Rapid Assessment for Identifying Species of Greatest Conservation Need: Towards a Unified Approach

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FEATURE Rapid Assessment for Identifying Species of Greatest Conservation Need: Towards a Unified Approach

Nicky M. H. Faucheux | Department of Biology/Aquatic Station, Texas State University, 601 University Drive, San Marcos, TX 78666 | Department of Wildlife, Fisheries, and Aquaculture, Mississippi State University, Mississippi State, MS. E-mail: [email protected] Cody A. Craig | Department of Biology/Aquatic Station, Texas State University, San Marcos, TX Timothy H. Bonner | Department of Biology/Aquatic Station, Texas State University, San Marcos, TX

U.S. Fish and Wildlife Service scuba divers search San Marcos River, Texas for the Fountain Darter Etheostoma fonticola. Fountain Darter is an endangered species of fish. Photo credit: Ryan Hagerty, U.S. Fish and Wildlife Service

© 2019 American Fisheries Society 488 Fisheries | Vol. 44 • No. 10 • October 2019 DOI: 10.1002/fsh.10289 Identification of imperiled species ranges from rapid, qualitative, expert opinion-based assessments to time-intensive, quantitative assessments. The purpose of our study was to develop a methodology to rapidly quantify species of greatest conservation need by incorporating the concepts of resiliency, redundancy, and representation, which are used by the U.S. Fish and Wildlife Service to identify imperiled species. We compiled records of species occurrences (a measure of redundancy), commonality (a measure of representation), and reported absences (a measure of resiliency) for 50 species of fish within three ecoregions of the southwestern USA. We used multivariate analysis to describe interrelationships among reach, drainage, and region occurrences; percent rare occurrences; and percent absent among reaches. Weighted summations of species scores for principal component axes I and II were sorted from least (i.e., towards low redundancy, representation, and resiliency) to greatest, and species were ranked. With a few limitations, our methodology provided a revisable, documented, and transparent approach to aid in the identification of species of greatest conservation need.

