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A reexamination of Syngnathus affinis Gunter 1870, with comparisons to Syngnathus scovelli (Evermann and Kendall 1896) (teleostei: Syngnathidae).

The Texas pipefish (Syngnathus affinis) is currently known from only a small number of specimens collected from geographically isolated locations in the vicinity of Corpus Christi Bay, Texas. The general rarity of this species, coupled with the fact that no new collections have been recorded in over 30 years, has led numerous researchers to postulate that this taxon represents a marine species that has become extinct. To determine the status of S. affinis, a reexamination of all known collections was undertaken and these were compared to recent collections of S. scovelli, a common syngnathid ranging throughout the Gulf of Mexico. Multivariate statistical techniques were used to compare the morphometric and meristic characters currently used to differentiate syngnathids. Analysis of Similarity revealed that a low degree of separation exists between meristic characters of the two species, and an even lower degree of separation was found with the morphological values. Based on the results of this study, the taxonomic validity of the nominal designation S. affinis is questioned. Previous records of S. affinis most likely represent misidentified specimens of S. scovelli.

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Considerable confusion surrounds the status of the Texas pipefish, Syngnathus affinis Gunther 1870. This nominal species is based on a single specimen (Lot 233) purchased at Steven's sales room (London) and registered simply as "Louisiana" and the questionable nature of the type-locality was indicated by Gunther's failure to discuss the source of the holotype (Dawson 1982). Nearly all occurrences of this species have come from the Corpus Christi Bay area of Texas, with only one other subsequent collection from Louisiana (five specimens from Prien Lake; Fowler 1933). A total of 36 specimens have reported since 1926, with 20 of the 30 Corpus Christi Bay specimens taken with S. louisianae and S. scovelli in two seine collections at Fish Pass (Dawson 1982). A single specimen collected in 1970 (but subsequently lost) constitutes the collection from the Laguna de Terminos area (Dawson 1982).

Early accounts of short-snouted pipefishes (snout length-to-head length ratios of 0.400 to 0.588) of the genus Syngnathus from the western Gulf of Mexico originally included only S. fuscus and S. scovelli (see Evermann & Kendall 1894:109 as Siphostoma fuscus; Breder 1929; Jordan et al. 1930; Herald 1942; Hoese 1958). These two species were separated primarily by the total number of trunk rings (19-21, rarely 18 in S. fuscus; 15-18, rarely 19 in S. scovelli) and dorsal fin rays (35-43 in S. fuscus; 27-35 in S. scovelli). Based on a reexamination of the holotype, Herald (1965) was the first to adopt the subspecies designation of S. fuscus affinis (Relict Northern Pipefish), although it was originally postulated that the holotype was a specimen of S. fuscus from an erroneous locality. Later, Hoese & Moore (1977) recognized S. fuscus affinis as a subspecies of S. fuscus known only from Corpus Christi Bay. Syngnathus fuscus fuscus is distributed along the Atlantic coast from Gulf of St. Lawrence in Canada southwards to northern Florida (Lazzari & Able 1990). Dawson (1982) dropped the subspecies designation, using the combination of trunk rings (modally 18), tail rings (33-34), and dorsal fin ray counts (37-41) to separate S. affinis from S. fuscus. Other characters presented by Dawson (1982) for distinguishing S. affinis from other western Atlantic congeners include moderate snout length (averages 0.42 snout-to-head length ratio) and depth (averages 0.33 snout depth-to-length ratio) in addition to a narrower preorbital bone. By contrast, Hubbs et al. (1994) incorporated all previous Gulf of Mexico specimens of S. fuscus as S. affinis. This practice was followed by McEachran & Fechhelm (1998), thereby eliminating the Gulf of Mexico from the distributional range of S. fuscus.

In order to resolve some of the confusion surrounding the identity and status of S. affinis, a reexamination of all known collections of this species was conducted and these were compared to recent collections of S. scovelli from the Corpus Christi Bay area. In this paper, the species status of S. affinis is questioned based on a multivariate analysis of the meristic and morphological characters currently used to identify pipefishes.

