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Background

It is our intent to discuss below only those topics directly relevant to the taxonomic split of the flatwoods salamander into two species (the frosted flatwoods salamander and the reticulated flatwoods salamander) and the listing of the reticulated flatwoods salamander as endangered in this section of the proposed rule. For more information on the flatwoods salamander, refer to the final listing rule published in the Federal Register on April 1, 1999 (64 FR 15691). The overall range covered by the reticulated and the frosted flatwoods salamanders is the same as is currently designated for the flatwoods salamander. However, the reticulated flatwoods salamander inhabits the western part of the range and the frosted flatwoods salamander inhabits the eastern part.

In light of the taxonomic split, we also reevaluated the status of the frosted flatwoods salamander. We determined that threatened status is appropriate for this species because 124 breeding ponds supporting 22 of the 26 (85 percent) total populations for the species are located on public lands, most of these populations are relatively stable, and, based on the best scientific information available, we have concluded there are a sufficient number of populations that the species is not in immediate danger of extinction. The scientific information supporting the presence of populations comes from a variety of sources, including those data compiled in the Florida, Georgia, and South Carolina Natural Heritage databases and individual state databases, and data supplied by Fort Stewart Military Installation, Townsend Bombing Range, Apalachicola National Forest, Francis Marion National Forest, and St. Marks National Wildlife Refuge.

In general, most threats for this species (for example, habitat loss, habitat degradation, inadequacy of existing regulatory mechanisms) are of a historical nature in the majority of the range because breeding ponds supporting 85 percent of frosted flatwoods salamander populations occur on public lands where the habitat is relatively protected. Appropriate habitat management has been more actively pursued and multiple ponds support existing populations in many cases. On the 15 percent of ponds on private lands, there are a number of potential future threats including habitat loss and degradation, disease, predation, and fire suppression. The threat from invasive plant species is considered imminent, even on public lands, because of the current difficulties in managing for the prevention of spread of invasive species into natural habitats. The threat from drought is considered imminent for all populations because it is a current problem for the species at all sites. We will publish a separate notice providing the updated fivefactor analysis for the frosted flatwoods salamander for public review and comment in the near future.

Taxonomic Classification

The original listing rule (64 FR 15691; April 1, 1999) described the geographic range of the flatwoods salamander as it was known at that time. Habitat for the species included occurrences across the lower southeastern Coastal Plain in Florida, Georgia, and South Carolina. Taxonomic revision resulted from research done by Pauly et al. (2007, pp. 415429) which split the flatwoods salamander into two species, the frosted flatwoods salamander and the reticulated flatwoods salamander. The Apalachicola River drainage forms a geographic barrier between the two species. This drainage is a common site for eastwest phylogeographic breaks in many other taxa as well. For this reason, the split of the flatwoods salamander into two species is currently accepted by the scientific community. We propose to amend the List of Endangered and Threatened Wildlife at 50 CFR 17.11(h) to reflect this revision to taxonomy.

Goin (1950, p. 299) recognized two distinct subspecies of flatwoods salamander based on morphological and color pattern variation. This split between the eastern and western portions of the salamander's range was later discounted in an analysis by Martof and Gerhardt (1965, pp. 342346) and for the past 40 years the concept of a single undifferentiated species persisted. Pauly et al. (2007, pp. 415429) conducted molecular and morphological analyses to test whether the flatwoods salamander, as originally described, followed a pattern of eastwest disjunction at the Apalachicola River as has been described in many other species. They were able to demonstrate this predicted phylogeographic break. Based on mitochondrial DNA (mtDNA), morphology, and allozymes, they recognize two species of flatwoods salamanders, frosted flatwoods salamander to the east of the Apalachicola drainage and reticulated flatwoods salamander to the west. The Apalachicola River is probably the cause of major disjunctions in species distributions due to the repeated marine embayments during the Pliocene and Pleistocene interglacials that likely caused a barrier to gene flow.

In the Pauly et al. (2007, pp. 415429) analyses, the use of mtDNA splits flatwoods salamander populations into two major clades east and west of the ApalachicolaFlint rivers. Samples from Jackson and Liberty Counties, Florida are informative because, geographically, they are located on opposite sides of the river but are phylogenetically distant with respect to mtDNA sequence divergence. In contrast, geographically distant populations on the same side of the Apalachicola River are very closely related. Their morphological analyses also support a taxonomic boundary at the ApalachicolaFlint rivers. Salamanders on opposite sides of this boundary significantly differed in both body shape and size based on multivariate analyses. The number of costal grooves (grooves along the side body of salamanders used in species identification), snoutvent length, six additional morphometric traits, and sexual dimorphisms in tail length, height, and width are all significantly different between the two taxa. Due to
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the importance of the tail in ambystomatid courtship and fertilization, tail differences may be particularly important.

Allozyme data presented in Shaffer et al. (1991, pp. 290291, 302) also indicated differences between salamanders on either side of the Apalachicola River. Their results demonstrated these populations have fixedallele differences, consistent with the mtDNA and morphological results.

The frosted and reticulated flatwoods salamanders can be differentiated from each other by the use of several morphological characters (Pauly et al. 2007, pp. 424425). The frosted flatwoods salamander generally has more costal grooves and tends to be larger than the reticulated flatwoods salamander. For individuals of the same size, the frosted flatwoods salamander has longer fore and hind limbs and alonger,wider, and deeper head. Male frosted flatwoods salamanders have longer tails than those of the reticulated flatwoods salamander. The belly pattern of the frosted flatwoods salamander consists of discrete white spots on a dark background while the spots are less distinct in the reticulated flatwoods salamander giving a ``salt and pepper'' appearance (Goin 1950, pp. 300314). The back pattern of the reticulated flatwoods salamander has a more netlike appearance than the frosted flatwoods salamander, as the common names imply.