Identification of imperiled species is an initial step in rarity, threats, and population trends (73%); expert opinion conservation management (Male and Bean 2005). However, (65%); and global species ranking systems (e.g., International current identification processes lack standardization, often Union for Conservation of Nature [IUCN], 35%; NatureServe, rely on imprecise and incomplete information, and require 60%). Using these sources, decisions to identify SGCN were interpretation (Waples et al. 2013). Regulatory agencies (i.e., based on criteria ranking (33%), expert opinion (25%), or a federal and state entities) use a variety of approaches when combination of both (42%). Sources and decisions have lim- identifying imperiled species. The U.S. Fish and Wildlife itations. Although all SWAPs are required to have the same Service (USFWS) uses an analytical approach (i.e., Species purposes, the sources and decision processes are not standard- Status Assessments [SSAs]) to guide decisions on identifi- ized. Furthermore, global species ranking system estimates of cation and listing of species as threatened or endangered rarity, threats, and trends are generalized for some taxonomic under the Endangered Species Act of 1973 (USFWS 2016). groups and regions rather than at the species level and state or The SSAs include a comprehensive review of historical and local scale (Faber-Langendoen et al. 2012; Master et al. 2012). current distributional, ecological, and biological information Expert opinion can be susceptible to the subjectivity, experi- for candidate species (Smith et al. 2018). Assessments include ence level, and knowledge breadth of the expert (Clark et al. a summary of documented and potential threats to species’ 2006; Halpern et al. 2007; Donlan et al. 2010). long-term viability and a forecast of the species’ future with Processes and purposes differ between the USFWS listing known and potential threats. Assessments are reviewed by of species and the listing of SGCN. As such, USFWS and non-USFWS professionals who are familiar with the species, SGCN listing processes represent opposite endpoints along a and the assessments are updated prior to publication. The as- gradient of methodologies to support assessment of species sessments are subsequently reviewed and updated with current imperilment. The USFWS process is time consuming, com- information every 5 years (USFWS 2014, 2016). Each SSA is piles and considers all available species information, and usual- a multi-year process and incorporates the “3Rs” concepts of ly is used for one or a few species at a time, whereas the SGCN resiliency (i.e., tolerating stochastic disturbances), redundan- process is more rapid, does not necessarily compile and con- cy (i.e., surviving catastrophic events), and representation (i.e., sider all available species information, and considers a great- enduring environmental conditions; Shaffer and Stein 2000; er number of species (e.g., all freshwater fishes within state Smith et al. 2018) as a framework for identifying the level of boundaries). However, several published methodologies for species imperilment, current risks, and future risks of extinc- identifying imperiled species are intermediate in completion tion (e.g., USFWS 2017a, 2017b). time and the number of species to quantify. Methodologies in- In 2001, the U.S. Congress appropriated funding for state, clude comparing trends between historical and recent species territory, and tribal wildlife grant programs to develop State occurrences by watershed (Hudy et al. 2008) and using mul- Wildlife Action Plans (SWAPs) for all U.S. states and terri- tiple metrics (e.g., area occupied and estimated abundance; tories (Department of the Interior and Related Agencies Moyle et al. 2011) to develop rankings and priorities based on Appropriations Act of 2002). Purposes of the SWAPs are to multivariate analysis (rather than linear ranking schemes; e.g., identify threats, remediation, and habitats of species of great- ranking by summing multiple metrics) to lessen collinearity est conservation need (SGCN; AFWA 2012). The SGCN are among metrics (Given and Norton 1993). aquatic and terrestrial organisms that are considered rare, The purpose of this study was to develop an adaptable declining, or vulnerable for the purpose of identifying, man- and standardized methodology that is more rapid than the aging, and preventing the listing of the organism under the USFWS process but more data-driven than current SGCN Endangered Species Act of 1973. Species are periodically processes. Specifically, we sought to integrate established pro- added or deleted from the SGCN list via public participation cedures (e.g., multi-metric) and aspects of the USFWS 3Rs and best available information. In a review of SGCN meth- framework in our methodology and to avoid the limitations odologies (Appendix S1 in the online version of this article), (i.e., expert opinion and the use of global species ranking sys- which we compiled from publicly available online SGCN doc- tems) found in many current SGCN processes. As such, we umentation for 50 states and two U.S. territories, public par- developed and assessed a methodology using freshwater fishes ticipation includes periodic stakeholder meetings with natural within three ecoregions of the southwestern USA. Steps in our resource experts (e.g., agency biologists, academia, and non- methodology were as follows: (1) compose a list of all fresh- government organizations). Sources used to identify SGCN water fishes reported within the ecoregions and filter the list varied among SWAPs in terms of detail, extent, and clarity. of fishes based on resident or peripheral status and availabil- Generally, SWAPs used available imperiled species lists (e.g., ity of information for each fish; (2) select a subset of remain- state and federally listed species, 77%); published and un- ing fishes that represent known rare and common species; (3) published data with quantitative and qualitative estimates of identify independent and semi-independent drainages; (4) use

