December 2016 and produced 20 juvenile Alabama shad. Even though no adults were captured in the spring survey, the collection of juvenile shad above JWLD indicates that some adult Alabama shad did successfully pass through the lock and spawn in the ACF system in 2016 (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, December 15, 2016). At the time this 12-month determination was prepared, the researchers had not yet calculated the CPUE for the juvenile survey.

Funding levels and research effort may also have contributed to the differences in abundance estimates between 2013-2016 (low number of fish captured) and 2009-2012 (large number of fish captured). Funding levels were much higher in 2009-2012 and researchers were pursuing additional research questions beyond population estimates that required them to capture more fish (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). From 2009-2012, researchers logged more research time on the Apalachicola River and targeted higher numbers of Alabama shad, which produced robust population estimates. As noted, environmental conditions greatly hampered research efforts in 2013-2015. It is unknown whether catch rates were influenced by environmental factors in 2016 or were strictly a reflection of very low population numbers, but reduced funding further exacerbated researchers' ability to increase survey efforts to offset research difficulties or to opportunistically take advantage of improved environmental conditions when they occurred (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). The differences in the trends in Alabama shad adult population estimates and the CPUE of adult Alabama shad between 2005-2016

can partially be explained by the differences in sampling effort levels due to both environmental conditions and funding levels (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016), although researchers believe the Alabama shad spawning populations in the ACF River system in 2013-2016 were smaller, especially compared to the 2009-2012 spawning populations.

As described above, low numbers of Alabama shad were captured in 2013-2015 and no adult Alabama shad were captured in 2016, producing low or no population estimates. From 2013-2016, the primary cause of low Alabama shad captures is likely that low numbers of Alabama shad returned to spawn in the ACF River system during those years (Sammons 2013, 2014, T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016). Conservation locking did not occur in 2013 and 2014 due to maintenance and improvements on the lock. Some Alabama shad captured by researchers were transported and released above JWLD, but the remaining fish in the population likely only had access to any downstream spawning habitat (Sammons 2013, 2014). However, while conservation locking appears to have significantly increased spawning and recruitment success of Alabama shad and expanded the species' access to additional habitat in the ACF River system, the ACF population has been the largest known population of Alabama shad for decades (Laurence and Yerger 1967) even before conservation locking occurred. The poor condition of Alabama shad in 2013, when most fish collected had unexplained external wounds (Sammons 2013, 2014), potentially led to poor spawning success and fewer returning spawners in the following years. The CPUE of juvenile Alabama shad in the Flint River in the fall of 2013 was low, although not the lowest observed and similar to the CPUE for 2012, which had the highest adult population estimate recorded since research commenced in 2005.

Environmental conditions may have affected both shad spawning activities and the ability of researchers to detect shad. Cold temperatures in 2013 and 2014 may have postponed the spring spawning runs until temperatures increased later in the season (and after Alabama shad research had already ceased), or the majority of Alabama shad may have forgone their annual spawning run and remained in their marine habitat (Sammons 2014). Water levels and discharge were much higher during Alabama shad sampling in 2014 than in the previous 2 years and may have hindered catch rates. The mean catch rate of Alabama shad below JWLD was inversely correlated with mean daily discharge over the past 5 years (Sammons 2014). This is similar to observations in other systems, and can mean high river discharge delayed or hindered spawning runs or affected the ability of researchers to capture shad. Kern (2016) found that the number of detections of tagged Alabama shad in 2013 and 2014, as well as the extent of upstream migration by shad, appeared to be influenced by river discharge, with the lowest number of detections and least amount of upstream movement occurring during years with relatively high river discharges. Sammons (2014; citing Holman and Barwick 2011, and Pierce

et al.

1985) noted that the inverse relationship between capture of fish by electrofishing results and high water level is well known. Alabama shad detection in general proved surprisingly difficult to researchers, in both the ACF River and the Alabama River systems, with large gaps in detections between areas where Alabama shad were known to have occurred (Kern 2016; S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2014; S. Sammons, Auburn University, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2015). Funding levels and research effort may also have contributed to the differences in abundance estimates between 2013-2016 (low number of fish captured) and 2009-2012 (large number of fish captured), with higher funding levels and increased effort in 2009-2012 compared to the later years (T. Ingram, Georgia DNR, pers. comm. to K. Shotts, NMFS, June 6, 2016).

To further evaluate potential causes and effects of the low capture rates in the ACF River system in 2013-2016, we compared the adult population estimates and CPUEs from spring sampling with the CPUE of juveniles sampled above JWLD in the fall. The CPUE for juvenile shad is a metric derived from surveys designed to assess the recruitment success of Alabama shad upstream of JWLD. Given the growth rate of Alabama shad, surveys for juveniles upstream of JWLD in the fall would indicate success of the spring spawning that occurred earlier in the year. Trends in juvenile CPUE did not appear to follow trends in the adult population estimates or the adult CPUEs. Further, the trends in juvenile CPUE did not appear to reflect the trends in adult population estimates either 1 or 2 years later, when juveniles would be of spawning age. Recapture rates of tagged adult Alabama shad ranged from 0 to 2.2 percent per year for tagged shad. There was not a strong relationship (r = 0.33) between population size and CPUE, nor between population size and the number of recaptured fish (r = 0.21). However, there was a strong positive relationship between population size and the number of fish tagged (r = 0.82). Interestingly, there is a very poor fitting relationship between the number of fish tagged and the number of fish recaptured (r = 0.15), which indicates the results are potentially heavily influenced by variability in the number of recaptures in a given year. The researchers' ability to capture, but not as easily recapture fish, may provide some indication that difficulties in detecting Alabama shad during research efforts factored into the low population estimates in addition to the actual population size being low.

The low catch rates of Alabama shad in 2013-2016, although potentially influenced by environmental conditions, detection ability, and research effort, primarily indicate that Alabama shad populations were much lower during those years than in the previous years of research since 2005. However, for an r strategist species such as Alabama shad that is inherently prone to high levels of natural variability, it is very difficult to interpret a population trend from 11 years of population estimates, with no historical abundances available for comparison. The abundance estimates for Alabama shad in the ACF River System demonstrate that the abundance in the system for the 11-year period is highly variable, and no population trend is apparent. The confidence intervals around each of the abundance estimates in the table show the wide range of uncertainty inherent in the abundance data.

Based on the life history strategy of the species and the short period over which abundance estimates have been available, we cannot discern a pattern or trend in the Alabama shad population in the ACF River system. As an r strategist, Alabama shad have high natural mortality that is balanced by a high growth rate (Adams 1980). R strategist populations are well-adapted to cope with unstable, unpredictable environments, and this also produces high natural variability in their populations (Elliott and Quintino 2007). Adams (1980) noted that fisheries for r strategists are “boom or bust,” and although catches can be very large some years, they will be characterized by erratic production levels overall.

Alabama shad belong to the clupeoids, an order of fish that show striking interannual or decadal variation in productivity and abundance, with the ability to persist at extremely low population numbers for 50-100 years then undergo a remarkable recovery with the population growing as fast as 40 percent per year (Mace et al. 2002). Sammons (2013) also noted that increases of Alabama shad populations can happen very quickly, as demonstrated by the rapid rise in population size between 2006-2009 and 2010-2012 (Sammons 2013). While the Alabama shad population appears to be much smaller based on the last 4 years of tag-recapture data as compared to the previous 7 years, we did not detect a discernable trend, the high interannual variability is not unexpected for this species, and the species is adapted to recover from very low numbers of fish, even if the population persists at depressed levels for long periods of time.

The studies in the ACF River system have produced the only abundance estimates, either historical or current, for Alabama shad in any river system. The following sections of the determination present the historical and current distribution of Alabama shad in other systems, which is primarily based on capture data from general multi-species surveys, project monitoring, captures incidental to other research studies, and anecdotal information.

Mississippi River

The Mississippi River is the largest river basin in North America and drains portions of Montana, the Dakotas, Nebraska, Minnesota, Wisconsin, Iowa, Illinois, Indiana, Ohio, West Virginia, Pennsylvania, Colorado, Kansas, Missouri, Kentucky, Tennessee, Texas, Oklahoma, Arkansas, Mississippi, and Louisiana. Alabama shad were historically found in parts of the Mississippi River and its tributaries and several small spawning populations remain.

Upper Mississippi River Mainstem

The Upper Mississippi River is the portion of the river upstream of Cairo, Illinois. In the Upper Mississippi River, Alabama shad were recorded in the 1994 Annual Status Report: “A Summary of Fish Data in Six Reaches of the Upper Mississippi River” (Gutreuter

et al.

1997) as being captured in a long-term fish resource monitoring program. The report was compiled by the U.S. Geological Survey (USGS), Minnesota DNR, Wisconsin DNR, Iowa DNR, the Illinois Natural History Survey, and the Missouri Department of Conservation. However, the Gutreuter

et al.

(1997) report did not include specific data on Alabama shad and other species, such as the number of fish caught, gear used, the location of capture, etc. Presently, there are 10 locks and dams on the Upper Mississippi River (north of the confluence with the Ohio River) that border the state of Iowa and an additional seven locks and dams south of the state that could prevent Alabama shad from reaching historical spawning grounds within Iowa (Steuck

et al.

2010). In 1915, 48 Alabama shad were collected from the Upper Mississippi River near Keokuk, Iowa, and it was reported that some of these fish were able to make it past the Keokuk Dam (Lock and Dam #19) farther upstream (Coker 1928). Iowa DNR has collected no Alabama shad in the Upper Mississippi River in the areas between Lock and Dams #16 and #19 in the last 25 years (Smith

et al.

2011). Barko's study (2004b) in the Upper Mississippi River, near the confluence of the Ohio and Missouri Rivers, found no Alabama shad between 1994 and 2000. A species richness study conducted by Koel (2004) indicates that the Upper Mississippi River in the state of Illinois does not support Alabama shad. The Upper Mississippi River Conservation Committee also indicated that there are only historical records of Alabama shad in the Upper Mississippi River, and none have been caught in over 10 years (Steuck

et al.

2010). However, Wilcox (1999) and Ickes (2014) both list Alabama shad as being present in the Upper Mississippi River.

Missouri River

The Missouri River is a major tributary of the Mississippi River and flows through Montana, North and South Dakota, Nebraska, Iowa, Kansas, and Missouri. The lower Missouri River and its tributaries, located in the center of Missouri, probably supported the greatest number of Alabama shad in the state, although the records are limited (Smith

et al.