In summary, in the Proposed Regulation Promulgation section of this document, we propose the taxonomic change to reflect the split of flatwoods salamander (Ambystoma cingulatum) to frosted flatwoods salamander (Ambystoma cingulatum) and reticulated flatwoods salamander (Ambystoma bishopi).
Listing of the Reticulated Flatwoods Salamander

History of the Action

On December 16, 1997, we published a proposed rule to list the flatwoods salamander as a threatened species (62 FR 65787). The final rule to list the species was published on April 1, 1999 (64 FR 15691). We are now proposing to list the reticulated flatwoods salamander as a new species that is currently known west of the ApalachicolaFlint Rivers as the flatwoods salamander.

Species Information

As far as we currently know, the lifehistory traits and habitat use of both the frosted flatwoods salamander and the reticulated flatwoods salamander are similar to those previously described for the flatwoods salamander. Both species of flatwoods salamanders are moderately sized salamanders that are generally black to chocolate black with fine, irregular, light gray lines and specks that form a crossbanded pattern across their backs (back pattern more netlike in the reticulated flatwoods salamander). The frosted flatwoods salamander generally tends to be larger than the reticulated flatwoods salamander, as described above. Adults are terrestrial and live underground most of the year. They breed in relatively small, isolated ephemeral ponds where the larvae develop until metamorphosis. Postmetamorphic salamanders migrate out of the ponds and into the uplands where they live until they move back to ponds to breed as adults. Both species of flatwoods salamander are endemic to the lower southeastern Coastal Plain and occur in what were historically longleaf pinewiregrass flatwoods and savannas.

The historical range of what is now considered the reticulated flatwoods salamander included parts of the States of Alabama, Florida, and Georgia, which are in the lower Coastal Plain of the southeastern United States west of the ApalachicolaFlint Rivers. We have compiled 26 historical (pre1990) records for the reticulated flatwoods salamander.

In Alabama, there are five historical localities for the reticulated flatwoods salamander, all in the extreme southern portion of the State in Baldwin, Covington, Houston, and Mobile Counties. Surveys have been conducted at numerous sites since 1992; however, no reticulated flatwoods salamanders have been observed in Alabama since 1981 (Jones et al. 1982, p. 51; Godwin 2008).

Two historical records for the reticulated flatwoods salamander are known for Georgia, one each in Baker and Early Counties. There has been no observation of this species at either of these sites in the last 20 years. Four new reticulated flatwoods salamander breeding ponds have been discovered since 1990. One pond is on the Mayhaw Wildlife Management Area owned by the State of Georgia in Miller County. Three ponds are on private property in Baker County. Currently, two reticulated flatwoods salamander populations are supported by these breeding sites in Georgia.

Nineteen historical (pre1990) records for the reticulated flatwoods salamander are known for Florida. Reticulated flatwoods salamander breeding has been documented at only five (26 percent) of these sites since 1990. Extensive surveys throughout the range of the Ambystoma cingulatum, conducted prior to the original listing in 1999, resulted in identifying 40 additional breeding sites. Thirtyone (78 percent) of these sites are located in Okaloosa and Santa Rosa Counties, primarily on Department of Defense lands. Currently, 19 populations of the reticulated flatwoods salamander are known from Florida.

The combined data from all survey work completed since 1990 in Florida and Georgia indicate there are 21 populations of the reticulated flatwoods salamander. Some of these populations are inferred from the capture of a single individual. Ten (48 percent) of the known reticulated flatwoods salamander populations occur, at least in part, on public land. Of these, Department of Defense lands in Florida harbor four populations of the reticulated flatwoods salamander at Eglin Air Force Base, Hurlburt Field, and Naval Air Station Whiting Field's Holley OutLying Field. State and local agencies in Florida and Georgia partially manage six additional populations. In Florida, Pine Log State Forest and Point Washington State Forest harbor a single population each; Northwest Florida Water Management District owns a small portion of the habitat occupied by a single population and shares management with the Yellow Creek Marsh State Buffer Preserve of most of another property supporting an additional population; and the Santa Rosa County School Board owns a portion of the habitat supporting a single population. In Georgia, the Mayhaw Wildlife Management Area supports a single population. Eleven (52 percent) reticulated flatwoods salamander populations are solely on private land.
Summary of Factors Affecting the Species (Reticulated Flatwoods Salamander)

Section 4 of the Act and regulations (50 CFR part 424) promulgated to implement the listing provisions of the Act set forth the procedures for adding species to Federal lists. A species may be determined to be an endangered or threatened species due to one or more of the five factors described in section 4(a)(1). The original listing rule for the flatwoods salamander (64 FR 15691) contained a discussion of these five factors. Only those factors relevant to the proposed reclassification of the reticulated flatwoods salamander (Ambystoma bishopi; Goin, 1950) from threatened to endangered are described below:
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A. The Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range

The major threat to the reticulated flatwoods salamander is loss of both its longleaf pineslash pine flatwoods terrestrial habitat and its isolated, seasonally ponded breeding habitat. The combined pine flatwoods (longleaf pinewiregrass flatwoods and slash pine flatwoods) historical area was approximately 32 million acres (ac) (12.8 million hectares (ha)) (Outcalt 1997, p. 4). This area has been reduced to 5.6 million ac (2.27 million ha) or approximately 18 percent of its original extent (Outcalt 1997, p. 4). These remaining pine flatwoods (nonplantation forests) areas are typically fragmented, degraded, secondgrowth forests (Outcalt 1997, p. 6). Conversion of pine flatwoods to intensively managed (use of heavy mechanical site preparation, high stocking rates, low fire frequencies) slash or loblolly plantations often resulted in degradation of flatwoods salamander habitat by creating wellshaded, closedcanopied forests with an understory dominated by shrubs or pine needles (Outcalt 1997, pp. 46; Palis 1997, pp. 6163). Disturbancesensitive groundcover species, such as wiregrass (Aristida stricta [= A. beyrichiana] Kesler et al. 2003, p. 9), dropseed (Sporobolus spp.), and perennial forbs were either greatly reduced in extent or were replaced by weedy pioneering species (Moore et al. 1982, p. 216; Outcalt and Lewis 1988, pp. 112; Hardin and White 1989, pp. 243244). In a study conducted by Hedman et al. (2000, p. 233), longleaf pine plots had significantly more herbaceous species and greater herbaceous cover than loblolly or slash pine plots. For example, wiregrass is often lost from a site when habitat is converted from longleaf pine forest to other habitat types using common mechanical site preparation methods (Outcalt and Lewis 1988, p. 2). Loss of wiregrass is considered an indicator of site degradation from fire suppression or soil disturbance (Clewell 1989; pp. 226, 230232). Flatwoods salamanders are unlikely to persist in uplands with a disturbed, wiregrassdepauperate groundcover (Palis 1997, p. 63).