Fisheries | www.fisheries.org 489 multi-metrics and multivariate analysis for measures of spe- occur based on museum records. Representation was defined as cies distributional breadth, commonality, and extirpation (i.e., a species’ ability to endure natural variability (Shaffer and Stein measures of the 3Rs); and (5) rank fishes along a gradient from 2000) and can be characterized by the breadth of genetic diver- least to greatest in redundancy, resiliency, and representation. sity and environmental diversity (Smith et al. 2018). We quanti- We hypothesized that species ranked low in 3Rs would be sim- fied representation using the relative abundance of a species as ilar to the USFWS list, IUCN categories, and local SGCN list, a surrogate for genetic diversity, given that genetic variation is which is representative of the SWAP process used by the ma- positively related to population size and abundant species would jority of states and territories of the USA (i.e., used published be more genetically diverse than rare species (Frankham 1996). and unpublished data; incorporated expert opinion). We also Occurrence (i.e., presence) of a species within a drainage predicted that some less studied species would not be ranked and reach was obtained and confirmed from museum vouch- among the species currently listed by the USFWS, IUCN, and er specimens (i.e., Fishes of Texas Project Database version 2; SGCN. In addition to the ranking developed herein, the com- Hendrickson and Cohen 2015) and published literature (i.e., pilation of species distributions, abundances, and potential Miller et al. 2005; Thomas et al. 2007; Hubbs et al. 2008). An extirpation by drainage provides documented and transparent independent drainage was defined as a drainage (1) lacking a records for rare and common species within a region to stake- contemporary (i.e., since the mid-Holocene) connection with holder committees for use when potential SGCN are identi- another drainage and (2) possessing a coastal or near-coastal fied and the list is revised. terminus with the Gulf of Mexico. The Rio Grande and the Nueces, Colorado, and Brazos rivers have separate coastal METHODS termini with the Gulf of Mexico. The Guadalupe and San Study Area Antonio rivers share a near-coastal terminus, connecting about The methodology was developed using freshwater fish com- 15 km upstream from San Antonio Bay. Within each indepen- munities within three ecoregions of the southwestern USA. dent drainage, semi-independent reaches—defined as reaches We selected these three ecoregions because they are hotspots with generally independent water sources from other reaches— of fish endemism and contain a mix of narrowly distributed were named streams, named tributaries of a stream, or reaches fishes, but also contain a large number of widely distributed of a named stream. Reaches were separated by confluences or fishes (Conner and Suttkus 1986), providing breadth in spe- by dams except for saline and freshwater spring reaches of the cies distributions, abundances, and reported extirpations. The Pecos River, which were separated by a salinity gradient. Species Chihuahuan Desert, Edwards Plateau, and South Texas Plains that were considered extinct or extirpated (N = 6 species) from ecoregions compose 32% of the surface area in Texas (Griffith the study area or with peripheral occurrences (N = 12 species) et al. 2007) and provide aquatic habitats for 70% (N = 7) of within the study area (Conner and Suttkus 1986; Maxwell 2012) the federally listed Texas fishes and 57% N ( = 32) of the Texas were removed from further analyses in order to only quantify SGCN fishes (Figure 1). The Chihuahuan Desert ecoregion fishes with primary occurrences within the study area. We ex- is about 13% of the surface area in Texas and is bounded by cluded an additional 14 species with widespread distributions the state boundary with New Mexico and the USA–Mexico (e.g., Mississippi Silverside Menidia audens, Largemouth Bass international boundary in the west to the Pecos River in Micropterus salmoides, and Green SunfishLepomis cyanellus) the east. Surface water and groundwater flows are within found within the ecoregions because several widespread species the Rio Grande basin and a few endorheic watersheds. The spanning multiple lineages were already included. Edwards Plateau ecoregion is about 11% of the surface area Relative abundance of a species within a reach was ob- in Texas and is bounded by the Pecos River in the west and tained from the most recently available fish community data the Balcones Escarpment in the east. Surface and groundwa- (published and unpublished data; 1988–2017). We retained ter flows are within the Rio Grande, Nueces River, Guadalupe relative abundances provided by the authors as calculated ([N River, San Antonio River, Colorado River, and Brazos River of individuals of a species]/[total N of individuals within the basins. The South Texas Plains ecoregion is about 8% of the fish community] × 100). We accepted reported fish communi- surface area in Texas and is bounded by the Edwards Plateau ty data and corresponding relative abundances as represen- ecoregion in the north, the Rio Grande in the south, and the tative of the reach if a study objective of the published or lower Rio Grande in the east. Surface and groundwater flows unpublished data was to quantify the fish community. Among are within the Rio Grande and Nueces River basins. the 24 data sets used in this study, source materials were from the published literature (57%), student theses (22%), unpub- Data Compilation lished data (17%), and agency reports (4%). Juvenile and We used museum records, published literature, and unpub- adult fish were taken with seines or with seines and electro- lished data to assess aspects of redundancy, resiliency, and rep- fishing; sampling took place in all available habitats within an resentation for fishes within the three ecoregions. Redundancy area using multiple passes or a systematic number of single- was defined as a species’ ability to survive catastrophic events pass seine hauls within an area, and sites were sampled once and can be measured based on the number of locations where or multiple times over a year or more. Differences in sampling a species persists (Shaffer and Stein 2000). We quantified re- designs and collection methodologies often limit estimations dundancy by the number of independent drainages and semi- and comparisons of species relative abundances across mul- independent reaches inhabited by a species. Resiliency was tiple studies conducted by different individuals. For exam- defined as a species’ ability to survive catastrophic events and ple, seines do not capture fish that are small enough to pass can be measured by a species persisting at a location (Shaffer through the mesh or fish that are large enough to outswim and Stein 2000) or by its population size (Smith et al. 2018). We the net (Hayes et al. 1996); therefore, seines have a tendency quantified resiliency by calculating the percent of drainages or to underestimate species occurrence and relative abundance reaches where the species was reported as absent in the most within the community (Bayley and Peterson 2001; Fischer recent sampling event but where it was previously known to and Paukert 2009). In other examples, studies sampling a