2011). The Missouri Fish and Wildlife Information System, maintained by the Missouri Department of Conservation (MDC), states that Alabama shad spawn in the Missouri River and two of its tributaries, the Gasconade and Osage Rivers (MDC 2015, Pflieger 1997). The MDC's earliest record of an Alabama shad in the Gasconade River was 23 fish collected in 1947 (C. Gemming, MDC biologist, pers. comm. to J. Rueter, NMFS, September 21, 2016). A study determining the habitat use of juvenile fish in the lower Missouri River did not identify Alabama shad as being present between 1987 and 1988 (Brown and Coon 1994). However, Galat (2005) recorded the presence of the species in the Lower Missouri River in 2005, and stated that Alabama shad are rare in the Ozark Plateaus region in southern Missouri. The MDC reported the collections, by trawl and electrofishing, of Alabama shad from the Gasconade River (41 fish in 1989, 4 fish in 1997, 17 fish in 2000, and 26 fish in 2012); the purposes and locations of those studies were varied (

e.g.,

project monitoring and fish surveys) and they were not directed at collecting Alabama shad (C. Gemming, MDC biologist, pers. comm. to J. Rueter, NMFS, September 21, 2016).

Meramec River

The Meramec River is a tributary of the Mississippi River whose confluence is just south of the confluence of the Missouri River. The entire length of the river is contained within Missouri. Alabama shad were known to spawn in the Meramec River prior to 1978 (Mills

et al.

1978) and a second spawning location in the river was discovered in the Big River tributary (Mills

et al.

1978). Between 1980 and 1997, 88 juvenile and 8 adult Alabama shad were captured in Missouri rivers, including the Meramec River (Pflieger 1997). The University of Tennessee reported the collection of 33 Alabama shad from the Big River shoals in 1990 (Fishnet2 2016, Catalogue #29.12) Burr

et al.

(2004) and Buchanan

et al.

(2012) list the Meramec as one of the remaining spawning rivers of Alabama shad. The Missouri Fish and Wildlife Information System, maintained by the Missouri Department of Conservation, also states that Alabama shad spawn in the Meramec River (MDC 2015).

Lower Mississippi River Mainstem

The Lower Mississippi River is the portion of the river downstream of Cairo, Illinois. Alabama shad historically used the Mississippi River as a means to reach many of its tributaries, but none have been found in the lower portion of the waterway in recent years. Surveys conducted by USACE on the Lower Mississippi River (north of Baton Rouge, Louisiana) in the early 1980s show a slow decline in the number of adult and juvenile Alabama shad (Pennington 1980, Conner 1983, Smith

et al.

2011). From the Thibodaux Weir on Bayou Lafourche, between Donaldsonville and Raceland, Louisiana, a single Alabama shad was caught using a gillnet in March of 2006 (Dyer 2007). Three Alabama shad were caught in Louisiana just west of Atchafalaya Bay between 1992 and 1996 by the Louisiana Department of Wildlife

and Fisheries (Smith

et al.

2011). However, no records of shad have been reported in recent years in annual fish surveys conducted by USGS in other Louisiana streams and rivers (Smith

et al.

2011).

Ohio River

The Ohio River is the largest tributary by volume of the Mississippi River and flows through Pennsylvania, Ohio, West Virginia, Kentucky, Indiana, and Illinois. Although the species was present and abundant enough to support a small and brief commercial fishery during the late 19th century and early 20th century in Ohio, by 1989 the majority of Alabama shad had been extirpated from the Ohio River (Pearson and Pearson 1989). The USGS has not collected any Alabama shad from the Ohio River since 1993 and the USFWS has no records of Alabama shad in its database (Smith

et al.

2011). Hammerson (2010) cites that Etnier and Starnes (1993) recorded the collection of a large adult from the Tennessee River (which flows into the Ohio River) just below Kentucky Dam in Marshall County, Kentucky, in July 1986. However, there have been no recent observations or collections of the species in the Tennessee River (Smith

et al.

2011). Although the species was once present in the Clinch and Stones Rivers (tributaries of the Tennessee River), no collections of Alabama shad were made in these systems after 1993 (Hammerson 2010, Etnier and Starnes 1993). Historically, the Wabash River, another tributary of the Ohio River, was said to have a “very limited number” of Alabama shad in its waters in the mid-1800s (Daniels 1860).

Arkansas River

The Arkansas River is a major tributary of the Mississippi River that drains Colorado, Kansas, Oklahoma, and Arkansas. Alabama shad have not been collected in the Arkansas River since an 1892 collection of one specimen in the Mulberry River tributary (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013). A few specimens were captured from the Poteau River, a tributary of the Arkansas River, prior to the 1950s (Cross and Moore 1952), but Lindsey

et al.

(1983) stated the species' status was unclear. A compilation of 20 years of fish collection data from Arkansas riverine systems by Matthews and Robison (1988) indicated no records of Alabama shad. The species may have been extirpated from the watershed by the construction of dams in the McClelland-Kerr Arkansas River Navigation System in the early 1970s (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013).

Red River

The Red River, a major tributary of the Mississippi River, flows through Texas, Oklahoma, Arkansas, and Louisiana. The Washita, North Fork, Kiamichi, and Little Rivers, as well as Lake Texoma, are part of the Red River system. A compilation of 20 years of fish collection data from Arkansas riverine systems by Matthews and Robison (1988) indicated no records of Alabama shad in the Arkansas portion of the river. During a 6-year sampling period from 1996-2001, no Alabama shad were caught in the Red River (Buchanan

et al.

2003). In a study on the effects of land alterations on fish assemblages, Rutherford

et al.

(1992) found no shad in the Little River. Presumably, Alabama shad are no longer able to reach their former spawning grounds in the Little River due to degradation of river habitat as a result of land modification (Buchanan

et al.

2003). No Alabama shad were collected from Lake Texoma or any of its adjoining rivers (Red and Washita Rivers) between 1948 and 1958 (Riggs and Bonn 1959). The Denison Dam likely excluded the species from these areas. The Altus Dam also likely excluded the species from Red River tributaries, including the North Fork, Brier Creek, and Kiamichi River, since there are no longer reports of Alabama shad (Winston and Taylor

et al.

1991, Matthews

et al.

1988). In recent years, during general river surveys conducted by the University of Oklahoma, Alabama shad have not been collected in southeast and central Oklahoma (Smith

et al.

2011).

Illinois and Marys Rivers

The Illinois and Marys Rivers are both minor tributaries of the Mississippi River contained solely within the state of Illinois. While there are historical records of shad within Illinois rivers (Smith

et al.

2011), the historical abundance of Alabama shad in Illinois is not known. The first collection of Alabama shad from the Illinois River was 47 fish taken in 1950 (Moore 1973). In a thorough report of the biodiversity of the state's rivers and streams, Page (1991) found no evidence of Alabama shad. However, Burr

et al.

(1996) reported two juvenile Alabama shad, one near the mouth of the Marys River in 1994 and one in the Grand Tower in Devils Backbone Park in 1995. These two captures support the hypothesis that some adult shad were able to spawn in these areas during that time. Before these two captures, the last Alabama shad to be captured in Illinois was a juvenile in 1962 (Burr

et al.

1996). Alabama shad appear to have been extirpated from many Illinois rivers and are considered rare in the state. Annual field studies conducted in the Illinois River by Illinois State University have resulted in no additional records of Alabama shad (Smith

et al.

2011).

White River

The White River is a minor tributary of the Mississippi River that flows through Missouri and Arkansas and was recently discovered to contain a spawning population of Alabama shad (Buchanan

et al.

2012). Matthews (1986) reported that no Alabama shad were found in White River tributaries from 1972-1973 or 1981-1983. However, the Arkansas Fish and Game Commission provided information during the public comment period on our 90-day finding that three Alabama shad were collected from the White River in 2006 (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013). Buchanan

et al.

(2012) were the first to report the species in the White River drainage when they collected 3 juvenile Alabama shad over a sand-gravel bar in August 2006. The researchers believe the shad were spawned in the mainstem White River or one of its tributaries and they noted that the morphology and size of the White River specimens compared well with Alabama shad previously reported from other drainages in the state.

Ouachita River

The Ouachita River is a minor tributary of the Mississippi River and flows through Arkansas and Louisiana. The Ouachita River system includes the Little Missouri and Saline Rivers. The Ouachita and Little Missouri Rivers contain spawning populations of Alabama shad (Buchanan

et al.

1999). Four pre-1900 records of Alabama shad from the Ouachita River are known: One specimen near Hot Springs and three at Arkadelphia (Buchanan

et al.

1999). Buchanan

et al.

(1999) reported that 16 juvenile specimens were collected from the Saline River in 1972 and 3 juvenile specimens at the juncture of the Little Missouri and Ouachita rivers in 1982. Buchanan

et al.

(1999) collected over 300 juvenile Alabama shad from the Ouachita River and the Little Missouri River between 1997 and 1998, and noted that Alabama shad were abundant at the four sites where they were collected. Buchanan

et al.

(1999) also documented a 1.3-kilogram (kg) adult taken on an artificial lure in April 1997

in the Ouachita River below Remmel Dam. The Arkansas Fish and Game Commission provided information during the public comment period on our 90-day finding that 10 Alabama shad were collected from the Ouachita River in 2005 during a survey to evaluate the influence of increased minimum flows after the relicensing of the Remmel Dam (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013). Several Alabama shad from the Ouachita River were also collected and photographed on October 12, 2012, for the purpose of illustrating a new edition of the “Fishes of Arkansas” (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013).

Although the Saline River in Arkansas is the only free flowing river left in the state, there have been no recent reports of Alabama shad (Buchanan 1999). The Monroe Museum of Natural History at the University of Louisiana has 16 Alabama shad that were collected from the Saline River in 1972 (Buchanan

et al.

2012). During the public comment period on the 90-day finding, the Arkansas Fish and Game Commission provided information from Layher

et al.

(1999) that their targeted assessment of Alabama shad at 80 sites in the Saline River did not encounter the species in the 4,863 fish collected and that severe drought conditions may have influenced the results (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013). Throughout the year, Arkansas State University conducts general fish sampling in the state's rivers and no captures of Alabama shad have been reported in recent years (Smith

et al.

2011).

Lake Pontchartrain, Lake Maurepas, and the Tangipahoa River

Alabama shad are only caught sporadically in the state of Louisiana, and there are limited data for the species in its rivers (Smith

et al.