Forest management that includes intensive site preparation may adversely affect flatwoods salamanders directly and indirectly (Means et al. 1996, p. 426). Bedding (a technique in which a small ridge of surface soil is elevated as a planting bed) alters the surface soil layers, disrupts the site hydrology, and often eliminates the native herbaceous groundcover. This can have a cascading effect of reducing the invertebrate community that serves as a food source for flatwoods salamander adults. Postlarval and adult flatwoods salamanders occupy upland flatwoods sites where they live underground in crayfish burrows, root channels, or burrows of their own making (Goin 1950, p. 311; Neill 1951, p. 765; Mount 1975, pp. 9899; Ashton and Ashton 2005, pp. 63, 65, 6871). The occurrence of these underground habitats is dependent upon protection of the soil structure. Intensive site preparation destroys the subterranean voids and may result in entombing, injuring, or crushing individuals.

Ecologists consider fire suppression the primary reason for the degradation of remaining longleaf pine forest habitat. The disruption of the natural fire cycle has resulted in an increase in slash and loblolly pine on sites formerly dominated by longleaf pine, an increase in hardwood understory, and a decrease in herbaceous ground cover (Wolfe et al. 1988, p. 132). Although reticulated flatwoods salamanders have been found at sites with predominately loblolly or slash pine, the longterm viability of populations at these sites is unknown. On public lands, prescribed burning is a significant part of habitat management plans. However, implementation of prescribed burning has been inconsistent due to financial constraints and limitations of weather (drought, wind direction, etc.) that restrict the number of opportunities to burn.

These alterations of the longleaf pine ecosystem, as a result of incompatible forest practices, have caused historic losses of reticulated flatwoods salamander habitat. Although conversion of native pine flatwoods to plantation forests is not considered a significant threat at this time, we have documented the historic extirpation of at least one previously known population each from Gulf and Jackson Counties in Florida, over the last four decades because of habitat degradation on lands currently managed as pine plantations. In addition, ponds surrounded by pine plantations and protected from the natural fire regime may become unsuitable reticulated flatwoods salamander breeding sites due to canopy closure and the resultant reduction in emergent herbaceous vegetation needed for egg deposition and larval development sites (Palis 1997, p. 62). In addition, lack of fire within the pond during periods of drydown may result in chemical and physical (vegetative) changes that are unsuitable for the salamander (Palis 1997, p. 62). Lack of fire in the ecotone may result in the development of a thick shrub zone making it physically difficult or impossible for adult salamanders to enter the breeding ponds (Ripley and Printiss 2005, pp. 12, 11).

Land use conversions to urban development and agriculture eliminated large areas of pine flatwoods in the past (Schultz 1983, pp. 2447; Stout and Marion 1993, pp. 422429; Outcalt and Sheffield 1996, pp. 15; Outcalt 1997, pp. 16). Urbanization and agriculture have resulted in the loss of one reticulated flatwoods salamander population from each of the following counties: Mobile and Baldwin Counties, Alabama; Escambia, Jackson, and Washington Counties, Florida; and Early County, Georgia. Two known populations have been extirpated from Santa Rosa County, Florida. State forest inventories completed between 1989 and 1995 indicated that flatwoods losses through land use conversion were still occurring (Outcalt 1997, pp. 36). Urbanization in the panhandle of Florida and around major cities is reducing the available pine forest habitat. Wear and Greis (2002, pp. 47, 92) identify conversion of forests to urban land uses asthe most significant threat to southern forests. They predict that the South could lose about 12 million ac (4.9 million ha) of pine forest habitat to urbanization between 1992 and 2020. Several relatively recent discoveries of previously unknown reticulated flatwoods salamander breeding sites in Santa Rosa County, Florida, have been made in conjunction with wetland surveys associated with development projects (Cooper 2008). No reticulated flatwoods salamanders have been observed at these degraded sites since completion of the projects (Cooper 2008).

In addition to the loss of upland forested habitat, the number and diversity of small wetlands where reticulated flatwoods salamanders breed have been substantially reduced. Threats to breeding sites include alterations in hydrology, agricultural and urban development, road construction, incompatible silvicultural practices, shrub encroachment, dumping in or filling of ponds, conversion of wetlands to fish ponds, domestic animal grazing, soil disturbance, and fire suppression (Vickers et al. 1985, pp. 2226; Palis 1997, p. 58; Ashton and Ashton 2005, p. 72). Hydrological alterations, such as those resulting from ditches created to drain flatwoods sites or fire breaks and plow lines, represent one of the most serious threats to reticulated flatwoods salamander breeding sites. Lowered water levels and shortened
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hydroperiods at these sites may prevent successful flatwoods salamander recruitment because larval salamanders require 11 to 18 weeks to reach metamorphosis and leave the ponds (Palis 1995, p. 352).