490 Fisheries | Vol. 44 • No. 10 • October 2019 Figure 1. Map of the study area in Texas. Light shaded areas represent the Chihuahuan Desert, Edwards Plateau, and South Texas Plains ecoregions. Dark shaded areas represent the hydrologic units of the semi-independent reaches within the study area. site once tend to underestimate species richness for an area Analysis more so than studies sampling a site multiple times over a Species data tables were constructed and consisted of col- year (Labay et al. 2015), and false absences (failure to detect umns that identified occurrences in independent drainages, a species when present; Gu and Swihart 2004; Denes et al. occurrences in semi-independent reaches, relative abundance, 2015) are common sampling problems even when sites are date of the relative abundance estimate, ACFOR category, sampled with multiple gear types over extended sampling absence, and citation for the most recent relative abundance periods. Similar to other published studies (e.g., Perkin and (Appendix S2 online). Species data tables were used to devel- Bonner 2011; Kollaus et al. 2015), we acknowledge potential op a species matrix, with each row representing a species and limitations in comparing relative abundances and community four columns consisting of our measures of redundancy (i.e., data among studies. number of independent drainages in which the species oc- Our data compilation efforts produced a total of 806,976 curred; number of semi-independent reaches in which the spe- fish collected from 54 reaches within the three ecoregions. cies occurred), resiliency (i.e., percentage of semi-independent Mean (±SD) number of fish per reach was 14,944 ± 61,188, reaches in which the species was categorized as absent), and and the median number of fish per reach was 4,082 representation (i.e., percentage of semi-independent reaches (range = 89–453,147). Species identified in published and in which the species was categorized as rare). For the spe- unpublished literature were accepted as reported and revised cies data tables, we added two additional columns for (1) the according to Page et al. (2013), although some species (e.g., number of independent drainages where a species occurred in Guadalupe Bass M. treculii: Bean et al. 2013; Headwater other ecoregions of Texas and (2) whether or not the species Catfish Ictalurus lupus: McClure-Baker et al. 2010; Bean occurred outside of Texas. These two columns were necessary et al. 2011) are known to hybridize with congeners. Species in order to improve our estimate of redundancy outside of relative abundances were sorted into categories using the our study area since some species are found only within the “ACFOR scale”: abundant (>75% in relative abundance), three ecoregions, whereas other species are found in other common (50–74%), frequent (25–49%), occasional (5–24%), ecoregions of Texas, in another state (i.e., New Mexico), or in or rare (>0% to 4%; Kent and Coker 1992; Stiers et al. 2011; another country (i.e., Mexico). Craig et al. 2017). The ACFOR scale was used to categorize The species matrix was assessed with principal compo- quantitative data and provide an interpretation of relative nents analysis (PCA). Species scores from principal compo- abundance data. Zero relative abundance (i.e., potentially ex- nent (PC) axes I and II (PC I and PC II) were weighted by the tirpated) was categorized as “absent” for species previously percentage of variation explained by each axis and then were reported in the stream or reach. Fishes in independent drain- summed together. The products of the PC II score multiplied ages and semi-independent reaches were excluded if museum by the proportion of variation explained were multiplied by vouchers and a collection with relative abundance records −1. Multiplication by −1 was necessary to convert PC I and were not available. PC II gradients into compatible linear contrasts to distinguish