2011). The Tangipahoa River begins in southwest Mississippi and drains into Lake Pontchartrain in Louisiana. Due west of Lake Pontchartrain, and connected by Pass Manchac and North Pass, is Lake Maurepas. No Alabama shad were caught in the Tangipahoa River in 1994 (Knight 1994) and none were collected in Lake Pontchartrain between 1996 and 2000. However, individuals were collected in Lake Maurepas from 1983 to 1984 and in 2009 using trawl and gillnets, indicating that some fish still pass through Lake Pontchartrain (Hastings 1987, O'Connell

et al.

2004, O'Connell

et al.

2009).

Pearl River

Multispecies studies of the Pearl River were conducted by Tulane University from 1963-1988 (Gunning and Suttkus 1990). Gunning and Suttkus (1990) looked at the relative abundance of 84 species over the course of the 25-year study, with sampling occurring at multiple stations in Louisiana and Mississippi either on a quarterly or annual basis. At stations where quarterly sampling was conducted, the spring survey occurred in February in the Mississippi portion of the river and April in the Louisiana portion of the river. Approximately 30 minutes were spent at each station unless the river was flooded and water depth limited sampling ability. Records from the Gunning and Suttkus (1990) sampling surveys show a steady decline in catches of Alabama shad. Sampling occurred in 16.1 km of the river above and below Bogalusa, Louisiana, for 25 years; a 64.4 km section of the West Pearl River was sampled for 16 years; and, a 64.4 km portion of the East Pearl River was sampled for 16 years. Between 1963 and 1965, 384 Alabama shad were caught from all river segments combined. Between 1965 and 1979, only 33 Alabama shad were captured. One Alabama shad was captured in the Pearl River between 1979 and 1988 (Gunning and Suttkus 1990). Gunning and Suttkus (1990) attributed the declining catch of Alabama shad to declining abundance of the species.

In the Gunning and Suttkus (1990) study, only one 30-minute multispecies survey was conducted during the spring once per year at some of their Pearl River stations. The studies targeting Alabama shad in the ACF River system are conducted over a 3-month period each year to ensure their collections encompass the peak spawning migration of Alabama shad, which can vary from year to year based on factors such as temperatures and river discharge (Sammons 2013, 2014, Kern 2016). Gunning and Suttkus (1990) state that the consistency of their methodology and the length of their study are sufficient to accurately indicate relative abundance. Gunning and Suttkus (1990) does provide one of the few long-term studies available for this species. However, as noted previously, low numbers of recorded Alabama shad individuals may be due, at least in part, to insufficient sampling effort during appropriate times (

i.e.,

spawning migrations) and with the appropriate gear to target the species (Mettee and O'Neil 2003). This was observed in the ACF in large differences in Alabama shad captured in multispecies surveys conducted by FFWCC (J. Wilcox, FFWCC, pers. comm. to K. Shotts, NMFS, November 12, 2013) versus studies targeting Alabama shad in ACF (Young 2010, 2011) during the same time period.

Smith

et al.

(2011) state no Alabama shad have been captured in the Pearl River since then, although FishNet contains records of Alabama shad captured from the Pearl River in 1996 by the Illinois Natural History Survey and 2004 by Tulane University (Fishnet2 2016, Catalogue #38236 and #198208).

Pascagoula River

The Pascagoula River system, made up of the Pascagoula, Leaf, and Chickasawhay Rivers, is the only system within the state of Mississippi inhabited by Alabama shad (Mickle

et al.

2010, Mickle 2010). A total of 531 Alabama shad (all age classes) were captured in the Pascagoula River system between 2004 and 2007 (307 from the Pascagoula River, 200 from the Leaf River, and 24 from the Chickasawhay River; Smith

et al.

2011). The Pascagoula River system has one of the remaining spawning populations of Alabama shad as evidenced by Mickle's (2006) collection of 193 age-0 Alabama shad from 10 sites between 2004 and 2005. The Leaf and Pascagoula Rivers contain the highest populations of Alabama shad within this system due to their unimpounded waters and variety of habitats, with a smaller Alabama shad population in the Chickasawhay River (Mickle

et al.

2010, Mickle 2010). Between 2004 and 2006, Mickle

et al.

(2010) captured 133 juvenile Alabama shad (66 from the Leaf River, 55 from the Pascagoula River, and 12 from the Chickasawhay River). Small numbers of Alabama shad were also caught in Black Creek, a tributary of the Pascagoula River, in 1986 and the late 1990s (Adams

et al.

2000).

Mobile Bay and the Mobile River Basin

The Mobile River basin spans Mississippi, Alabama, Georgia, and Tennessee. The Mobile River, which empties into Mobile Bay, branches upstream into the Alabama, Cahaba, Tallapoosa, Coosa, Tombigbee, and Black Warrior Rivers. The Alabama shad was first described as a species in 1896 in the Black Warrior River near Tuscaloosa, Alabama (Jordan and Evermann 1896). Alabama shad were once prevalent in the Mobile River basin (Evermann and Kendall 1897).

Numerous juvenile Alabama shad were recorded in the Alabama River in 1951, the late 1960s, and the early 1970s

(Boschung 1992, Mettee and O'Neil 2003). A single Alabama shad (15.3 cm) was also captured in Dog River (a small tributary draining into Mobile Bay) in 1964 (Williams and Gaines 1974, Boschung 1992, Hammerson 2010). On the Alabama River, Claiborne Lock and Dam was opened for navigation in 1969 (Freeman

et al.

2005). Upstream from Claiborne Lock and Dam, Millers Ferry Lock and Dam was constructed for the purpose of both power generation and navigation, with the lock opening in 1969 and power coming on line in 1970. Sampling in Mobile Bay in 1972 yielded no Alabama shad. Two individuals were caught in the Alabama River in the 1990s: One in 1993 below Claiborne Lock and Dam, and one in 1995 below Miller's Ferry Lock and Dam (Smith

et al.

2011). More recently, in February 2004, a single specimen (32.8 cm) was captured by the Alabama Department of Conservation and Natural Resources, Marine Resources Division, in Heron Bay (adjacent to Mobile Bay), presumably making its upstream spawning migration (Smith

et al.

2011). The Alabama Division of Wildlife and Freshwater Fisheries conducted a year-long study in 2009 in the Alabama River that did not collect any Alabama shad.

Despite the existence of a thorough historical fisheries record of the Cahaba River system, no recent captures of Alabama shad from the upper reaches of the Cahaba River are documented. Both the Pierson

et al.

(1989) general fish faunal survey of the river from 1983-1988 and the Onorato

et al.

(1998 and 2000) sampling between 1995-1997 found no Alabama shad present in the upper region of the Cahaba River. The last Alabama shad collected was in 1968 and the only previously recorded fish reported in the Cahaba River at Centreville, Alabama, was in 1965 (Onorato

et al.

2000, Boschung 1992). The last specimen to be captured from the Coosa River was in 1966 (Boschung 1992). No Alabama shad were captured during fish sampling in the Tallapoosa River by Freeman

et al.

(2001).

Mettee and O'Neil (2003) state that Alabama shad have not been found in the Tombigbee River since the 1901 construction of the Tombigbee lock system in the waterway. However, records provided by the Mississippi Museum of Natural Science during the public comment period on our 90-day finding showed that 5 Alabama shad were captured in the Tombigbee River in 1969 and one in 1971 (M. Roberts, Curator of Fishes, Mississippi Museum of Natural Science, pers. comm. to K. Shotts, NMFS, October 21, 2013). In the Black Warrior River of Alabama, where the species was first described in 1896, one Alabama shad was subsequently collected, over one hundred years later in 1998 (Mettee and O'Neil 2003).

Conservation locking, similar to efforts conducted in the ACF River system, was undertaken on the Alabama River at Claiborne Lock and Dam and Miller's Ferry Lock and Dam in 2009 by the Alabama Department of Conservation and Natural Resources, USACE, and Auburn University after USGS suggested the locks could be used as a means of fish passage (Simcox 2012). At that time, no efforts were made to quantify passage efficiency or even monitor which species may be passing upstream and downstream through the locks. Freeman

et al.

(2005) stated that substantial potential for restoring populations of migratory, large-river fishes such as Alabama sturgeon (

Scaphirhynchus suttkusi

), Gulf sturgeon, Alabama shad, and southeastern blue sucker (

Cycleptus meridionalis

) entailed modifying Claiborne and Miller's Ferry, the two downstream-most dams on the Alabama River. Enhancing fish passage at Claiborne and Millers Ferry Locks and Dams could restore connectivity between the lower Alabama River and the Cahaba River, encompassing over 400 km of riverine habitat from the Gulf to the fall line.

In 2014, a study was initiated to determine if conservation locking could be used to pass Alabama Shad upriver or downriver during spawning season through the navigation locks at Claiborne Lock and Dam and Miller's Ferry Lock and Dam. With support from the FFWCC and Georgia DNR, Alabama shad from the ACF River system were collected and tagged before being stocked in the Alabama River. Fifteen Alabama shad were tagged and released below Claiborne Lock and Dam, and an additional 38 Alabama shad were tagged and released above the dam. These fish were tracked both upstream and downstream of the dam. Of the Alabama shad released above the dam, 18 were later detected at 18 different locations, and 7 definite mortalities (no movement between successive locations) were eventually confirmed. The 7 confirmed mortalities occurred in the section of the Alabama River below Claiborne Lock and Dam to its confluence with the Tombigbee River. Kern and Sammons (2015) note that further research is necessary to determine whether Alabama shad found suitable spawning habitat in this location and halted downstream movements, or whether they died as a result of cumulative stress from handling and transport. One fish was detected approximately 53 mi (85 km) below Claiborne Lock and Dam, indicating successful downriver passage through the lock. Twenty fish were never detected. There were large areas where no tagged fish were detected, and some fish moved over 50 mi (80 km) in 2 days. “Leap-frogging” was also observed, with shad being detected at downstream and upstream locations, but escaping detection in between.

Of the 15 tagged fish released below Claiborne Lock and Dam, 3 were detected 93 times. One fish was detected 12 days after release below Gravine Island (just north of Mobile Bay) and was detected again upriver 6 days later, just below Claiborne Lock and Dam. This movement pattern indicated “fallback” (fish that move a great distance downriver shortly after stocking), but in this case, the fish eventually moved upriver. Another fish remained in the vicinity of Claiborne Lock and Dam for 9 days and was not detected thereafter. A third fish was detected several times moving downstream after release but not later. No tagged Alabama shad were detected above Claiborne Lock and Dam and researchers hypothesized this low number could have been due to high water events or mortalities.