USGS has documented multiple drought periods in the southeastern United States since the 1890s (USGS Open File Report 00380, p. 1). Among significant periods documented in the last three decades are: 19801982, 19841988, 19982000 (USGS Water Supply Paper 2375) and currently from 20062008. Although a naturally occurring condition, drought presents additional complications for a species, like reticulated flatwoods salamander, which has been extirpated from most of its historic range and for which populations are represented by single ponds. Palis et al. (2006, (p. 56) conducted a study in Florida on a population of the closely related frosted flatwoods salamander during a drought from 19992002. This study found three consecutive years of reproductive failure and a steadily declining adult immigration to breed at the site as the drought progressed. Taylor et al. (2005, (p. 792) noted that wide variation in reproductive success is common among pondbreeding amphibians that depend on seasonal filling of these areas, but that adult persistence may buffer against fluctuations in that success, particularly for species that are long lived. Although Palis et al. (2006) suggested that the flatwoods salamander may only live about four years (based on captive animals), we are currently unsure of the exact life span of wild individuals. Because of this, it is difficult to predict how long adults could persist in the landscape without a successful breeding event to replenish the population. However, Taylor et al. (2005, pp. 792, 796) constructed a model to look at how many years of reproductive failure would be required to result in local extinction of pondbreeding salamanders (with varying life spans) and found that even without total reproductive failure, populations required moderate to high upland postmetamorphic survival to persist. Catastrophic failure in this study created fluctuations in the population, raised the threshold of survival required to achieve persistence, and imposed the possibility of extinction even under otherwise favorable environmental conditions. Reproductive failure for this species was closely tied to hydrologic conditions; insufficient or short hydroperiod was the primary cause for complete failure. In addition, early filling of the ponds could also facilitate the establishment of invertebrate or vertebrate predators before hatching of the eggs(p.796). Palis et al . (2006, p. 67) discussed the necessity of protecting clusters of flatwoods salamander breeding sites, especially those with different hydrologic regimes, to guard against population declines at any one breeding site resulting from stochastic events, such as droughts (Palis 2006, p. 7). Currently, the only place this situation exists for the reticulated flatwoods salamander is on Eglin Air Force Base and these populations are threatened with the construction of a proposed highway.

Habitat fragmentation of the longleaf pine ecosystem resulting from habitat conversion threatens the survival of the reticulated flatwoods salamander. Large tracts of intact longleaf pine flatwoods habitat are fragmented by pine plantations, roads, and unsuitable habitat. Most reticulated flatwoods salamander populations are widely separated from each other by unsuitable habitat. This has been verified through recent reviews of aerial photography and site visits to localities of historical and current records for the species. Studies have shown that the loss of fragmented populations is common, and recolonization is critical for their regional survival (Fahrig and Merriam 1994, pp. 50 56; Burkey 1995, pp. 527540). Amphibian populations may be unable to recolonize areas after local extirpations due to their physiological constraints, relatively low mobility, and site fidelity (Blaustein et al. 1994, pp. 60, 6768). In the case of the reticulated flatwoods salamander, 70 percent of populations only have one breeding pond and if the habitat at that site is destroyed, recolonization would be impossible (see further discussion of metapopulation dynamics under Factor E.

Roads contribute to habitat fragmentation by isolating blocks of remaining contiguous habitat. They may disrupt migration routes and dispersal of individuals to and from breeding sites. Road construction can result in destruction of breeding ponds, as described above. In addition, vehicles may also cause the death of reticulated flatwoods salamanders when they are attempting to cross roads (Means 1996, p. 2). Road construction resulted in the destruction of a historic reticulated flatwoods salamander breeding pond in Escambia County, Florida (Palis 1997, p. 62). A road through Eglin Air Force Base (Eglin AFB) and Hurlburt Field has been proposed and the preferred alternative was selected in 2007 (Northwest Florida Transportation Corridor Authority 2007; Arnold 2007). We are currently in consultation regarding this bypass project, however, currently there are no viable alternatives to the preferred alternative and the alignment cannot be moved further north on the base due to its potential to impact the mission (Arnold 2007). We believe this proposed road would destroy or severely degrade 22 breeding sites that support the largest reticulated flatwoods salamander population (Mittiga 2007). These breeding sites represent 44 percent of the known reticulated flatwoods salamander ponds. This Eglin population represents the only population of this species supported by more than three breeding ponds and functions as a metapopulation.

Offroad vehicle (ORV) use within reticulated flatwoods salamander breeding ponds and their margins severely degrades the wetland habitat. In the Southeast, ORV use impacts habitat used by flatwoods salamanders and has the potential to cause direct mortality of individual salamanders and is a threat on both public and private land. On public lands there may be areas designated as off limits to ORV use (U.S. Forest Service 2007, p. 19), but these restrictions are very hard to enforce. Even a single afternoon of individuals riding their ORVs in a pond can completely destroy the integrity of breeding sites by damaging or killing the herbaceous vegetation and rutting the substrate (Ripley and Printiss 2005, pp. 1112). There is also the potential for direct injury or mortality of salamanders by ORVs at breeding sites (Ripley and Printiss 2005, p. 12).

Insummary, the loss of habitat is a significant threat the reticulated flatwoods salamander. This threat is compounded by the current environmental conditions, proposed projects, projects which do not require Corps permits, and the nature of pondbreeding salamanders to undergo periodic reproductive failure. We consider this threat to be imminent and of high magnitude because of this species' narrow range and the loss of its habitat loss that is currently occurring at a rapid rate on lands in private ownership within the range of this species. Fiftyseven percent of reticulated flatwoods salamander populations are on private land, where habitat continues to be degraded by fire suppression and inappropriate management. The proposed road project on Eglin could result in destruction or degradation of 44 percent of remaining breeding ponds and the only metapopulation that exists for the reticulated flatwoods salamander. Rangewide historic losses of both upland and wetland habitat have
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occurred due to conversion of flatwoods sites to agriculture, urban development, and intensively managed pine plantations. The remaining flatwoods habitat continues to be threatened by fire suppression and other incompatible forest management practices, road construction, and habitat fragmentation across the range of the species. Localized threats to existing wetland breeding sites include alterations in hydrology from agriculture, urban development, road construction, and incompatible forest management; ORVs; and fire suppression. As a result, we have determined that the present or threatened destruction, modification, or curtailment of the reticulated flatwoods salamander is a significant threat to the species.
B. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes

Overcollecting does not appear to be a threat to the reticulated flatwoods salamander at this time. There is no evidence of a past or current problem with collection of this species. Consequently, we have determined that overutilization for commercial, recreational, scientific, or educational purposes is not a threat to the reticulated flatwoods salamander at this time.