MATERIALS AND METHODS

Collections of Syngnathus affinis were obtained from museums (Academy of Natural Sciences [ANSP], British Museum of Natural History [BMNH], California Academy of Science [CAS], Field Museum of Natural History [FMNH], Gulf Coast Research Laboratory [GCRL], Texas A&I University [TAIC], Texas A&M University [TCWC], Texas Memorial Museum [TNHC], National Museum of Natural History [USNM], and Yale University [YPM]). Collections of S. scovelli were made by the author from every location in the Corpus Christi Bay area where S. affinis were previously recorded (Fig. 1). Each specimen was examined using the characteristics outlined in Dawson (1982), with the following measurements taken with dial calipers under a stereo-microscope (10X): head length, snout length, snout depth, trunk depth, anal depth, pectoral fin length, and dorsal fin base length. Measurements were taken to the nearest 0.1 mm and expressed as a percentage of head length. Meristic counts included: trunk rings, tail rings, dorsal fin rays, dorsal fin rings (subdorsal rings) over the trunk, subdorsal rings over the tail, and total dorsal fin rings.

Multivariate statistical techniques were used to compare the similarity of the meristic and morphological characters among the samples (i.e., individual pipefish specimens). Analyses were performed using Primer-E (Version 6.0) software (Clarke & Warwick 2001). Samples were standardized to account for scale differences in measurement units. A matrix of Euclidean distance similarities between samples was created. Significant differences in rank similarities between groups of samples were tested by Analysis of Similarity (ANOSIM). In the ANOSIM procedure, the probability of a priori groupings of samples is estimated by repeated permutations of the data (i.e., repeated random relabelling of samples in the matrix). Values of the R statistic can range from -1 to 1, although R will usually fall between 0 and 1 with R values > 0.4 indicating higher degrees of discrimination between groups. Similarities between the samples are graphically represented with non-metric multidimensional scaling (MDS) ordinations (Kruskal 1964). Although outcomes of the ANOSIM are not dependant on MDS ordinations, the ordinations are presented here as they are a helpful way of visualizing patterns in the data. Stress values indicate how well the two-dimensional plot represents relationships among samples in the multidimensional space. Stress values < 0.15 indicate a good fit. MDS ordinations may be arbitrarily rotated so axes are not labeled.

Material examined.-Syngnathus affinis (N = 106). Numbers in parenthesis are number of specimens followed by size range; measurements are in mm SL. "Louisiana", BMNH 1854.7.3.2 (holotype)(1, 144); Texas, Corpus Christi Bay and vicinity: CAS 39674 (1, 80); FMNH 40309 (2, 206, 218); GCRL 15252 (10,55-123); TAIC 3807 (as S. fuscus 1,123); TAIC 5307 (as S. fuscus 72, 65-148); TNHC 27813 (9,78-93); TNHC 28102 (as S. fuscus 1, 91); USNM 132675 (2, 117-174); Galveston Bay, TCWC 11633.01 (1,109); Florida, Egmont Key, YPM 8724 (1, 89); Louisiana, Prien Lake, ANSP 55455 (5,95-102).

Syngnathus scovelli (N = 170), uncataloged. Texas, Corpus Christi Bay and vicinity: Corpus Christi Bay (16, 74-118); Fish Pass (18, 72-120); Upper Laguna Madre (9, 75-105), Baffin Bay (17, 60-86); Aransas Bay (2, 61-85); Redfish Bay (3, 57-113).

RESULTS

A total of 170 pipefish were collected by the author between June 2005 and November 2005 from the Corpus Christi Bay area. Field identifications resulted in the collection of 148 S. scovelli and 22 S. louisianae. Other collections provided by the Texas Parks and Wildlife Department (TPWD) Coastal Fisheries' systematic bag seine sampling efforts in Upper Laguna Madre, Corpus Christi, and Aransas bays during this same time period resulted in an additional 19 S. scovelli and 3 S. louisianae specimens. No new specimens of S. affinis were collected during this study. Individuals of S. scovelli (n = 65) were randomly selected from this collection and used in the multivariate comparisons.