In 2015, 27 Alabama shad from the ACF River system were tagged and stocked below Miller's Ferry Lock and Dam (and above Claiborne Lock and Dam). Detections of tagged fish were much higher in 2015 than 2014, likely due to higher river flows in 2014 (Kern and Sammons 2015), with 17 of the 27 fish detected for a total of 371 detections. Similar to 2014, large movements over short time periods were observed, with most of the movements being in a downstream direction. No fish were found to have successfully navigated upstream of Miller's Ferry Lock and Dam, although many of the fish passed downstream of Claiborne Lock and Dam.

Escambia River and Conecuh River

The Conecuh River begins in Alabama and becomes the Escambia River at the Florida border. Alabama shad were documented in the Escambia/Conecuh River system as early as 1900 (Evermann and Kendall 1900). This system contains one of the known remaining Alabama shad spawning populations (Smith

et al.

2011). Bailey (1954) reported the capture of two individuals in the Escambia River in 1954. In 2009, two Alabama shad were caught in the Escambia River by FFWCC, one in spring and one in the fall (Smith

et al.

2011; E. Nagid, FFWCC, pers. comm. to K. Shotts, NMFS, November 26, 2014). Studies indicate there are small populations of Alabama shad in

southern Alabama, including within the Conecuh River (Barkuloo 1993, Adams

et al.

2000, Mettee and O'Neil 2003). Smith

et al.

(2011) reported that 11 Alabama shad were captured in the Conecuh River in 2000 and one in 2010 by the Alabama Department of Wildlife and Fisheries.

Choctawhatchee River

The Choctawhatchee River begins in Alabama. As it flows south, it is joined by one of its tributaries, the Pea River, then continues through the Florida panhandle and into the Gulf of Mexico. Some studies indicate there are small spawning populations of Alabama shad in southern Alabama, including in the Choctawhatchee and Pea Rivers (Barkuloo 1993, Adams

et al.

2000, Mettee and O'Neil 2003, Young 2010). Smith

et al.

(2011) reported the capture of 400 Alabama shad from the Choctawhatchee River system in 2000.

Ochlockonee River

Alabama shad were historically present in the Ochlockonee River, a fast running river that flows from Georgia into Florida. Smith

et al.

(2011) reported that the last specimens to be collected in the Ochlockonee River were captured in 1977 below Jackson Bluff Dam (Swift 1977). During the public comment period announced in the 90-day finding, FFWCC reported that 4 Alabama shad were collected near the Talquin (Jackson Bluff) Dam in 2011 (J. Wilcox, FFWCC, pers. comm. to K. Shotts, NMFS, November 12, 2013).

Econfina River

The Econfina River is a minor river draining part of the Big Bend region of Florida. It empties into Apalachee Bay. Historical data for Alabama shad are not available for this river, but, FFWCC reported during the public comment period that 1 Alabama shad was collected in the Econfina River in 2006 (J. Wilcox, FFWCC, pers. comm. to K. Shotts, NMFS, November 12, 2013).

Suwannee River

The Suwannee River originates from the Okefenokee Swamp in Georgia and runs south through Florida. Historically, the Suwannee River has been the easternmost boundary of the Alabama shad's range (Herald and Strickland 1946). There is still a spawning population of Alabama shad in the Suwannee River (Smith

et al.

2011). Sporadic sampling in the Suwannee River has included Alabama shad (Mettee and O'Neil 2003). Records from the Florida Museum of Natural History and the FFWCC show that 3-27 Alabama shad were collected annually between 1990-1995 (FishNet2 2016; search terms “

Alosa alabamae,

” “1990-2016,” and “Suwannee”). Mickle (2010) collected 6 fish. Smith

et al.

(2011) reported that FFWCC caught 15 Alabama shad on the Withlacoochee River, a tributary of the Suwannee River, in late November 2010 (Smith

et al.

2011). The Florida Museum of Natural History also shows that 2 Alabama shad were collected in 2015 (FishNet2 2016; Catalogue #238044 and #238066).

Extinction Risk Assessment

We estimated both the current extinction risk for Alabama shad and the anticipated risk in the foreseeable future. We defined the “foreseeable future” as the timeframe over which threats or the species' response to those threats can be reliably predicted to impact the biological status of the species. First, we evaluated demographic factors associated with population viability (abundance, productivity, spatial distribution, and diversity) and how they are contributing to the extinction risk of Alabama shad. We then performed a threats assessment using the factors listed in Section 4(a)(1) of the ESA by identifying the severity of threats that exist now and estimating their severity in the foreseeable future.

We used the methods developed by Wainwright and Kope (1999) to organize and summarize our findings on the contributions of the demographic factors and threats listed in ESA Section 4(a)(1) to the extinction risk of Alabama shad. This approach has been used in the review of many other species (Pacific salmonids, Pacific hake, walleye pollock, Pacific cod, Puget Sound rockfishes, Pacific herring, and black abalone, and foreign sawfishes) to summarize the status of the species according to demographic risk criteria. McElhany

et al.

(2000) examined short and long-term trends in abundance, productivity, spatial structure, and genetic variability as the primary indicators of risk. Populations that are more fragmented have less genetic exchange and therefore less connectivity, increasing the risk of extinction. Loss of fitness and loss of diversity can occur from random genetic effects and increase the risk of extinction for a species. We used the five-level qualitative scale from Wainwright and Kope (1999) to describe our assessment of the risk of extinction for Alabama shad for each demographic category, both currently and in the foreseeable future. We also used this scale to describe our assessment of each of the threats from ESA Section 4(a)(1). At the lowest level, a factor, either alone or in combination with other factors, is considered “unlikely” to significantly contribute to risk of extinction for a species. The next lowest level describes a factor that, on its own, is considered to be at “low” likelihood of contributing to the extinction risk, but could contribute in combination with other factors. The next level is considered a “moderate” risk of extinction for the species, but in combination with other factors contributes significantly to the risk of extinction. A ranking of “likely” means that factor by itself is likely to contribute significantly to the risk of extinction. Finally, the most threatening factors are considered “highly likely” to contribute significantly to the risk of extinction.

Both “low” and “moderate” rankings require that the demographic factor or threat be considered alone, as well as in combination with other factors. In this determination, we first consider each of the demographic factors and threats independently, then evaluate how they may interact in combination to contribute to the extinction risk of Alabama shad. Our rankings of demographic factors and threats do not translate directly to extinction risk conclusions. Ranking simply describes how we considered the information. For instance, one or more demographic factors could be ranked as “highly likely” to be contributing to the extinction risk of a species without concluding that the species is threatened or endangered. For example, low abundance may be considered to present a moderate threat to the extinction risk of Alabama shad, but is offset by the species' high productivity and wide spatial distribution.

In some cases, there was not enough information or too much uncertainty in pending outcomes to rank a threat's contribution to the risk of extinction for Alabama shad using the categories established by Wainwright and Kope (1999). In those cases, we classify the contribution of the threat to the extinction risk of Alabama shad as being “unknown.” Even for threats we ultimately classify as unknown, we provide and evaluate whatever information is available, in some cases providing information on how related surrogate species (

e.g.,

other

Alosas

) may be responding to the identified potential threat. NMFS recently issued updated ESA listing guidance (May 26, 2016) that states in order to list a species, the agency must affirmatively determine on the basis of a set of scientific facts that a species is at risk. The ESA does not allow for listings to be based on giving the species the benefit of the doubt. The guidance

clarifies that in the absence of any information about threats to a species, the null hypothesis is that the risk is low (generally low, not as defined by Wainwright and Kope (1999). Specific supporting information must be cited in order to elevate the potential threat to a moderate or high risk category (again generally, not as defined by Wainwright and Kope (1999). In cases where we classified a threat as having an “unknown” risk to the species, we considered whether the “unlikely” or “low” category established in Wainwright and Kope (1999) was most appropriate. Because the “low” category by definition states that a threat could contribute to the extinction risk of a species in combination with other factors, per the listing guidance, we ultimately evaluated “unknown” threats as being “unlikely” to significantly contribute to the risk of extinction for Alabama shad.

We determined the extinction risk for the species as a whole by integrating the demographic risks and the threats assessment, including considerations of any uncertainty in the risks and threats. We made a determination as to whether the species warrants listing as threatened or endangered, or whether we believe listing is not warranted. Finally, we determined whether there was a significant portion of the species' range that may warrant listing as threatened or endangered.

Foreseeable Future

Per NMFS' May 2016 revised listing guidance, the “foreseeable future” describes the extent to which the Secretary can, in making determinations about the future conservation status of the species, reasonably rely on predictions about the future (Department of the Interior Solicitor's Memorandum M-37021, “The Meaning of `Foreseeable Future' in Section 3(20) of the Endangered Species Act” (Jan. 16, 2009)). Those predictions can be in the form of extrapolation of population or threat trends, analysis of how threats will affect the status of the species, or assessment of future events that will have a significant new impact on the species. We believe that the appropriate period of time corresponding to the foreseeable future should account for the Alabama shad's life-history characteristics and the most significant threats facing the species.

The Alabama shad is an early-maturing species (Mickle

et al.

2010) with high productivity (Mettee and O'Neil 2003, Ingram 2007). Like other members of the

Alosa

family, Alabama shad populations may fluctuate significantly from year to year (Sammons and Young 2012). The time period associated with the foreseeable future for Alabama shad should be long enough to assess population response while taking into consideration the high variability inherent in the species. Below, we discuss generation time in relation to our ability to reliably predict the species' conservation status.

In defining the foreseeable future, we considered generation time, specifically defined here as the time it takes for a sexually mature Alabama shad to be replaced by offspring with the same spawning capacity. Age-2 to age-4 fish make up the majority of spawning Alabama shad; therefore, using our definition, the generation time for Alabama shad is 4-8 years. Generation time is inversely related to productivity and/or resilience. Highly productive species with short generation times are more resilient than less productive, long-lived species, as they are quickly able to take advantage of suitable conditions for reproduction (Mace

et al.

2002). Species with shorter generation times, such as Alabama shad (4-8 years), experience greater population variability than species with long generation times, because they maintain the capacity to replenish themselves more quickly following a period of low survival (Mace

et al.