Fisheries | www.fisheries.org 491 species with low redundancy, representation, and resiliency threatened, vulnerable, or endangered, the near-threatened from those with high redundancy, representation, and resil- fishes were within ranks 11–36, vulnerable fishes were with- iency. A single number was associated with each species of in ranks 4–36, and endangered fishes were within ranks 1–20. fish. Species numbers were sorted in ascending order, with the Among the top-10 fish species ranked by our methodology, lowest number representing the fish with collectively the esti- one species was considered endangered, two species were con- mated lowest redundancy, representation, and resiliency and sidered vulnerable, one species was considered data deficient, the highest number representing the fish with collectively the and six species were considered of least concern by IUCN. estimated highest redundancy, representation, and resiliency. Among the 24 fishes listed as Texas SGCN within the study Species by rank were compared to species currently listed by area, 18 Texas SGCN were within ranks 1–20, and all 24 Texas USFWS, SGCN, and IUCN. The Texas SGCN (Texas Parks SGCN were within ranks 1–38 based on our methodology. and Wildlife Department 2012) list was used, although a revised listing is forthcoming. Species categories listed by IUCN DISCUSSION were acquired on July 3, 2017. We expected that species ranked low in the 3Rs would be similar to the USFWS, IUCN, and SGCN listings. In general, RESULTS there was correspondence among the lists and our rankings. In total, 61 species were considered for this analysis. Species that ranked low in the 3Rs were among the species Eleven species (18% of species considered) were excluded listed by USFWS, IUCN, and SGCN. We also anticipated due to a lack of relative abundance data (e.g., Pecos Pupfish and found that some of the species not identified by USFWS, Cyprinodon pecosensis) or a lack of museum and historical re- IUCN, and SGCN were ranked among fishes that were low in cords (e.g., Alligator Gar Atractosteus spatula). Species data the 3Rs (e.g., Tex-Mex Gambusia G. speciosa). Lack of des- tables were constructed for the remaining 50 species (82%). ignation as an imperiled species might be related to several The 50-species data tables represented 12 families of fish and factors, including a lack of specified threats or deficient data consisted of narrowly distributed fishes (i.e., those occurring (i.e., IUCN category for Tex-Mex Gambusia) or a lack of in one drainage) and widely distributed fishes (i.e., those oc- standardization in the designation process (i.e., USFWS from curring in up to six drainages). Species occurred in 1–50 reach- 1967 to 1999; Andelman et al. 2004). Given the correspon- es (Table 1). Thirteen species (26%) occurred only within the dence of this methodology with existing lists as well as the three ecoregions. identification of species low in 3Rs that are not on existing Principal component axes I and II explained 71% of the lists, our methodology met the intended purpose of providing total variation in the species data matrix (Figure 2). Axis I a rapid quantitative assessment and ranking for potentially explained 49% of the total variation and described primarily 82% of the fishes found within the study area based on their a redundancy gradient, contrasting narrowly distributed fish- distribution, commonality, and potential for extirpation. As es found in fewer drainages and reaches (i.e., negative scores) intended, the ranked list provides quantitative information— from widely distributed fishes found in greater numbers of while removing expert opinion limitations in subjectivity, drainages and reaches (i.e., positive scores; Table 2). Species experience level, and knowledge breadth (Clark et al. 2006; with strong positive scores along PC I included the Western Halpern et al. 2007; Donlan et al. 2010) and removing the MosquitofishGambusia affinis, Longear SunfishL. megalotis, limitations of global ranking systems—to assist in the SGCN Bluegill L. macrochirus, and Channel CatfishI. punctatus. identification process. Species with strong negative scores included the Comanche In comparison with the current SGCN list, our top-20 Springs PupfishC. elegans, Clear Creek Gambusia G. heter- ranked fishes are listed as SGCN except for the Tex-Mex ochir, and Fountain Darter Etheostoma fonticola. Axis II ex- Gambusia and Spotfin GambusiaG. krumholzi. Spotfin plained 22% of the total variation and described primarily a Gambusia occurrence in Texas was first reported in 1997 resiliency and representation gradient, contrasting fishes with but was reported as a new species, the San Felipe Gambusia greater percent absence or percent rare (i.e., positive scores) G. clarkhubbsi (Garrett and Edwards 2003). Later, the San from those with fewer percent absences and occasional to abun- Felipe Gambusia was deemed a junior synonym of the Spotfin dant in relative abundance (i.e., negative scores). Species with Gambusia (Echelle et al. 2013). The San Felipe Gambusia is strong positive scores along PC II included the Rio Grande included on the current SGCN list (Texas Parks and Wildlife Shiner Notropis jemezanus, Longnose Dace Rhinichthys cat- Department 2012) and will be replaced with the Spotfin aractae, and Speckled Chub Macrhybopsis aestivalis. Species Gambusia on the revised SGCN list (Texas Parks and Wildlife with strong negative scores included the Fountain Darter, Rio Department, in press). Four of the fishes within the ranks Grande Cichlid Herichthys cyanoguttatus, and Largespring of 21–30 are listed as SGCN. The other six species are now Gambusia G. geiseri. highlighted for additional discussion by a stakeholder group. Weighted summations of species scores for PC I and II were Among the six species, four (i.e., Spotted Gar Lepisosteus sorted from least (i.e., toward low redundancy, representation, oculatus, Orangespotted SunfishL. humilis, Rainwater and resiliency) to greatest (i.e., toward high redundancy, rep- Killifish Lucania parva, and Plains Killifish Fundulus zebri- resentation, and resiliency) and were ranked (Table 3). Final nus) have ubiquitous distributions outside of the study area scores ranged from −1.20 for Comanche Springs Pupfish to (Hendrickson and Cohen 2015). However, two other species 1.74 for Western Mosquitofish. When compared to USFWS (Largespring Gambusia and Texas Logperch Percina car- listed species, IUCN categories, and the current Texas SGCN bonaria) should be assessed for listing as SGCN since both are list, ranks assigned by this study were more similar to the endemic to drainages within Texas. Texas SGCN list than to the USFWS list or IUCN categories. Our methodology also highlighted fishes that were con- Among the six fishes that were listed by USFWS within the sidered SGCN despite having high resiliency, redundancy, study area, all were ranked in the top 20 with our methodolo- and representation. Guadalupe Bass (rank = 32) is listed by gy. Among the 13 fishes that were listed by the IUCN as near SGCN and ranked lower than eight other non-SGCN fishes.