ANOSIM results of the meristic characters (Table 1) revealed a relatively low degree of separation of the a priori designations (R = 0.363, P < 0.001). MDS configuration of the meristic characters is shown in Fig. 2. The most cohesive group of S. affinis samples fell on the left side of the MDS, with the majority of these samples constituting the Fish Pass (GCRL 15252) and the Upper Laguna Madre (TAIA 5307) collections. The remainder of the S. affinis collections from other Texas bays, as well as the Louisiana (ANSP 55455) and Florida (YPM 8724) specimens were scattered throughout the ordination among the S. scovelli collections. Based on the meristic information, the holotype was located in the middle of the variability exhibited by the S. affinis collections. Proportional morphological measurements between the groups were less distinct, as shown in Fig. 3. While statistically significant (R = 0.123; P < 0.001), the morphologically-based R value between S. affinis and S. scovelli is negligibly small. The test reveals that the two 'species' probably do not have exactly the same proportional characteristics (the null hypothesis R = 0 can be rejected) and that these measurements are strongly overlapping and differ somewhat (R is closer to zero). Unlike the meristic characters, ordination of the morphological information failed to detect any cohesive groupings of the S. affinis samples. The holotype was again located within the range of variability encompassed by S. affinis.
Table 1. Counts and proportional measurements of the holotype and non-
type specimens of Syngnathus affinis Gunter 1870 with comparisons to S,
scovelli. Morphometric characters expressed in percent of head length,
except for SL in mm and snout depth-to-length ratio.

 Holotype Non-type Specimens
Character (BMNH 1854.7.3.2) S. affinis (n = 50)

 Range Mean SD

Morphometric
 Standard Length 144 64-218 -- --
 Head length 17.8 8.4-23.2 -- --
 Snout length 0.42 0.37-0.52 0.42 0.04
 Snout depth 0.18 0.13-0.24 0.19 0.03
 Snout depth-to-length 0.43 0.28-0.61 0.46 0.08
 Trunk depth 0.28 0.23-0.38 0.31 0.03
 Anal depth 0.24 0.19-0.38 0.27 0.04
 Pectoral length 0.14 0.14-0.30 0.21 0.03
 Dorsal base length 1.05 0.86-1.44 1.11 0.12

Meristic
 Trunk rings 18 16-19 17.5 0.97
 Tail rings 33 31-36 33.7 1.45
 Total rings 51 47-55 51.1 2.28
 Subdorsal trunk rings 5.75 3.00-5.50 4.30 0.60
 Subdorsal tail rings 3.50 4.00-5.75 4.81 0.49
 Total subdorsal rings 9.25 7.50-10.5 9.11 0.83
 Dorsal fin rays 35 31-40 36.0 2.63

 Corpus Christi Bay Area
Character S. scovelli (n = 65)

 Range Mean SD

Morphometric
 Standard Length 57-120 -- --
 Head length 7.2-15.0 -- --
 Snout length 0.37-0.47 0.42 0.02
 Snout depth 0.13-0.22 0.18 0.02
 Snout depth-to-length 0.32-0.56 0.42 0.06
 Trunk depth 0.22-0.37 0.31 0.03
 Anal depth 0.20-0.35 0.27 0.03
 Pectoral length 0.15-0.26 0.20 0.03
 Dorsal base length 0.89-1.18 1.04 0.07

Meristic
 Trunk rings 15-17 16.0 0.43
 Tail rings 31-34 32.2 0.81
 Total rings 46-50 48.2 0.94
 Subdorsal trunk rings 2.25-4.50 3.72 0.55
 Subdorsal tail rings 3.50-5.75 4.54 0.55
 Total subdorsal rings 7.00-9.25 8.27 0.45
 Dorsal fin rays 30-36 32.5 1.59


DISCUSSION

Little or no literature is available describing the specific characteristics, physiology, or habitat requirements of S. affinis. Presumably, S. affinis shares similar habitat (shallow, nearshore submerged aquatic vegetation) and food requirements as S. scovelli (Joseph 1957; Huh & Kitting 1985; Bolland & Boettcher 2005). Because few specimens have been reported since 1977, this species is currently described as among the rarest in the Gulf of Mexico and it is presumed to be extinct (Roberts & Hawkins 1999). Reasons for disappearance include habitat decline and degradation, caused by human-influenced fishing, shrimping, and dredging activities (Roberts & Hawkins 1999; Musick et al. 2000). While seagrass decline is cited as a specific reason for this demise, seagrass beds in the vicinity of Corpus Christi Fish Pass (the area of highest concentrations of S. affinis to date) have increased dramatically between 1974 and 1994 (Pulich & White 1997). Similar declines in populations of S. scovelli from comparable locations around the Corpus Christi Bay area have not been noted (bag seine collections 1982-2005; TPWD Coastal Fisheries database, Austin, Texas). While not currently listed as threatened or endangered by the National Marine Fisheries Service, the American Fisheries Society recommends listing the Distinct Population Segments of S. affinis as 'endangered' because of their "general overall rarity, endemic nature, and restricted geographic range" (Musick et al. 2000).