2002). We believe that the impacts from the threats on the biological status of the species can be confidently predicted within the 12- to 24-year (three-generation) timeframe. Given their high population variability, projecting out further than three generations could lead to considerable uncertainty in estimating the population trajectory for Alabama shad. The timeframe of three generations is widely used to assess trends in populations and has been applied to decision-making models by many other conservation management organizations, including the American Fisheries Society (AFS), the Convention on the International Trade in Endangered Species of Wild Flora and Fauna (CITES), and the International Union for Conservation of Nature (IUCN).

The foreseeable future timeframe is also a function of the reliability of available data regarding the identified threats and extends only as far as the data allow for making reasonable predictions about the species' response to those threats. In our extinction risk assessment, we determined the abundance of Alabama shad and the presence of dams are the highest ranked threats, both contributing a moderate level of risk to Alabama shad. The remaining threats are ranked as either contributing a low or unknown level of risk to Alabama shad, or being unlikely to contribute to the species extinction risk.

Small populations may have less of a buffer against threats than large populations (McElhany

et al.

2000). We ranked low abundance as posing a moderate threat to Alabama shad's extinction risk. Our consideration of generation time above discusses how the abundance of Alabama shad is variable, and the species can fluctuate widely from year to year. We determined projecting out further than three generations could lead to considerable uncertainty in estimating the population trajectory for Alabama shad.

We also consider the timeframe over which the effect of dams on Alabama shad populations can be predicted. Dams are believed to be the main cause of the initial decline of Alabama shad. Existing dams continue to block habitat and cause downstream effects today, but few new dams have been built since the mid-1980s (Graf 1999). The threat of dams to Alabama shad has not increased for the past 30 years, and is not expected to increase in the future due to the advent of environmental laws and public awareness that occurred after the era of big dam building (Doyle

et al.

2003, Graf 1999). The threat of dams to Alabama shad is more likely to decrease in the future, as dams are either removed or additional fish passages are added. Environmental concerns are coinciding with a policy window in which many private dams are coming up for regulatory re-licensing with the Federal Energy and Regulatory Commission (FERC) and operational guidelines for publicly-operated dams are being reviewed (Doyle

et al.

2003). Upstream effects from dams may be reduced through fish passage technology, which is becoming increasingly efficient (Roscoe and Hinch 2010). Fish passage may be voluntarily implemented at dams, or even required by Federal regulations in some instances. Downstream effects from dams are also becoming better understood and dam operators are becoming more willing and able (and may be required in some instances) to alter operations to minimize the ecological effects downstream (Poff and Hart 2002). Further, an estimated 85 percent of the dams in the United States will be near the end of their operational lives by 2020 (Doyle

et al.

2003). Economic considerations and environmental concerns may result in dam removals, as maintenance, operation, repairs are often much costlier than dam removal (Doyle

et al.

2003, Stanley and Doyle 2003).

It is unknown to what extent the implementation of fish passage, modifications to dam operations, or dam removal will occur in rivers inhabited by Alabama shad. The lack of new dam building in the past 30 years coupled with increased environmental regulation and public awareness makes it unlikely that the threat of dams to Alabama shad will increase and more likely that there could be a decrease of this threat to the species. However, we cannot predict where dam modifications or removal may occur, and how Alabama shad may be affected. Our ability to predict the response of Alabama shad populations to the threat is limited by the life history characteristics of the species (

i.e.,

its variability in response to all of the factors affecting the population) rather than any variability in the threat of dams itself.

In defining foreseeable future, we further considered the interaction of demographic characteristics (parameters describing the viability of a population, such as abundance and productivity) and the species' response to various threats, primarily dams. Smith

et al.

(2011) conducted a population viability analysis (PVA) on Alabama shad in the ACF River system. Researchers selected 20 years as the timeframe over which the PVA could reliably model population responses of Alabama shad based on the species' demographic characteristics and various combinations of natural and anthropogenic threat scenarios affecting their survival and growth. The 20-year timeframe used in the PVA falls within the three-generation timeframe discussed above. This timeframe takes into account aspects of the species' life history and also allows the time necessary to provide for the recovery of populations. Thus, we determined for the purpose of the extinction risk assessment, a 20-year timeframe, corresponding approximately to the three-generation time period, to be appropriate for use as the foreseeable future for Alabama shad.

Demographic Risks

Threats to a species' long-term persistence are manifested demographically as risks to its abundance, population growth rate, spatial structure and connectivity, and genetic and ecological diversity. These demographic risks provide the most direct indices or proxies of extinction risk. A species at very low levels of abundance and with few populations will be less tolerant to environmental variation, catastrophic events, genetic processes, demographic stochasticity, ecological interactions, and other processes compared to large numbers in many populations (

e.g.,

Meffe and Carroll 1994, Caughley and Gunn 1996). A population growth rate that is unstable or declining over a long period of time has less resiliency to future environmental change (

e.g.,

Lande 1993, Middleton and Nisbet 1997, Foley 1997). A species that is not widely distributed across a variety of well-connected habitats is at increased risk of extinction due to environmental perturbations, including catastrophic events, compared to a species that is widely distributed (Schlosser and Angermeier 1995, Hanski and Gilpin 1997, Tilman and Lehman 1997, Cooper and Mangel 1999). A species that has lost locally adapted genetic and ecological diversity may lack the ability to exploit a wide array of environments and endure short- and long-term environmental changes (

e.g.,

Groot and Margolis 1991, Wood 1995). Assessing extinction risk of a species involves evaluating whether risks to its abundance, population growth rate, spatial structure, and/or diversity are such that it is at or near an extinction threshold, or likely to become so in the foreseeable future.

Abundance

A small population faces a host of risks intrinsic to its low abundance while large populations exhibit a greater degree of resilience (McElhany

et al.

2000). The only population estimates available for Alabama shad are from the ACF River system in Florida, Alabama, and Georgia. This system is believed to have the largest population of Alabama shad. Population estimates fluctuated widely from 2005 to 2015. For instance, 26,193 Alabama shad were estimated to be in the system in 2011. The following year, the estimate of Alabama shad peaked at 122,578. Sammons and Young (2012) noted that the population sizes of species in the

Alosa

genus commonly fluctuate widely. Researchers in the ACF River system believe that Alabama shad abundance may be a response to conservation efforts in the system (Schaffler

et al.

2015). They also note that variability in population number may be linked to environmental conditions. Specifically, Sammons and Young (2012) believe that heavy rainfall in 2009 may have led to strong year classes in 2010 and 2012.

No population estimates are available for other rivers, although several hundred Alabama shad have been captured in studies conducted in the past 15-20 years in the Pascagoula (Mississippi), Choctawhatchee (Florida/Alabama), and Ouachita (Arkansas/Louisiana) River systems. The annual Alabama shad population estimates in the ACF River system were developed through mark-recapture studies. The initial capture of less than a hundred to over 1,000 Alabama shad resulted in population estimates of thousands to over 100,000 Alabama shad. Mark-recapture can be used to produce abundance estimates without capturing every individual in the population because in addition to counting the number of individuals captured during the study, they estimate the detection probability of individuals (

i.e.,

the probability that an individual will be captured during the study; Yoccoz

et al.

2001). Detection probability can be influenced by population size, but can also be influenced by the sampling season and methodologies used, as well as a species' habitat affinities (Gu and Swihart 2004). Population estimates cannot be reliably developed from studies that collect a species, but do not consider its associated detection probability. Pellet and Schmidt (2005) note that it is often very difficult, if not impossible, to detect all individuals, populations, or species, and found during their surveys that the detection probability for a common species of tree frog was very high, while the detection probability of a common toad species was very low. Yoccoz

et al.

(2001) note that detection probability is generally less than 100 percent and usually variable. Although we cannot estimate the population abundance of Alabama shad in the Pascagoula, Choctawhatchee, and Ouachita Rivers, based on the likelihood that the species' detection probability is less than 100 percent, we can infer that the sizes of those Alabama shad populations are greater than the hundreds of fish collected in those systems. For instance, during the 2013 targeted study in the ACF, 251 Alabama shad were captured and 1 recaptured to yield the population estimate of 2,039 (S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, JWLD Fish Passage Year-End Summary Meeting, January 2014).

Generally, the number of Alabama shad in rivers other than the ACF, Pascagoula, Choctawhatchee, and Ouachita is likely to be small. A multi-state, multi-agency report from 1994 (Gutreuter

et al.

1997) indicates that Alabama shad were found in the Upper Mississippi River, but does not note the number or locations of fish caught. Smaller numbers (one to several dozens) of Alabama shad have been captured in the last 25 years in portions of the Lower Mississippi River, Mississippi River tributaries (Missouri, Marys, and

White Rivers), Mobile, Escambia, Conecuh, Ochlockonee, Econfina, and Suwannee Rivers.

Alabama shad was never an economically important species, and, therefore, information from fisheries statistics, such as landings data, is rare. Hildebrand (1963) noted that Alabama shad were considered unfit for human consumption, and the lack of demand produced no incentive to capture the species or record its presence and abundance. Most of the recent directed research studies on Alabama shad have occurred in the ACF and Pascagoula River systems. Capture data for other systems comes from general multi-species surveys, captures incidental to other research studies, and anecdotal information. Mettee and O'Neil (2003) note that low numbers of recorded Alabama shad individuals may be due, at least in part, to insufficient sampling effort during appropriate times (

i.e.,

spawning migrations) and with the appropriate gear to target the species. Hildebrand (1963) noted the importance of proper gear, citing greatly increased catches of Alabama shad that occurred in Kentucky when surface-fishing seines were substituted for bottom-fishing seines. The lack of data is echoed in the responses received from fish and wildlife agencies during the public comment period on our 90-day finding. The Arkansas Fish and Game Commission stated they could not assess the status of Alabama shad in their state because of the scarcity of information on the species, the lack of targeted surveys, and the unknown detectability of the species (M. Oliver, Chief of Fisheries, Arkansas Fish and Game Commission, pers. comm. to K. Shotts, NMFS, November 5, 2013). It is unknown whether the lack or low numbers of Alabama shad reported for many river systems accurately reflects the abundance in those systems or whether it is indicative of the lack of targeted studies, but ultimately, the population abundance in these areas is still unknown.

The threshold abundance below which Alabama shad populations cannot rebound (quasi-extinction) is unknown. In conducting the PVA on Alabama shad from the ACF River system, Smith

et al.

(2011) conservatively assumed 420 females as the threshold for quasi-extinction based on the lowest recorded population abundance for the ACF River system at the time (from Ely

et al.

2008). That assumption was not based on a minimum number of females needed to recover the population, but instead the lowest number of females observed in the viable population during previous studies. In fact, Smith

et al.