492 Fisheries | Vol. 44 • No. 10 • October 2019 Table 1. The number of drainages and reaches inhabited by each species of fish within the study area (three ecoregions of Texas), the percentage of reaches where each species is categorized as rare or where the species was absent from the most recent collections, the number of independent drainages inhabited by each species in Texas but outside of the study area, and whether the species occurs (denoted with 1) or not (denoted with a 0) outside of Texas. Percentage of Percentage of Independent Found extant reaches total reaches drainages in outside of Species Drainages Reaches where rare where absent Texas Texas Spotted Gar Lepisosteus oculatus 4 13 100 54 3 1 Gizzard Shad Dorosoma cepedianum 6 24 100 54 4 1 Central Stoneroller Campostoma anomalum 6 38 72 16 3 1 Mexican Stoneroller Campostoma ornatum 1 4 0 50 0 1 Plateau Shiner Cyprinella lepida 2 5 100 20 0 0 Red Shiner Cyprinella lutrensis 6 40 38 40 4 1 Proserpine Shiner Cyprinella proserpina 1 10 20 50 0 0 Blacktail Shiner Cyprinella venusta 6 41 25 12 3 1 Manantial Roundnose Minnow Dionda argentosa 1 9 0 33 0 0 Devils River Minnow Dionda diaboli 1 4 67 25 0 1 Roundnose Minnow Dionda episcopa 1 7 100 71 0 1 Guadalupe Roundnose Minnow Dionda nigrotaeniata 3 19 86 26 0 0 Nueces Roundnose Minnow Dionda serena 1 5 25 20 0 0 Speckled Chub Macrhybopsis aestivalis 1 8 100 75 0 1 Texas Shiner Notropis amabilis 6 34 34 15 0 1 Tamaulipas Shiner Notropis braytoni 1 10 60 50 0 1 Ironcolor Shiner Notropis chalybaeus 1 1 100 0 2 1 Chihuahua Shiner Notropis chihuahua 1 3 100 33 0 1 Rio Grande Shiner Notropis jemezanus 1 7 100 86 0 1 Sand Shiner Notropis stramineus 5 25 82 56 2 1 Bullhead Minnow Pimephales vigilax 6 35 76 51 4 1 Longnose Dace Rhinichthys cataractae 1 5 100 80 0 1 River Carpsucker Carpiodes carpio 5 25 100 48 4 1 Gray Redhorse Moxostoma congestum 6 35 100 46 0 1 Mexican Tetra Astyanax mexicanus 6 36 73 28 2 1 Yellow Bullhead Ameiurus natalis 6 22 100 55 3 1 Headwater CatfishIctalurus lupus 3 16 100 56 0 1 Channel CatfishIctalurus punctatus 6 41 100 27 4 1 Plains KillifishFundulus zebrinus 2 12 67 50 2 1 Rainwater KillifishLucania parva 3 7 80 29 0 1 Western MosquitofishGambusia affinis 6 50 49 14 4 1 Largespring Gambusia Gambusia geiseri 3 10 25 20 0 0 Clear Creek Gambusia Gambusia heterochir 1 2 0 50 0 0 Spotfin GambusiaGambusia krumholzi 1 1 100 0 0 0 Pecos Gambusia Gambusia nobilis 1 4 0 25 0 1 Tex-Mex Gambusia Gambusia speciosa 1 4 0 50 0 1 Leon Springs PupfishCyprinodon bovinus 1 1 100 0 0 0 Comanche Springs PupfishCyprinodon elegans 1 3 0 67 0 0 Orangespotted SunfishLepomis humilis 3 12 100 75 3 1 Bluegill Lepomis macrochirus 6 40 86 8 4 1 Longear SunfishLepomis megalotis 6 45 84 4 4 1 Redspotted SunfishLepomis miniatus 5 18 100 56 3 1 Guadalupe Bass Micropterus treculii 5 21 100 19 0 0 Fountain Darter Etheostoma fonticola 1 2 0 0 0 0 Rio Grande Darter Etheostoma grahami 1 7 83 14 0 1 (Continues)