Extensive sampling of the known localities around the Corpus Christi Bay area where S. affinis had previously been reported was unsuccessful. In the limited time frame used for this study, a total of 192 pipefishes were collected from nearshore habitats. Syngnathus scovelli made up the majority of these collections, revealing that this species is indeed the dominant syngnathid found in coastal regions of the Gulf of Mexico (Bolland & Boettcher 2005). Admittedly, the field sampling used in this study was limited in scope, concentrating primarily on the immediate vicinities of known locals of S. affinis populations.

A spatially larger scope of sampling within the shallow, nearshore habitats is performed by TPWD, which conducts systematic bag seine sampling in each bay system along the Texas coast as a fishery-independent measure used to track the relative abundance and sizes of finfish (Martinez-Andrade et al. 2005). Since 1975, approximately 37,500 bag seine samples in shallow, nearshore habitats along the Texas coast have produced over 3,600 S. scovelli (TPWD Coastal Fisheries database, Austin, Texas). By stark contrast, no S. affinis have been recorded during these 30 years of sampling. This systematic monitoring of nearshore habitats has revealed that the highest densities of S. scovelli are found in Coastal Bend region of Texas (San Antonio, Aransas, Corpus Christi, and Upper Laguna Madre bay systems; see Fig. 1), and these areas of abundant populations of S. scovelli are generally the same areas that were sampled extensively for this study. Given the general overlap in the meristic characters between S. affinis and S. scovelli as outlined in this paper, it is quite possible that field identifications of S. scovelli by TWPD staff could have erroneously included at least some S. affinis in the thousands of individuals reported. Previous taxonomic keys (Parker et al. 1972; Hoese & Moore 1977; Murdy 1983) recognized S. fuscus as the only other short-snouted pipefish in the genus Syngnathus from Texas waters, yet S. fuscus was similarly absent from TPWD surveys during the 1975-2005 period. Again, misidentifications could account for this apparent absence of S. fuscus from TPWD surveys of the Texas coast.

[FIGURE 1 OMITTED]

With no recent collections of S. affinis available for investigation, investigations of its specific status rest on existing museum specimens. This study did locate additional museum specimens (n = 74) of S. affinis not listed in Dawson (1982), and these were included in the present analysis. These new records call into question the limited distributional range of S. affinis, with this 'species' now recorded from around the northern Gulf of Mexico (1 from near Galveston Bay in Texas; 72 from the Upper Laguna Madre in Texas, and 1 from Egmont Key in Florida). This new range is fully encompassed by the known range of S. scovelli (Dawson 1982).

The ANOSIM tests used for this study revealed that for the meristic information, a relatively low degree of separation was found between S. affinis and S. scovelli (Table 1). Early works describing S. affinis were primarily based on meristic differences found in the short-snouted pipefishes from the western Gulf of Mexico (Herald 1965; Parker et al. 1972), yet those works recognized that only a few individuals had ever been collected. The present analysis also found differences in the mean numbers of dorsal fin rays, trunk rings and tail rings, as well as trunk and tail subdorsal rings, although the ranges of these counts always overlapped, in some cases greatly, between the two nominal taxa. While the meristic-based ANOSIM was significant, this low of an R value is indicative of a high degree of overlap in the a priori groupings. This can happen when the number of replicates is large for the groups, thus giving a very large number of possible permutations. Biologically trivial differences can still be statistically significant when power is large. More importantly, the ANOSIM procedure based on the morphometric values failed to detect any consistent pattern of differences between the two forms. While the stress value calculated for the morphometric data was larger than the meristic configuration (0.12 vs. 0.06, see Fig. 2), the ordination of the morphological information still provides a potentially useful 2-dimensional picture (below the 0.15 level, see Clarke & Warwick 2001). Scaled as a function of head length, average ratios of snout depth, pectoral fin length, and dorsal fin base length were higher in S. affinis, whereas snout length, trunk depth, and anal depth were equivalent with S. scovelli. Each of these characters used in this analysis varied between the two forms by no more than, at most, the standard deviation of the average ratios. This lack of divergence can clearly be seen in the MDS ordination (Fig. 3).