(2011) report that a viable spawning population persists in the Suwannee River at the eastern edge of the species' range, even though sporadic sampling since 2003 has only reported a total of 6-15 individual Alabama shad. We do not have historical abundances of Alabama shad, which can be indicative of abundance levels associated with low extinction risk. However, populations may also be at low risk of extinction at abundance levels below historical levels, and accurate estimates of historical abundance are not essential for evaluating extinction risk. Information from other species in the

Alosa

genus indicates that the species can rebound from extremely low abundance. The 12-month determination for 2 species of river herring (78 FR 48944; August 12, 2013), which determined that listing alewives (

A. pseudoharengus

) and blueback herring (

A. aestivalis

) under the ESA was not warranted, states that highly fecund, short generation time species like river herring may be able to withstand a 95 to 99 percent decline in biomass (Mace

et al.

2002). The 12-month determination (78 FR 48944; August 12, 2013) states that both alewives and blueback herring may have declined by more than 98 percent from their historical baseline (Limburg and Waldman 2009), but that the abundance of each species is stable or increasing, indicating the species are self-sustainable and are at a low to moderate-low risk of extinction.

Directed studies and current data on Alabama shad abundance are mostly lacking. The available population estimates for the ACF River system since 2005 are relatively large and highly variable. Ely

et al.

(2008) compared Alabama shad and American shad. They noted that, given the similarities in life history characteristics of Alabama shad and American shad and the similarities in discharge, drainage area, and latitude between the Apalachicola River and other southeastern rivers, the populations of adult Alabama shad and American shad might be expected to be similar. Ely

et al.

(2008) cited the number of American shad reaching the first barrier to migration in the Savannah River, estimated as nearly 190,000 (Bailey

et al.

2004), and the number in the Altamaha River system estimated as 133,000 (Georgia DNR 2005), and concluded that the population size of the Alabama shad in the Apalachicola River from 2005-2007 (approximately 2,700-26,000 shad) was relatively small. Subsequent to the Ely

et al.

(2008) study, the numbers of Alabama shad in the Apalachicola River generally increased, ranging from 2,000-122,500 from 2008-2012. It is not known what the historical abundance of Alabama shad was in the ACF River system, but the Alabama Shad Restoration Plan for the ACF River System (NMFS

et al.

2012) projected that the carrying capacity (the maximum population of a species that can survive indefinitely in a given environment) for Alabama shad in the ACF is approximately 1.3 million adults. Capture data from other systems are limited or lacking but suggest low to moderate sized populations in some rivers and absence in others.

The only current population estimates available for Alabama shad are in the ACF River system. Because Alabama shad were never commercially or recreationally important, few historical records exist. There are no recorded historical population sizes in any river systems for comparison, although anecdotal information on observations and small, short-lived fisheries provide some historical context (

e.g.,

Coker 1929, 1930). However, many researchers recognize that Alabama shad populations have experienced decline from historical population sizes (

e.g.,

Gunning and Suttkus 1990, Buchanan

et al.

1999, Mettee and O'Neil 2003, Mickle

et al.

2010).

Declines have been estimated in other

Alosa

species with longer historical records. Hall

et al.

(2012) attempted to estimate historical alewife populations in Maine for the years 1600-1900 using analyses of nineteenth and twentieth century harvest records and waterway obstruction records dating to the 1600s and estimated that obstructed spawning access reduced the annual alewife productivity per watershed to 0-16 percent of pre-dam estimates. The 12-month listing determination for river herring (78 FR 48944; August 12, 2013) reported that of the riverine stocks of alewife and blueback herring for which data were available and were considered in a stock assessment, 22 were depleted, 1 was increasing, and the status of 28 stocks could not be determined because the time-series of available data was too short. In most recent years, 2 riverine stocks were increasing, 4 were decreasing, and 9 were stable, with 38 rivers not having enough data to assess recent trends. Both alewives and blueback herring may already be at or less than 2 percent of the historical baseline. Because historical landings data are available for alewife and blueback herring, population modeling was feasible and used to determine the stability of the stocks in light of the declines. The conclusion of the 12-

month determination (78 FR 48944; August 12, 2013) was that listing alewife and blueback herring under the ESA was not warranted because the abundance of each species is stable or increasing, indicating the species are self-sustainable and are at a low to moderate-low risk of extinction.

Population sizes of Alabama shad and other

Alosa

species are known to be variable and the species can quickly rebound from low population numbers. Alabama shad are spawning and persisting in river systems along the Gulf Coast and in tributaries of the Mississippi River. Even smaller populations are considered to be self-sustaining (

e.g.,

eastern Alabama rivers, Mettee and O'Neil 2003, Suwannee River, Smith

et al.,

2011). The range of Alabama shad appears to be stable (Smith

et al.

2011). However, low abundance in combination with other factors could contribute significantly to the risk of extinction since smaller populations have less of a buffer against threats than larger populations. This aligns with the definition of a “moderate risk” under the risk classification system by Wainwright and Kope (1999).

For comparison, the next highest ranking under Wainwright and Kope's (1999) classification system is for a threat that is presently low or moderate, but is likely to increase to high risk in the foreseeable future if present conditions continue. Although based largely on anecdotal information rather than population estimates and trends, we believe there is sufficient evidence to indicate that there have been declines in the abundance of Alabama shad and their low abundance could contribute significantly to their long-term risk of extinction. However, we do not have information suggesting that threats to Alabama shad populations are likely to lead to further decline to the point that their abundance would present a high risk to the species. The primary threat that led to the initial decline of the species was the installation of dams that block access to upriver spawning habitat (evaluated under Factor A of this listing determination). Although most dams are still in place and represent an obstacle to spawning Alabama shad, very few dams have been built in the last 30 years (Graf 1999). Few environmental laws were in existence when the dams were originally built, but the development and implementation of conservation measures in the last 20 years (Doyle

et al.

2003) are likely to lessen the effect of dams on Alabama shad rather than to pose an increasing threat to the species. Other threats evaluated in this listing determination are ranked as either contributing a low or unknown level of risk to Alabama shad, or being unlikely to contribute to the species extinction risk. As discussed in each of these sections evaluating these threats, we do not have information that they will increase in the foreseeable future. Therefore, we ranked abundance throughout its range as contributing a moderate level of risk to the overall current and foreseeable extinction risk of Alabama shad.

Productivity

Population growth rate (productivity) and factors that affect productivity provide information on how well a population is responding in the habitats and environmental conditions it is exposed to during its life cycle (McElhany

et al.

2000). Whether a species' productivity has declined, or is declining, toward the point where populations may not be sustainable and whether habitat quality restricts productivity to non-sustainable levels are key pieces of information in assessing a species' extinction risk (Wainwright and Kope 1999). In assessing the productivity of Alabama shad, we considered life history traits, the number of spawning populations, and trends in abundance over time.

Several life history traits make Alabama shad a relatively productive species (Smith

et al.

2011). They reach sexual maturity quickly. Males start spawning as early as 1 year old, and females start spawning at 2 years old (Mickle

et al.

2010). Female Alabama shad are known to release large numbers of eggs. Individual females in the Apalachicola River produce from 26,000-250,000 eggs and from 36,000-357,000 in the Choctawhatchee River (Mettee and O'Neil 2003, Ingram 2007). Females may have multiple spawning periods within the same spawning season (Mettee and O'Neil 2003). Because of the age range among spawning Alabama shad (1-5 years for males, 2-6 years for females), individuals may spawn multiple times in a lifetime (Laurence and Yerger 1967, Mettee and O'Neil 2003, Ingram 2007, Mickle

et al.

2010). Recent information from the ACF River system suggests that female Alabama shad may spawn only once during their lifetime, but may release several batches of eggs during the weeks that they are spawning (S. Herrington, The Nature Conservancy, pers. comm. to K. Shotts, NMFS, November 2015).

We also considered the number of Alabama shad spawning populations to assess the productivity of Alabama shad. The largest spawning population of Alabama shad is in the ACF River system, with smaller spawning populations believed to exist in the Missouri/Gasconade/Osage, Meramec, White, Ouachita/Little Missouri, Pascagoula/Leaf/Chickasawhay, Escambia/Conecuh, Choctawhatchee/Pea, and the Suwanee River systems. The life history traits of Alabama shad combined with the presence of multiple spawning populations contributes to the productivity potential of Alabama shad. Highly productive species with short generation times, like Alabama shad, are more resilient than less productive, long lived species, as they are quickly able to take advantage of suitable conditions for reproduction (Hutchings and Reynolds 2004, Mace

et al.

2002, Musick 1999). Species with shorter generation times, such as Alabama shad (4 to 8 years), experience greater population variability than species with long generation times, because they maintain the capacity to replenish themselves more quickly following a period of lower survival (Mace

et al.

2002). This resilience was observed in the ACF River system when Alabama shad populations quickly increased when access to upstream spawning habitat was re-established by conservation locking through an existing dam.

Alabama shad populations are generally believed to have declined in many areas where they were historically found. However, it is difficult to quantify any declines because of a lack of historical abundance data for most river systems and the lack of current population estimates for populations other than the ACF River system. Records of Alabama shad in the Pearl River are fairly complete and show a steady decline of the species. This decline was based on the total number of fish captured over time; it did not include estimating population numbers through the use of mark-recapture methods, like those used in the Apalachicola River. In the Pearl River, consistent sampling occurred in several sections of the river over 16-25 years: 384 fish captured 1963-1965; 33 captured 1965-1979; and 1 individual captured 1979-1988 (Gunning and Suttkus 1990). Since then no records of shad have been reported during annual fish surveys conducted by several of the state's universities in the Pearl River (Smith

et al.

2011). Surveys conducted by USACE on the Lower Mississippi River (north of Baton Rouge, Louisiana) in the early 1980s also recorded the number of individuals encountered and showed a slow decline in the number of both adult and juvenile Alabama shad (Pennington 1980, Conner 1983, Smith

et al.

2011). We can use the low

numbers or lack of Alabama shad captures/observations throughout the rest of their range to indicate declines from historical abundances. But it is hard to relate those numbers with the estimates for the Apalachicola that were calculated using mark-recapture techniques. However, it is clear that while once abundant enough to support small commercial fisheries in Alabama, Arkansas, Kentucky, Indiana, Ohio, and Iowa, Alabama shad are rarely collected throughout much of their former range (Adams

et al.