Fisheries | www.fisheries.org 493 Table 1. (Continued)

Percentage of Percentage of Independent Found extant reaches total reaches drainages in outside of Species Drainages Reaches where rare where absent Texas Texas Greenthroat Darter Etheostoma lepidum 4 26 85 23 2 1 Orangethroat Darter Etheostoma spectabile 4 18 80 44 2 1 Guadalupe Darter Percina apristis 1 4 100 50 0 0 Texas Logperch Percina carbonaria 5 21 92 43 1 0 Rio Grande Cichlid Herichthys cyanoguttatus 6 30 96 10 1 1

Figure 2. Fishes (first three letters of genus and specific epithets provided; codes defined in Table 3) distributed along principal component axes I and II (PC I and PC II), representing species with wide distributions (i.e., positive along PC I) and narrow distributions (negative on PC I) and species with numerous reach extirpations (positive on PC II) and few reach extirpations (negative on PC II). Some fish names are jittered to allow readability.

Factors that influenced listing of the Guadalupe Bass as an of known and potential threats to the species ranking can jus- SGCN include the quantified threat of introgression with the tify the listing of a species as an SGCN with a lower rank introduced Smallmouth Bass M. dolomieu (Bean et al. 2013). than other non-SGCN. The Texas Shiner Notropis amabilis Thus, the Guadalupe Bass is an example of how the addition (rank = 38) has greater than average redundancy and representation. Its endemic status was the primary factor in listing it as an SGCN. However, recent work by Craig et al. (2017) Table 2. Results for the principal components analysis (PCA) used to create the rankings from the data matrix. Values represent loadings indicated higher redundancy and representation and therefore along principal component axes I and II (PC I and PC II) for variables suggested the Texas Shiner’s deletion from the forthcoming used in the PCA. SGCN list. Quantified measures of redundancy, representa- Variable PC I PC II tion, and resiliency for the Texas Shiner now have context to support its removal from the SGCN list, given that measures Drainages 0.54 −0.17 of the 3Rs are provided for other fishes within the region. Reaches 0.53 −0.21 Our methodology was not applicable to 18% of the Drainages outside of the study 0.52 0.02 fishes within the study area due to a lack of verifiable mu- area seum records or a lack of relative abundance data. Lack of Found outside of Texas 0.33 0.49 information is common in assessment and ranking efforts Percent rare 0.22 0.38 (O’Grady et al. 2004; McGeoch et al. 2012), with Hudy et al. (2008) reporting incomplete data in 33% of their study area Percent absent −0.06 0.73 when assessing Brook Trout Salvelinus fontinalis populations Total variance explained 0.4905 0.2243 by watersheds. As such, our inability to assess 18% of the