C. Disease or Predation

Although disease has not been specifically documented in the reticulated flatwoods salamander thus far, disease outbreaks with mass mortality in other species of salamanders indicate that disease may be a threat for this species as well (Daszak et al. 1999, p. 736). ``Red leg'' disease (Aeromonas hydrophila), a pathogen bacterium, caused mortality of the mole salamander (A. talpoideum) at the breeding pond of the reticulated flatwoods salamander in Miller County, Georgia (Maerz 2006), and reticulated flatwoods salamanders have not been observed at this site since the disease was reported. In addition, Whiles et al. (2004, p. 211) found a parasitic nematode (Hedruris siredonis, family Hedruridae) in larvae of the closely related frosted flatwoods salamander from South Carolina and Florida. This parasite has been found in other ambystomatids and can cause individuals to become undersized and thin, thus reducing their fitness (Whiles et al. 2004, p. 212). The infestations were not considered heavy and were probably not having a negative impact on the larvae studied; however, environmental degradation may change the dynamics between salamander populations and normally innocuous parasites (Whiles et al. 2004, p. 212). Ranaviruses in the family Iridoviridae and chytrid fungus may be other potential threats, although the susceptibility of the reticulated flatwoods salamander to these diseases is unknown. Ranaviruses have been responsible for dieoffs of tiger salamanders throughout western North America and spotted salamanders (A. maculatum) in Maine (Daszak et al. 1999, p. 736). Chytrid fungus has been discovered and associated with mass mortality in tiger salamanders in southern Arizona and California, and the Santa Cruz longtoed salamander (A. macrodactylum croceum) (Vredenburg and Summers 2001, p. 151; Davidson et al. 2003, p. 601; PadgettFlohr and Longcore 2005, p. 50). This discussion of disease in other species of closely related salamanders indicates the potential existence of similar threats to reticulated flatwoods salamander populations.

Exposure to increased predation by fish is a threat to the reticulated flatwoods salamander when isolated, seasonally ponded wetland breeding sites are changed to or connected to more permanent wetlands inhabited by fish species not typically found in temporary ponds. Studies of other ambystomatid species have demonstrated a decline in larval survival in the presence of predatory fish (Semlitsch 1987, p. 481). Ponds may be modified specifically to serve as fish ponds or sites may be altered because of drainage ditches, firebreaks, or vehicle tracks that can all provide avenues for fish to enter the wetlands.

Red imported fire ants (Solenopsis invicta) are potential predators of flatwoods salamanders, especially in disturbed areas. They have been seen in areas disturbed by the installation of drift fences at known breeding sites (Palis 2008). Mortality of amphibians trapped at drift fences has occurred when fire ants were present and traps were not monitored with sufficient frequency (NCASI 2002, p. 6). The severity and magnitude, as well as the longterm effect of fire ants on reticulated flatwoods salamander populations is currently unknown.

Diseases of amphibians in the southeastern United States remain largely unstudied. However, given the incidence of disease in species which could be considered surrogates for the flatwoods salamander, the probability exists for similar infections to occur in reticulated flatwoods salamander populations. Predation by fish is a historic threat that continues to be a localized problem when ditches, firebreaks, or vehicle ruts provide connections allowing the movement of fish from permanent water bodies into reticulated flatwoods salamander breeding sites. Fireants also have the potential of being a localized threat, particularly in disturbed areas. We consider this threat to be imminent and of high magnitude because 70 percent of populations are supported by a single breeding pond and diseases, fish, and invertebrate predators have been found at ponds within the range and are known to cause mortality or reproductive failure in related species. Additionally 57 percent of ponds are on private land, increasing the probability of fish being introduced to a breeding site, which would then cause the breeding habitat to become unsuitable, and result in the extinction of the population. Fire ants also have the potential of being a localized threat, particularly in disturbed areas. As such, we believe that these threats would also act to exacerbate other threats to the species.

D. The Inadequacy of Existing Regulatory Mechanisms

There are no existing regulatory mechanisms for the protection of the upland habitats where reticulated flatwoods salamanders spend most of their lives. Section 404 of the Clean Water Act is the primary Federal law that has the potential to provide some protection for the wetland breeding sites of the reticulated flatwoods salamander. However, due to recent case law (Solid Waste Agency of Northern Cook County (SWANCC) v. U.S. Army Corps of Engineers 2001; Rapanos v. U.S. 2006), isolated wetlands are no longer considered to be under Federal jurisdiction (not regulatory wetlands). Wetlands are only considered to be under the jurisdiction of the Corps if a ``significant nexus'' exists to a navigable waterway or its tributaries. Currently, some Corps Districts do not coordinate with us on flatwoods salamanders and, since isolated wetlands are not considered under their jurisdiction, they are often not included on maps in permit applications (Brooks 2008). We are aware of two isolated wetlands that supported flatwoods salamander populations that have been lost since 2006 under this scenario.

Longleaf pine habitat management plans have been written for public lands occupied by the reticulated flatwoods salamander. They include management plans for Stateowned lands and integrated natural resource management plans (INRMPs) for Department of Defense lands. Most of the plans contain specific goals and objectives regarding
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habitat management that would benefit reticulated flatwoods salamanders including prescribed burning. However, because multipleuse is the guiding principle on most public land, protection of the flatwoods salamander may be just one of many management goals including timber production and military and recreational use. Implementation of the plans has often been problematic due to financial and logistic constraints. In addition, the plans do not provide assured protection from habitat destruction or degradation from land use changes such as the proposed road on Eglin AFB and Hurlburt Field (see Factor A, above).