2000, Daniels 1860). Alabama shad are believed to possibly be extirpated from the Ohio River since 1989 (Pearson and Pearson 1989). Alabama shad are considered rare in the state of Illinois and appear to have been extirpated from many rivers in the state (Smith

et al.

2011).

Declines have been estimated in other

Alosa

species with longer historical records. Hall

et al.

(2012) attempted to estimate historical alewife populations in Maine for the years 1600-1900 using analyses of nineteenth and twentieth century harvest records and waterway obstruction records dating to the 1600s. They estimated that obstructed spawning access in 9 watersheds reduced the annual alewife productivity per watershed to 0-16 percent of pre-dam estimates, equaling a cumulative lost fisheries production of 11 billion fish from 1750 to 1900 (Hall

et al.

2012).

Attempts have been made to estimate past abundances of Alabama shad and habitat carrying capacity for conservation planning by using examples from other

Alosa

species. Comparisons have been made between Alabama shad and American shad. Ely

et al.

(2008) noted that, given the similarities in life history characteristics of Alabama shad and American shad and the similarities in discharge, drainage area, and latitude between the Apalachicola River and other southeastern rivers, the populations of adult Alabama shad and American shad might be expected to be similar. Ely

et al.

(2008) cited the number of American shad reaching the first barrier to migration in the Savannah River, estimated as nearly 190,000 (Bailey

et al.

2004), and the number in the Altamaha River system estimated as 133,000 (Georgia DNR 2005), and concluded that the population size of the Alabama shad in the Apalachicola River from 2005-2007 (approximately 2,700-26,000 shad) was relatively small. Subsequent to the Ely

et al.

(2008) study, the numbers of Alabama shad in the Apalachicola River generally increased, ranging from 2,000-122,500 from 2008-2012 (as noted earlier, the 2013-2015 data was considered to be skewed by sampling difficulties). Additionally, Ely

et al.

(2008) noted that fluctuations in abundance of American shad are well documented (citing Hattala

et al.

1996, Atlantic States Marine Fisheries Commission 1998, Moring 2005) and variations in year-class strength typically observed in this genus suggest that populations of Alabama shad are capable of recovering quickly to historical levels under favorable conditions. A multi-agency Alabama Shad Restoration Plan for the Apalachicola-Chattahoochee-Flint River System (NMFS

et al.

2012) calculated that the carrying capacity for the system is 1.3 million adult Alabama shad (700,000 in the Chattachoochee and 600,000 in the Flint), derived from the amount of free-flowing habitat in the mainstem and major tributaries of the Flint and Chattahoochee Rivers and using American shad population indices as a surrogate.

In summary, we find the productivity potential for Alabama shad is relatively high, given its life history characteristics and the presence of multiple spawning populations within the species' range. This relatively high productivity potential of Alabama shad was confirmed in the ACF River system when population numbers greatly increased when access to historical spawning habitat was provided. Available data suggest a decline in abundance in many systems. Other

Alosa

species with longer and more complete historical records, such as alewife, have also shown declines in abundance. A comparison with American shad populations at similar latitudes and a habitat study indicate that the Alabama shad population in the ACF River system may be smaller than expected and below carrying capacity in the system. Managers and researchers note that low numbers of recorded Alabama shad individuals may be due, at least in part, to insufficient sampling effort during appropriate times (

i.e.,

spawning migrations) and with the appropriate gear to target the species. We ranked productivity, on its own, to be at low risk of contributing significantly to the current and foreseeable risk of extinction for Alabama shad.

Spatial Distribution

McElhany

et al.

(2000) stated that spatial structure is an important consideration in evaluating population viability because it affects evolutionary processes and can affect a population's ability to respond to environmental change. Wainwright and Kope (1999) stated that it is important to determine whether existing populations adequately represent historical patterns of geographic distribution and biodiversity and whether population fragmentation poses a risk. The historical distribution of Alabama shad spanned the Gulf Coast from the Suwannee River, Florida, to the Mississippi River, Louisiana. Within the Mississippi River and its tributaries, the species spanned north to Illinois and Iowa, westward to Oklahoma, and eastward to Kentucky and Ohio. The species is believed to be extirpated in some of the farthest reaches of its historical range, such as the Upper Mississippi River and Mississippi River tributaries in Oklahoma, Illinois, and Kentucky/Ohio. However, Alabama shad can still be found in river systems in Arkansas, Missouri, and along the Gulf Coast. The current range of Alabama shad encompasses a diverse array of habitats, which potentially contributes to population stability. Smith

et al.

(2011) state that the current range of Alabama shad is believed to be stable.

Maps displaying the best available information on the historical and current range (presence) of Alabama shad by river, including where the species continues to spawn, can be found at:

http://sero.nmfs.noaa.gov/protected_resources/listing_petitions/species_esa_consideration/index.html

(see Figures 1 and 2 for the eastern and western portions of the range, respectively). Historical and current range, as well as spawning rivers, are based on reports of the species presence from the literature (see the “Distribution and Abundance” section), but the maps do not represent the number of fish reported from a river system. In most cases, we do not have information on the exact portion(s) of river systems historically or currently inhabited by Alabama shad, or where spawning habitat is located. In the ACF River system (where the majority of recent directed research on Alabama shad is occurring), the map shows that Alabama shad likely do not pass above dams at Albany and George Andrews Lake. In other systems, it is unknown to what degree locks and dams and/or low head dams block upstream passage or allow some shad to move upstream and downstream. This is discussed in greater detail in the “Dams” section under “A. The Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range.” In cases where no information is available on the specific extent of Alabama shad or its spawning habitat within a river system, we included the entire river

system as part of the range of Alabama shad.

In developing the maps reflecting the historical and current range of Alabama shad, we determined we would include positive reports of Alabama shad over the last 24 years. The 24-year time frame was selected because dams within the geographic range of Alabama shad were completed 30 or more years ago (mid-1980s; Graf 1999). Since dams have the ability to alter the range of shad within rivers, older/pre-dam studies reporting shad would not reflect any alterations of the species' distribution due to the dam. Further, any alterations in the distribution of Alabama shad may not happen immediately after construction of a dam. Therefore we considered the maximum age observed in Alabama shad (6 years; Mettee and O'Neil 2003). We only included reports of Alabama shad that occurred at least 6 years after the era of dam-building ended (

i.e.,

24 years ago or less). Positive reports of Alabama shad in a river system in the last 24 years would indicate that new generations of shad persisted in the river system after the end of the dam-building era, even if a dam was constructed in the system. Therefore, positive reports collected during the 24-year time frame accounted for the presence of dams with the range of Alabama shad. We also used information from the literature on where the species is potentially extirpated to indicate the historical versus current range. In many instances, the information demonstrating persistence during the last 24 years is limited to just one or several verified identifications of Alabama shad. However, in view of the high productivity of shad, the challenges associated with detecting the species in non-targeted studies, and the episodic, anecdotal nature of available information, we believe it is reasonable to extrapolate from information confirming presence during the last 24 years that Alabama shad continue to occur in these systems.

In some cases, such as the Mississippi River, Alabama shad are shown to inhabit a tributary but not the river mainstem. Although the mainstem is not included as part of the historical range, this does not necessarily indicate Alabama shad are not present in the mainstem, only that we did not find a positive report of their presence in the last 25 years. In the example of the Mississippi River, the river mainstems are often not the subject of research surveys as high river flows and high vessel traffic raise concerns for human safety. Also, as noted earlier in this determination, Alabama shad can be difficult to detect, in both non-targeted or targeted surveys. Positive reports in the tributaries without reports from the mainstem could indicate the presence of landlocked populations or it could simply indicate that shad were present in the mainstem, but not surveyed or detected. Given the pelagic nature of Alabama shad, and their migratory life style, we believe that Alabama shad likely inhabit the mainstem of the rivers adjacent to the tributaries where they were reported.

Spatial structure contributes to the resiliency of populations to various disturbances, which can occur across a range of spatial scales, from localized disturbances affecting a few miles of stream and therefore only a portion of a population, to regional impacts from events such as droughts that affect multiple populations (Williams

et al.

2008). Hilborn

et al.

(2003) state there is growing recognition that many fish stocks consist of multiple combined geographic components. Spatial diversity in populations can lead to greater stability in fish species (Jorgensen

et al.

2016). Schindler

et al.

(2010) referred to this as a “portfolio effect” that is analogous to the effects of asset diversity on the stability of financial portfolios. Hilborn

et al.

(2003) reported a “portfolio effect” in the resilience of sockeye salmon in Bristol Bay, Alaska, which the researchers attributed to the maintenance of diverse geographic locations and life history strategies that comprise the sockeye salmon stock. At different times during the 1900s, different geographic regions and different life history strategies contributed to the productivity of the stock, and Hilborn

et al.

(2003) concluded this likely buffered the stock against large-scale environmental conditions, providing long-term stability. Jorgensen

et al.

(2016) studied Chinook salmon populations from the Columbia River and also observed differential contributions of populations to species productivity, noting differences in migratory corridors, climate, and geology as potential factors.

The current range of Alabama shad (the species' portfolio) encompasses a diverse array of habitats, which potentially contributes to population stability. Many Federal agencies and non-governmental organizations classify terrestrial and aquatic systems based on ecoregions, large areas of similar climate where ecosystems recur in predictable patterns (USFS 2016). Ecoregions are a widely recognized and applied geospatial unit for conservation planning, developed to represent the patterns of environmental and ecological variables known to influence the distribution of biodiversity features at broad scales (Abell

et al.

2008). The boundaries of an ecoregion encompass an area within which important ecological and evolutionary processes most strongly interact (Abell

et al.

2008). Conservation of blocks of natural habitat large enough to be resilient to large-scale disturbances and long-term changes are essential for large river systems in particular (Abell

et al.

2008).

Under several widely used ecoregion classification systems, Alabama shad populations inhabit heterogeneous habitats across multiple diverse ecoregions. Alabama shad occupy six ecoregion “divisions” that the U.S. Forest Service classifies based on precipitation, temperature, and vegetation or other natural land cover. The Environmental Protection Agency (EPA) identified four levels of ecoregions by analyzing patterns of biotic and abiotic phenomena, both terrestrial and aquatic. These phenomena include geology, landforms, soils, vegetation, climate, land use, wildlife, and hydrology (EPA 2016). Even at the coarsest level, the EPA's Level I ecoregion, which highlights major ecological areas, Alabama shad populations occupy 2 of the 12 ecoregions in the continental United States: The Eastern Temperate Forests and the Great Plains. The species occupies 4 of the 25 Level II ecoregions, and 14 of the 105 Level III ecoregions. The Nature Conservancy (TNC) uses a terrestrial ecoregion classification system similar to the EPA Level III ecoregions. Alabama shad populations occupy nine TNC terrestrial ecoregions.