494 Fisheries | Vol. 44 • No. 10 • October 2019 Table 3. Names, codes for genus and specific epithets (used in Figure 2), final scores, and rankings of fishes. Ranking scale contrasts species with low redundancy, resiliency, and representation (i.e., rank 1) and species with high redundancy, resiliency, and representation (i.e., rank 50). Letter “X” under USFWS denotes species that are listed by the U.S. Fish and Wildlife Service as threatened or endangered. International Union for Conservation of Nature (IUCN) classifications are as follows: endangered (EN), vulnerable (VU), near threatened (NT), least concern (LC), data deficient (DD), and not evaluated (NE). Letter “X” under SGCN denotes species listed as Texas species of greatest conservation need. Final Species Code score Rank USFWS IUCN SGCN Comanche Springs PupfishCyprinodon elegans Cyp ele −1.20 1 X EN X Rio Grande Shiner Notropis jemezanus Not jem −1.10 2 LC X Longnose Dace Rhinichthys cataractae Rhi cat −1.09 3 LC X Clear Creek Gambusia Gambusia heterochir Gam het −1.07 4 X VU X Speckled Chub Macrhybopsis aestivalis Mac aes −0.98 5 LC X Roundnose Minnow Dionda episcopa Dio epi −0.97 6 LC X Guadalupe Darter Percina apristis Per apr −0.97 7 LC X Mexican Stoneroller Campostoma ornatum Cam orn −0.92 8 LC X Tex-Mex Gambusia Gambusia speciosa Gam spe −0.92 9 DD Proserpine Shiner Cyprinella proserpina Cyp pro −0.89 10 VU X Manantial Roundnose Minnow Dionda argentosa Dio arg −0.77 11 NT X Tamaulipas Shiner Notropis braytoni Not bra −0.75 12 NE X Nueces Roundnose Minnow Dionda serena Dio ser −0.73 13 LC X Chihuahua Shiner Notropis chihuahua Not chi −0.73 14 NE X Pecos Gambusia Gambusia nobilis Gam nob −0.70 15 EN X Devils River Minnow Dionda diaboli Dio dia −0.66 16 X EN X Fountain Darter Etheostoma fonticola Eth fon −0.64 17 X EN X Spotfin GambusiaGambusia krumholzi Gam kru −0.60 18 VU Leon Springs PupfishCyprinodon bovinus Cyp bov −0.60 19 X VU X Plateau Shiner Cyprinella lepida Cyp lep −0.55 20 EN X Rio Grande Darter Etheostoma grahami Eth gra −0.49 21 VU X Headwater CatfishIctalurus lupus Ict lup −0.37 22 DD X Largespring Gambusia Gambusia geiseri Gam gei −0.35 23 LC Rainwater KillifishLucania parva Luc par −0.35 24 LC Plains KillifishFundulus zebrinus Fun zeb −0.25 25 LC Ironcolor Shiner Notropis chalybaeus Not cha −0.18 26 LC X Guadalupe Roundnose Minnow Dionda nigrotaeniata Dio nig −0.17 27 LC X Orangespotted SunfishLepomis humilis Lep hum −0.15 28 LC Texas Logperch Percina carbonaria Per car 0.17 29 LC Spotted Gar Lepisosteus oculatus Lep ocu 0.19 30 NE Orangethroat Darter Etheostoma spectabile Eth spe 0.21 31 LC Guadalupe Bass Micropterus treculii Mic tre 0.22 32 NT X Sand Shiner Notropis stramineus Not str 0.40 33 LC Redspotted SunfishLepomis miniatus Lep min 0.42 34 LC Gray Redhorse Moxostoma congestum Mox con 0.54 35 LC Greenthroat Darter Etheostoma lepidum Eth lep 0.57 36 NT Yellow Bullhead Ameiurus natalis Ame nat 0.65 37 LC Texas Shiner Notropis amabilis Not ama 0.75 38 LC X Rio Grande Cichlid Herichthys cyanoguttatus Her cya 0.79 39 LC River Carpsucker Carpiodes carpio Car car 0.79 40 LC Gizzard Shad Dorosoma cepedianum Dor cep 0.86 41 LC Mexican Tetra Astyanax mexicanus Ast mex 1.01 42 LC Bullhead Minnow Pimephales vigilax Pim vig 1.11 43 LC Red Shiner Cyprinella lutrensis Cyp lut 1.29 44 LC Central Stoneroller Campostoma anomalum Cam ano 1.32 45 LC (Continues)

Fisheries | www.fisheries.org 495 Table 3. (Continued)

Final Species Code score Rank USFWS IUCN SGCN Blacktail Shiner Cyprinella venusta Cyp ven 1.39 46 LC Channel CatfishIctalurus punctatus Ict pun 1.46 47 LC Bluegill Lepomis macrochirus Lep mac 1.59 48 LC Longear SunfishLepomis megalotis Lep meg 1.73 49 LC Western MosquitofishGambusia affinis Gam aff 1.74 50 LC

species should not overly limit the use of the methodology. ACKNOWLEDGMENTS Nevertheless, the methodology highlighted gaps in knowledge Funding was provided by the Department of Biology at for 18% of the fishes within the study area, which can be used Texas State University. We thank M. Huertas and M. C. Green to prioritize these species for future research. In addition to (Texas State University) for comments on earlier versions of limits on species applicability, another limitation of this meth- the manuscript. There is no conflict of interest declared in this odology is the need for species relative abundance data at in- article. dependent and semi-independent reaches. We relied primarily on local sources (i.e., university research and state agency re- REFERENCES ports) to gather relative abundance data. In the absence of lo- AFWA (Association of Fish and Wildlife Agencies). 2012. 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