At the State and local levels, regulatory mechanisms are limited. Although not listed as threatened or endangered in Alabama, the reticulated flatwoods salamander is listed among those nongame species for which it is ``unlawful to take, capture, kill, or attempt to take, capture or kill; possess, sell, trade for anything of monetary value, or offer to sell or trade for anything of monetary value'' (Alabama Department of Conservation and Natural Resources 2008, p. 1). The flatwoods salamander is listed as a threatened species in the State of Georgia (Jensen 1999, pp. 9293). This designation protects the species by preventing its sale, purchase, or possession in Georgia and by prohibiting actions that cause direct mortality or the destruction of its habitat on lands owned by the State of Georgia (Ozier 2008). There is only one known flatwoods salamander population on lands owned by the State of Georgia, and that is Mayhaw Wildlife Management Area. In 2001, the Florida Fish and Wildlife Conservation Commission (FFWCC) listed the flatwoods salamander (which would include the reticulated flatwoods salamander) as a species of special concern (FFWCC 2007, p. 2) and prohibited direct take except through permit. As part of the listing process, a statewide management plan was developed for the salamander in Florida (FFWCC 2001, p. 160). This plan sets an ambitious conservation goal of maintaining at least 129 selfsustaining populations of flatwoods salamanders (would include both frosted and reticulated flatwoods salamander species) in Florida. The plan also outlines a monitoring plan for population status assessment, an implementation strategy for the management of populations, and areas for future research. The Alabama and Florida regulations offer no protection against the most significant threat to the reticulated flatwoods salamander, loss of habitat.

In summary, existingregulatory mechanisms provide little direct protection of reticulated flatwoods salamander habitat, the loss of which is the most significant threat to the species. Reticulated flatwoods salamander breeding sites may in some instances come under the jurisdiction of the Corps, but most often they are provided little regulatory protection. These inadequacies represent rangewide historic and known threats to the reticulated flatwoods salamander on private lands within the range. We consider this threat as imminent because the existing regulations are not protecting against the other imminent threats to the species. Also, this threat is of high magnitude because of the small range of the species, and because 57 percent of populations are not protected from further development because they are located on private lands.
E. Other Natural or Manmade Factors Affecting Its Continued Existence

Metapopulations, which are neighboring local populations close enough to one another that dispersing individuals could be exchanged (gene flow) at least once per generation, are important to the long term survival of temporary pond breeding amphibians. In these species, such as the reticulated flatwoods salamander, breeding ponds may differ in the frequency of their ability to support amphibian reproduction. As a result, extirpation and colonization rates can be a function of pond spatial arrangement as well as local habitat quality (Marsh and Trenham 2001, p. 41). Of the 21 known reticulated flatwoods salamanders populations, only 6 (29 percent) are supported by more than one breeding pond and only one (5 percent) population (on Eglin AFB Hurlburt Field) is supported by more than three breeding ponds. For 71 percent (15 out of 21) of the known reticulated flatwoods salamander populations, any one of the many threats that may render a breeding pond unsuitable could cause the extirpation of the affected population.

Invasive plant species, such as cogongrass (Imperata cylindrica), threaten to further degrade existing flatwoods habitat. Cogongrass, a perennial grass native to southeast Asia, is one of the leading threats to the ecological integrity of native herbaceous flora, including that in the longleaf pine ecosystem (Jose et al. 2002, p. 43). It has been documented that cogongrass can displace most of the existing vegetation except large trees. Especially threatening to the reticulated flatwoods salamander is the ability of cogongrass to outcompete wiregrass, a key vegetative component of flatwoods salamander habitat. Changing the species composition in this way can alter the soil chemistry, nutrient cycling, and hydrology of an infested site (Jose et al. 2002, p. 43). Reticulated flatwoods salamander habitat management plans will need to address threats posed by cogongrass and other invasive plant species and include strategies to control them. An integrated management approach to controlling cogongrass is outlined in Jose et al. (2002, p. 42).

Pesticides (including herbicides) may pose a threat to amphibians such as the reticulated flatwoods salamander, because their permeable eggs and skin readily absorb substances from the surrounding aquatic or terrestrial environment (Duellman and Trueb 1986, pp. 199200). Negative effects that commonly used pesticides and herbicides may have on amphibians include delayed metamorphosis, paralysis, reduced growth rate, and mortality (Bishop 1992, pp. 6769). Herbicides used near reticulated flatwoods salamander breeding ponds may alter the density and species composition of vegetation surrounding a breeding site and reduce the number of potential sites for egg deposition, larval development, or shelter for migrating salamanders. Aerial spraying of herbicides over outdoor pond mesocosms (semifield approximations of ponds) has been shown to reduce zooplankton diversity, a food source for larval reticulated flatwoods salamanders, and cause very high (68 to 100 percent) mortality in tadpoles and juvenile frogs (Relyea 2005, pp. 618626). The potential for negative effects from pesticide and herbicide use in areas adjacent to breeding ponds would be reduced by avoiding aerial spraying (Tatum 2004, p. 1047).

Studies of other ambystomatid species have demonstrated a decline in larval survival in the presence of predatory fish, as mentioned above under Factor C. One of the potential reasons for this decline may be the negative effect that these fish have on the invertebrate prey of salamander larvae. The invertebrates found by Whiles et al. (2004, p. 212) in a study of larval frosted and reticulated flatwoods salamander gut contents are typical of freshwater habitats in the Southeast that do notcontainpredatory fish on a regular basis. The presence of predatory fish has a marked effect on invertebrate communities and alters prey availability for larval salamanders
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with the potential for negative effects on larval fitness and survival (Semlitsch 1987, p. 481). Wherever connections have been created between permanent water and flatwoods salamander ponds, through installation of firebreaks, ditches, and so on, this threat from predatory fish exists.

Studies of reticulated flatwoods salamander populations since the original species classification of flatwoods salamander was listed (64 FR 15691; April 1, 1999) have been limited due to drought. Data on the numbers of adults within existing populations does not exist. However, given the low number of individuals encountered even when breeding is verified, populations are likely to be very small at any given breeding site. Small populations are at increased threat of extirpation from natural processes (genetic isolation, inbreeding depression, and drought), as well as the manmade threats listed above.