TNC also uses freshwater ecoregions with boundaries describing broad patterns of species composition and associated ecological and evolutionary processes (Abell

et al.

2008). Along the Gulf Coast, Alabama shad occupy four freshwater ecoregions: The Apalachicola (containing the ACF River system and the Econfina River), the West Florida Gulf (includes the Escambia and Choctawhatchee River systems), Mobile Bay (containing the Mobile River system), and the Lower Mississippi (includes portions of the White River). In the northern part of their range, Alabama shad occupy three freshwater ecoregions: The Central Prairie (containing the Missouri River and its tributary, the Osage River), the Ozark Highlands (including a portion of the White River), and the Ouachita Highlands (including the Ouachita River and its Little Missouri River tributary). The ecoregions along the Gulf Coast are similarly defined by humid subtropical climates, but diverge in other characteristics. The Apalachicola ecoregion lies entirely within the coastal

plain, but the variety of habitats found in its rivers provide the foundation for a diverse freshwater fauna. Rivers in the Apalachicola ecoregion flow through shaded ravines with cool spring inputs, resembling habitats of more northerly regions. This ecoregion supports more species than adjacent lowland ecoregions. The West Florida Gulf ecoregion is defined by the lowland drainages that flow through extensive floodplain oak-hickory-pine forests. This ecoregion does not boast the same fish richness as the neighboring Mobile Bay. The Mobile Bay ecoregion has the highest level of aquatic diversity in the eastern Gulf. This is largely due to the variety of physiographic provinces occurring in this ecoregion, its size, and its escape from Pleistocene glaciation. This ecoregion is centered in central Alabama and includes eastern Mississippi, western Georgia, and a small area in southern Tennessee. The northern part of the ecoregion is characterized by Appalachian Blue Ridge and Appalachian mixed mesophytic forests, considered some of the most biologically diverse temperate forests in the world. These grade into Southeastern mixed forests, which are demarcated from conifer forests in the south by the fall line of the Atlantic Piedmont. Historically, rivers and streams in this ecoregion stretched over 1000 mi. Today, flow in the Mobile River is regulated by a series of upstream reservoirs on the Etowah, Coosa, and Tallapoosa rivers, and to a lesser extent by the locks and dams of the Tombigbee River. The Lower Mississippi ecoregion is also distinguished by its species richness, particularly in fish. The entire Mississippi basin has served as a center for fish distribution as well as a glacial refugium, and as such it is home to many of the species found in surrounding drainages. As a result, it is the second richest ecoregion in North America.

Compared to other ecoregions, Alabama shad experience different climatic conditions in the Central Prairie, which has hot continental summers and cold winters, with periodic arctic blasts. Most of the streams and rivers in the ecoregion are meandering with low to moderate flow. The diversity of species in this ecoregion is high relative to adjacent ecoregions due to the presence of diverse habitats that were not interrupted during glacial periods. The Ozark Highlands ecoregion is part of the western Mississippi River drainage but is distinctive because of its relative biogeographical isolation. It is a region of high gradient headwater streams surrounded by coastal plains and prairie. The Ozark Highlands contain a diversity of freshwater habitats, including fens, sinkholes and springs, which feed the clear headwaters of larger, free-flowing streams. Many of these habitats served as refugia during periods of glacial maximas. The Ozarks are home to a unique assemblage of species. Like the Ozark Highlands, the Ouachita Highlands ecoregion is distinguished by its relative biogeographic isolation. The ecoregion is a source area for several larger streams and is an area of high-gradient and spring-fed springs, and can almost be considered an island surrounded by the Great Plains, coastal plains, and prairie. The ecoregion is characterized by oak-hickory-pine forests, which are some of the best developed in the United States.

Habitat heterogeneity is considered to be important for the stability of populations, and Oliver

et al.

(2010) found that heterogeneous landscapes containing a variety of suitable habitat types were associated with more stable population dynamics in a butterfly species. Oliver

et al.

(2010) noted that many studies have suggested that the beneficial effects of heterogeneity may buffer a broad range of taxa against environmental change. Based on common ecoregion classifications, the watersheds inhabited by Alabama shad populations contain a diverse array of landscapes, vegetation, geology, hydrology, and climate.

We also considered the spatial structure of the spawning populations of Alabama shad. In assessing the viability of salmonid populations, which are anadromous and exhibit homing tendencies like Alabama shad, McElhany

et al.

(2000) stated that it is practical to focus on spawning group distribution and connectivity because many of the processes that affect small population extinction risk depend on the breeding structure. The spatial arrangement of suitable spawning and rearing habitat within a watershed can be dynamic through time as a result of periodic disturbances that create a mosaic of varying habitat conditions (Reeves

et al.

1995). Efforts to understand population diversity have focused on population connectedness, through the analysis of DNA collected from individuals across the landscape or tagging data to quantify dispersal between populations (Jorgensen

et al.

2016). Alabama shad continue to spawn in river systems in Florida, Alabama, Georgia, Mississippi, Louisiana, Arkansas, and Missouri. While most Alabama shad spawn in their natal rivers, Waters

et al.

(2000) proposed that shad species may stray more than other anadromous fishes and estimated that American shad are expected to have over 10 effective migrants per generation. In fact, Mickle

et al.

(2006) and Kreiser and Schaefer (2009) found slight genetic distinctions between populations from the Mississippi River basin and coastal Gulf of Mexico drainages. Kreiser and Schaefer (2009) attributed this to Alabama shad straying from their natal rivers at a rate of about 10 migrants per generation, consistent with the estimate by Waters

et al.

(2000) for American shad. This indicates the possibility that Alabama shad could enhance and repopulate nearby river systems within their range. This was also observed in anadromous Pacific salmon. Similar to Alabama shad, these species exhibit high spawning site fidelity, but are well-adapted to dynamic environments through straying by adults (to connect populations) and high fecundity (also similar to Alabama shad; Reeves

et al.

1995, Jorgensen

et al.

2016).

The historical range of Alabama shad has contracted and this species is believed to be extirpated from some river systems. Few targeted research studies were conducted since the time a majority of dams may have altered Alabama shad's distribution, therefore we can rely only on anecdotal reports from monitoring activities and multispecies surveys from the last 24 years to determine their current range. However, the remaining spawning populations of the species appear to be geographically widespread. Their range appears to have become stable once dam building ended, and lost access to spawning habitat is likely to be restored through dam removal and fish passage, and protections under environmental laws have increased. Although spawning populations in some places are small, the species exists in multiple ecoregions, representing a diverse array of ecosystems that has the potential to buffer the species against environmental changes and promote population stability. Genetic studies (Kreiser and Schaefer 2009, Waters

et al.

2000) show that exchange between river populations is occurring at higher rates than is expected for other anadromous species. Therefore, we ranked spatial distribution throughout its range, on its own, to be at low risk of contributing significantly to the current and foreseeable risk of extinction for Alabama shad.

Diversity

In a spatially and temporally varying environment, genetic diversity is

important for species and population viability because it (1) allows a species to use a wider array of environments than they could without it, (2) protects a species against short-term spatial and temporal changes in the environment, and (3) provides the raw material for surviving long-term environmental changes (McElhany

et al.

2000). Small populations may be at risk from random genetic effects, Allee effects, and directional effects (Wainwright and Kope 1999).

Alabama shad are believed to be philopatric and generally return to the same rivers to spawn, which has resulted in slight genetic differences among river drainages (Meadows

et al.

2008, Mickle 2010). These genetic differences could result in characteristics (

e.g.,

faster growth rates, higher temperature tolerance, etc.) that lead to variable spawning strategies among river drainages. Kreiser and Schaefer (2009) also noted slight genetic differences between Alabama shad from the Mississippi River basin and coastal Gulf of Mexico drainages; however, they determined there has been no significant genetic differentiation among different river populations of Alabama shad.

Moyer (2012) evaluated the genome of Alabama shad collected from the ACF River system to assess the influence of genetic factors on their extinction risk, including whether the construction of JWLD blocking access to upstream spawning habitat affected their genetic diversity. Genetic diversity of Apalachicola River shad was calculated based on the average number of alleles (the possible forms in which a gene for a specific trait can occur), observed heterozygosity (having different alleles in regard to a specific trait), and expected heterozygosity. Moyer (2012) found no evidence of fine-scale population structure in the ACF River system. The observed genetic variation found in Alabama shad was lower than expected based on other shad studies. These findings suggest that the genetic variation of Alabama shad in the ACF River system has been severely reduced by a bottleneck event. Moyer (2012) concluded that the bottleneck likely did not result from the construction of JWLD or from any other anthropogenic activity. Moyer (2012) stated the reduced genetic diversity appears to be the result of past events that occurred during the Pleistocene. Bowen

et al.

(2008) made a similar determination for Alabama shad while studying the phylogenetic relationships across North American

Alosa

species. Their study also indicated that the genetic bottleneck occurred when the originating ancestor(s) of Alabama shad traveled around the Florida peninsula into the Gulf of Mexico during or after the Pleistocene and became geographically separated from Atlantic populations.

Loss of genetic diversity can reduce an organism's adaptive capacity to respond to differing environmental conditions and increase a species' extinction risk. However, population bottlenecks can also have positive outcomes on a species' genetic diversity, fitness, and extinction risk (Bouzat 2010). Moyer (2012) noted that populations or species that have undergone population bottlenecks throughout their evolutionary history may have reduced genetic load. Genetic load is the combination of harmful genes that are hidden in the genetic make-up of a population and may be transmitted to descendants. The genetic load of a population reduces the fitness of that population relative to a population composed entirely of individuals having optimal genotypes. Hedrick (2001) stated that a population with reduced genetic load resulting from a bottleneck may have increased viability and be more likely to recover from near-extinction than a population that has not experienced such an evolutionary bottleneck.

Modeling conducted by Moyer (2012) indicated that the Pleistocene bottleneck for Alabama shad was intense. The maintenance of genetic variability in a finite population can be understood through the concept of effective population size, which is not an actual abundance estimate but an estimate of the number of individuals in an ideal population that would give the same rate of random genetic drift (change in the frequency of a gene variant) as in the actual population (Lande 1988). The effective population size for Alabama shad

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