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Given the plasticity of meristic characters within western Atlantic species of Syngnathus (e.g., tail rings ranging from 28 - 34 in S. scovelli and 32-35 in S. affinis; dorsal fin rays ranging from 25 - 37 in S. scovelli and 35 - 41 in S. affinis; see Tables XL, XLI, XLII, and XLIII in Dawson 1982), the variability and gradients of these traits suggests that all the material examined for this study represent different phenotypes of S. scovelli. Individuals currently identified as S. affinis, on the basis of higher counts of trunk rings, tail rings, and dorsal fins rays, most likely represent individuals at the upper limits of these features currently seen in western Gulf of Mexico populations of S. scovelli. Based on the multivariate techniques used for this study, there appears to be little justification for recognizing S. affinis and S. scovelli as distinct species as the former is shown herein to be indistinct from the latter.

Before invalidating S. affinis as a nominal taxon, extensive field work must be conducted in the western Gulf of Mexico to document that there is indeed only a single specimen of short-snouted Syngnathus within the area. These collections should undoubtedly encompass a much greater temporal scale than the six months used for this study. Given the uncertainty in the type locality for S. affinis, "Louisiana" is certainly within the geographic range of S. scovelli. Morphometric and meristic characters of the holotype of S. affinis all lay within the range of variation found in S. scovelli. If invalidation of S. affinis ultimately proves to be the proper action, the Principle of Priority (International Commission of Zoological Nomenclature (ICZN) 2000) states that the valid name of any taxa be the oldest available name applied to it (in this case, S. affinis is senior to S. scovelli). While S. affinis is senior, the Principle of Priority further states that it is not intended to be used to upset a long-accepted name in its accustomed meaning by the introduction of a name that is its senior synonym or homonym (ICZN 2000: Article 23.2). Therefore, if further research corroborates the present hypothesis of invalidating S. affinis, all short-snouted pipefishes from the western Gulf of Mexico should be referred to as S. scovelli.

ACKNOWLEDGEMENTS

I would like to thank the staffs of each museum for allowing me permission to examine specimens in their care and for their prompt response to inquires and loan requests for the few existing collections of the Texas pipefish. Patrick Campbell (BMNH) provided the morphometric data from the holotype. This project was never explicitly funded by research grants, but I gratefully acknowledge the continued support of Sportfish Restoration Funds, without which the time for data synthesis and interpretation would not have been possible. I would like to dedicate this paper to the memory of B. A. Thompson, Coastal Fisheries Institute, Louisiana State University, with whom my initial conversations about the origins of the Texas pipefish and the Prien Lake collections provided the original impetus for this work.

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Musick, J.A., M.M. Harbin, S.A. Berkeley, G.H. Burgess, A.M. Eklund, L. Findley, R.G. Gilmore, J.T. Golden, D.S. Ha, G.R. Huntsman, J.C. McGovern, S.J. Parker, S.G. Poss, E. Sala, T.W. Schmidt, G.R. Sedberry, H. Weeks, & S.G. Wright. 2000. Marine, Estuarine, and Diadromous Fish Stocks at Risk of Extinction in North America (Exclusive of Pacific Salmonids). Fisheries, 25(11):6-30.

Parker, J.C. (ed.), B.J. Galloway, & D. Moore. 1972. Key to the Estuarine and Marine Fishes of Texas. Texas A&M University, 177 pp.

Pulich, W., Jr. & W.A. White. 1997. Current status and historical trends of seagrass in the Corpus Christi Bay National Estuary Program area. Corpus Christi Bay National Estuary Program Publication No. 20. Texas Natural Resource Conservation Commission, Austin, Texas, 131 pp.

Roberts, C.M., J.P. Hawkins, N. Chapman, V. Clarke, A.V. Morris, R. Miller, & A. Richards. 1998. The threatened status of marine species. A Report to the World Conservation Union (IUCN), Species Survival Commission, and Center for Marine Conservation, Washington, D.C, 10 pp.

Roberts, C.M. & J.P. Hawkins. 1999. Extinction risk in the sea. Trends Ecol. Evol., 14(6):241-246.

JT at: James.Tolan@tpwd.state.tx.us

James Tolan

Texas Parks and Wildlife Department, Coastal Fisheries 6300 Ocean Dr., NRC 2501, Corpus Christi, Texas 78412
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