In summary, there a number of other natural or manmade factors that either threaten, or have the potential to threaten, that have been historic threats and continue to threaten the reticulated flatwoods salamander. The loss of metapopulation structure in the distribution of reticulated flatwoods salamander populations was a rangewide threat that caused historic losses of this species. It continues to be a current threat for most of the remaining reticulated flatwoods salamander populations, particularly on Eglin Air Force Base. Fire suppression and inadequate habitat management continue to cause the degradation of occupied sites, primarily on private land. Invasive plant species probably did not have much of a historic impact on salamander populations, but they are a rangewide potential threat, especially as they become more widespread and difficult to control. Rangewide, low densities of individuals in a given population have been a historic threat and continue to be a threat for most reticulated flatwoods salamander populations, particularly in the face of the past and current drought conditions and given the nature of pondbreeding amphibians to experience periodic reproductive failures naturally. The impact competing predators may have on the salamander's prey base, and the threat of pesticide and herbicide use, are less clear as historic threats but remain potential localized threats for the species. Therefore, while we have determined that other natural and manmade factors, such as invasive species, pesticides, and competition for the species' prey base may threaten the reticulated flatwoods salamander, the severity and magnitude of these threats are not currently known. Acting in coordination with major threats listed above with each other, these threats constitute additional complicating factors which could exacerbate other threats. In addition, small population size is particularly detrimental when combined with habitat loss, the ongoing drought, and the nature of this pondbreeding amphibians to experience periodic reproductive failure.

Determination

We have carefully assessed the best scientific and commercial information available regarding the past, present, and future threats to the reticulated flatwoods salamander. In summary, the significant threat to the reticulated flatwoods salamander listed in Factor A (above), is loss of its habitat. However, a variety of localized threats factors (which fall under Factors A, D, and E) continue to impact existing wetland breeding sites including alterations in hydrology from agriculture (including ``ditching,'' which results in the introduction of predatory fish), urban development, road construction, and incompatible forest management, ORV use, fire suppression, and disease also threaten the species, but the severity and magnitude of these threats is not currently known. As a result, we have determined that these factors will exacerbate the effects of threats due to habitat loss and drought. As described in Factor E above, small populations are at increased threat of extirpation from natural processes (genetic isolation, inbreeding depression, and drought), as well as the manmade threats listed above. Furthermore, as described in Factor D (above), existing regulatory mechanisms provide little direct protection of reticulated flatwoods salamander habitat, the loss of which is the most significant threat to the species. Reticulated flatwoods salamander breeding sites may in some instances come under the jurisdiction of the Corps, but most often they are provided little regulatory protection. This is likely the reason that two populations were lost recently to development. These inadequacies of existing regulatory mechanisms addressing habitat loss represent rangewide historic and potential threats to the reticulated flatwoods salamander. Finally, there are potential localized threats from fire ants, pesticides, and invasive plants for which the extent of impact is yet undeterminable, but that we believe are legitimate threats due to both their impact on surrogate species and their prevalence in the types of habitats used by this species.

Only 21 reticulated flatwoods salamander populations are known. Fifteen (71 percent) of these populations are supported by only one breeding site. A population with only one breeding site has a tenuous future just given randomly varying environmental factors without considering the additional threats of habitat destruction and degradation that further threaten these populations. As noted previously, we are currently experiencing drought conditions. Palis et al. (2006, p. 56) studied a frosted flatwoods population in Florida during a drought from 19992002. This study documented three consecutive years of reproductive failure and a steady declining adult immigration to the site for breeding as the drought progressed. Catastrophic reproductive failure occurs even in healthy populations of pondbreeding amphibians. When it does occur, the modeling efforts of Taylor et al. (2005, p. 796) showed that each year of reproductive failure raises the threshold of survival required to achieve persistence and imposes the possibility of extirpation even under otherwise favorable environmental conditions. Taylor et al . (2005, p. 799) reminds us that particularly with small populations or low population growth rates (as exists with the reticulated flatwoods salamander) effects of reproductive failure are made worse by demographic stochasticity. Even in populations with multiple breeding ponds, amphibian populations may be unable to recolonize areas after local extirpations due to their physiological constraints, relatively low mobility, and site fidelity (Blaustein et al. 1994, pp. 60, 6768). In the case of the reticulated flatwoods salamander, 71 percent of populations have only one breeding pond. If the habitat at that site is destroyed, recolonization would be impossible and the population supported by that breeding pond would be extirpated. Since the early 1990s, fourreticulated flatwoods salamander populations have been lost, two populations due to urbanization and two populations due to inappropriate forest management. The most robust reticulated flatwoods salamander population remaining is currently threatened by a proposed road through Eglin AFB. The preferred alignment for this road (Mittiga 2007) could destroy or degrade 44 percent of the known reticulated flatwoods salamander breeding sites. This is significant because the Eglin AFB population is the only location which is supported by more than 3 breeding ponds and functions as a metapopopulation. In other words, this population has the
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best chance of surviving demographic and environmental stochasticity given the distribution of breeding sites within reticulated flatwoods salamander dispersal distance of each other. However, habitat supporting this population continues to decline due to inadequate prescribed burning. The presence of a road in this vicinity, even if there are no direct impacts to vegetative structure or hydrology of the breeding and upland sites, will only decrease the opportunities to burn the area and increase the habitat degradation.

Habitat loss on private lands is an imminent threat that is compounded by a variety of other factors. Fire suppression on private lands occupied by the reticulated flatwoods salamander represents one of the biggest threats to the species' habitat and the continued existence of the species on these sites. In addition, we have lost at least two ponds since 2006 in the range of the reticulated flatwoods salamander that we believe resulted from the continuing threat that isolated wetlands are rarely, if ever, under the jurisdiction of the Corps, thus resulting in limited to no regulatory mechanisms addressing this imminent threat. The Eglin bypass (described as sections FWB/ Niceville Bypass, Navarre Bypass and SR 87, collectively) are shown on the Northwest Florida Transportation Corridor Authority website as priority projects for the next five years, meaning FY 2008FY 2012 (Prioritized Master Plan). A preferred alternative was selected in 2007, but no environmental analysis has been conducted at present. This preferred alignment was chosen because any move further north would impact the mission of base. We believe there is a reasonable expectation that this road could be built, and it is considered an imminent threat to the species, its habitat, and overall to the continued existence of the population on Eglin AFB. We believe that combined, the effect of the historical and ongoing drought, historical, current, and projected habitat loss and degradation (including the proposed bypass on Eglin), and the exacerbating effects of disease, predation, small population size, and isolation would result in the reticulate flatwoods salamander being in danger of extinction throughout all of its range. We believe these threats, in particular the threats from habitat loss and drought, to be current and are projected to continue at the current rate or increase in the future. Further, we have determined that these threats are operating on the species and its habitat with a high degree of magnitude in that they affect the species throughout all of its range and with a high degree of severity, as discussed above.

Based on the best available scientific and commercial information, we have determined that the reticulated flatwoods salamander is in danger of extinction throughout all or a significant portion of its range. Therefore, we are proposing to list the reticulated flatwoods salamander as an endangered species under the Act. Endangered status reflects the vulnerability of this species to factors that negatively affect the species and its limited and restricted habitat.
We are soliciting comments on this proposed rule and threats to the species. Similarly, we request any available information on ongoing or proposed development activities within reticulated flatwoods salamander habitat.
Available Conservation Measures
Conservation measures provided to species listed as endangered or threatened under the Act include recognition, recovery actions, requirements for Federal protection, and prohibitions against certain practices. Recognition through listing results in public awareness and conservation by Federal, State, and local agencies, private organizations, and individuals. The Act provides for possible cooperation with the States and requires that recovery actions be carried out for all listed species. The protection required of Federal agencies and the prohibitions against certain activities involving listed plants are discussed in ``Effect of Critical Habitat Designation'' for critical habitat and are further discussed, in part, below.
Section 7(a) of the Act requires Federal agencies to evaluate their actions with respect to any species that is proposed or listed as endangered or threatened and with respect to its critical habitat, if any is being designated. Regulations implementing this interagency cooperation provision of the Act are codified at 50 CFR part 402. Section 7(a)(4) requires Federal agencies to confer with the Service on any action that is likely to jeopardize the continued existence of a species proposed for listing or result in destruction or adverse modification of proposed critical habitat. If a species is listed subsequently, section 7(a)(2) requires Federal agencies to ensure that activities they authorize, fund, or carry out are not likely to jeopardize the continued existence of the species or destroy or adversely modify its critical habitat. If a Federal action may affect a listed species or its critical habitat, the responsible Federal agency must enter into formal consultation with the Service.
Federal agency actions within the species habitat that may require conference or consultation or both as described in the preceding paragraph include management and any other landscape altering activities on Federal lands administered by the Department of Defense, Fish and Wildlife Service, and U.S. Forest Service; issuance of section 404 Clean Water Act permits by the Army Corps of Engineers; construction and management of gas pipeline and power line rightsof way by the Federal Energy Regulatory Commission; and construction and maintenance of roads or highways by the Federal Highway Administration.

The Act and its implementing regulations set forth a series of general prohibitions and exceptions that apply to all endangered wildlife. The prohibitions, codified at 50 CFR 17.21 for endangered wildlife, in part, make it illegal for any person subject to the jurisdiction of the United States to take (includes harass, harm, pursue, hunt, shoot, wound, kill, trap, capture, or collect; or to attempt any of these), import, export, ship in interstate commerce in the course of commercial activity, or sell or offer for sale in interstate or foreign commerce any listed species. It is also illegal to possess, sell, deliver, carry, transport, or ship any such wildlife that has been taken illegally. Certain exceptions apply to agents of the Service and State conservation agencies.

We may issue permits to carry out otherwise prohibited activities involving threatened or endangered wildlife species under certain circumstances. Regulations governing permits are codified at 50 CFR 17.22 for endangered species. You may obtain permits for scientific purposes, to enhance the propagation or survival of the species, and for incidental take in connection with otherwise lawful activities. Critical Habitat

It is our intent to discuss only those topics directly relevant to the designation of critical habitat for the frosted and reticulated flatwoods salamander in this section of the proposed rule. For more information on the previous proposed rule to designate critical habitat for the flatwoods salamander, refer to the Federal Register document published on February 7, 2007 (72 FR 5856). The proposed rule, as presented herein,
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replaces the previous proposed rule in its entirety.

Previous Federal Actions

The flatwoods salamander was listed as threatened on April 1, 1999 (64 FR 15691). At that time, we found that designation of critical habitat for the flatwoods salamander was not prudent because such designation would not be beneficial and may increase threats to the species. On April 1, 2005, Center for Biological Diversity, Wild South, and Florida Biodiversity Project filed a lawsuit against the Secretary of the Interior alleging failure to designate critical habitat for the flatwoods salamander. In a courtapproved settlement agreement, we agreed to reevaluate the need for critical habitat for the species and if prudent submit a proposed designation of critical habitat to the Federal Register by January 30, 2007, and submit a final decision on the proposed critical habitat rule for publication in the Federal Register by January 30, 2008. A proposed rule to designate critical habitat for the flatwoods salamander published in the Federal Register on February 7, 2007 (72 FR 5856). Since that proposed rule published, new information has become available on taxonomy and additional threats to occupied habitat that has necessitated a reevaluation of the proposed rule. On January 25,

FOR FURTHER INFORMATION CONTACT Ray Aycock, Field Supervisor, U.S. Fish and Wildlife Service, Mississippi Field Office, 6578 Dogwood View Parkway, Jackson, MS 39213; telephone: 6013211122; facsimile: 601 9654340. If you use a telecommunications device for the deaf (TDD), call the Federal Information Relay Service (FIRS) at 8008778339.