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Feeding ecology of nonnative, inland Fundulus grandis in the Lower Pecos River.

Nonnative Gulf killifish, Fundulus grandis, have been observed in the Pecos River in Texas since the late 1970s (Hillis et al., 1980; Linam and Kleinsasser, 1996; Cheek and Taylor, 2015). They were likely introduced via bait-bucket releases (Hillis et al., 1980). Other inland, nonnative populations of this species have been recorded in the upper Rio Grande and the Brazos River in Texas (Hillis et al., 1980; Hubbs et al., 2008). In the Lower Pecos River below Red Bluff Dam and above Independence Creek, fish assemblage structure is constrained by very high salinity, a result of natural saline inputs exacerbated by cumulative impacts of flow alteration (Hoagstrom, 2009). In this portion of the main-stem Pecos, fish diversity has declined substantially, and assemblages contain only a few tolerant, euryhaline species (Cheek and Taylor, 2015). Fundulus grandis is one of the most abundant species in these reaches according to recent surveys (Cheek and Taylor, 2015; East, 2015). Interactions with native species have not been studied, but Cheek and Taylor (2015) documented declining abundance of native Fundulus zebrinus in the Lower Pecos in a comparison with surveys in 1987 (Linam and Kleinsasser, 1996) and suggested that the decline might be due in part to competition for resources with F. grandis.

In native coastal ecosystems along the Atlantic and the Gulf of Mexico, F. grandis occur in marshes, sea grass beds, and lower reaches of rivers with salinities ranging from fresh to hypersaline (Crego and Peterson, 1997). In these habitats, F. grandis consume a wide variety of prey items, including aquatic and terrestrial arthropods, mollusks, small fishes, plant material, and algae (Harrington and Harrington, 1961; Rozas and LaSalle, 1990; Ley et al., 1994). The ecology of F. grandis in systems outside their native range is poorly understood. Nonnative, inland populations of F. grandis might be ecologically distinct from those in estuarine ecosystems because of differences in habitat characteristics, resource availability, and interactions with other species. Information on feeding ecology is needed to better understand potential ecological effects of this species in inland ecosystems. Because nonnative piscivores are known to have severe negative impacts on native fishes in the southwestern United States (e.g., Meffe, 1985; Marsh and Douglas, 1997), an examination of the extent of piscivory by F. grandis outside their native range is also important for assessing potential impacts. Thus, our objectives were to examine dietary resource use of F. grandis in the Pecos River with gut contents analysis and to carry out a preliminary investigation of fish consumption rates with timed laboratory feeding trials.

We surveyed fish assemblages at 12 sites in the main stem of the Pecos River (U.S. 84 crossing near Santa Rosa, New Mexico; Bitter Lake National Wildlife Refuge, New Mexico; U.S. 82 crossing near Artesia, New Mexico; C.R. 745 crossing near Malaga, New Mexico; F.M. 652 crossing near Orla, Texas; F.M. 1776 crossing near Coyanosa, Texas; F.M. 1053 crossing near Imperial, Texas; U.S. 385 crossing near Girvin, Texas; S.H. 349 crossing near Iraan, Texas; I-10 crossing near Sheffield, Texas; below confluence with Independence Creek at Independence Creek Preserve, Texas; and F.M. 2083 crossing near Pandale, Texas). We collected fishes using seines (6.1 x 1.8 m, 4.8 mm mesh) in June 2013. We surveyed sites at Bitter Lake National Wildlife Refuge, Artesia, Orla, Iraan, and Independence Creek Preserve a second time in September 2013. We carried out a minimum of five 5-m seine hauls, with more performed as needed until we captured no new species, during each sampling event. At sites where F. grandis were collected, we euthanized adult specimens and preserved them for gut contents analysis. In the laboratory, we removed stomach contents, identified them, and measured them for length and volume. Where possible, we identified consumed fishes to species and identified invertebrates to order. Because Cyprinodon variegatus have hybridized extensively with Cyprinodon pecosensis in the Lower Pecos main stem (Echelle and Conner, 1989; Wilde and Echelle, 1992), and we were unable to distinguish between hybrids and pure C. variegatus, we classified pupfish consumed by F. grandis collected below Loving, New Mexico as Cyprinodon species. We grouped prey items into the following broad categories before analyses: fishes and fish parts, gastropods, crustaceans, aquatic insects, terrestrial insects, algae, and detritus/sediment. We calculated percent frequency of occurrence as the percentage of F. grandis stomachs containing one or more individuals of each prey category. We calculated volumetric proportions of each prey category in stomach contents following Winemiller (1990).

We also carried out timed laboratory feeding trials for a preliminary investigation of the extent of piscivory in F. grandis. For the trials, we collected adult F. grandis (85-139 mm total length [TL]) and prey fishes (juvenile Cyprinodon species and Lucania parva, 20-34 mm TL) from the Pecos River near Iraan, Texas in September 2014 using baited minnow traps and seining. We allowed fishes to acclimate in lab aquaria for 2 weeks before trials started. We exposed aquaria to a 12-h light, 12-h dark light cycle and maintained them at 19-22[degrees]C. We fed all fishes TetraMin[R] (Tetra, Blacksburg, Virginia) flakes during this time; we did not feed F. grandis during the 24 h before feeding trials. Before each trial, we anesthetized F. grandis and prey with buffered MS-222 (Argent Laboratories, Redmond, Washington), weighed, and measured them. We then placed one F. grandis and 10 randomly selected prey fish in a 38-L feeding trial tank separated by a perforated plastic divider for 1 h to allow the fish to resume normal behavior. The trial began when the barrier was lifted and continued for 30 min. We weighed and measured remaining fish prey after the trial so that we could determine which sizes of prey had been consumed. We carried out a total of 27 30-min trials with different F. grandis individuals.

We collected F. grandis at all Lower Pecos River sites sampled below the confluence with the Black River in New Mexico and above the confluence with Independence Creek in Texas. At sites below Red Bluff Reservoir in the Permian Basin region, F. grandis and another coastal nonnative species, C. variegatus (and hybrids with native C. pecosensis), dominated fish samples. We also collected F. grandisjust below the confluence with Independence Creek in the Edwards Plateau region, but we observed none farther downstream near Pandale, Texas, although they are known to be present farther downstream (Fishes of Texas, http://www.fishesoftexas.org/home/). We collected no F. grandis above the confluence with the Black River in New Mexico. Gut contents analysis of 66 field-caught F. grandis revealed that the most commonly consumed prey category was fishes (Cyprinodon species, Menidia beryllina, and L. parva; Table 1). We found up to 18 fish in individual F. grandis stomachs, with prey fish size ranging from 8 to 25 mm TL. The size range of F. grandis individuals with stomachs containing fish encompassed nearly the full size range of adults captured (55-100 mm standard length). Other categories commonly consumed were aquatic insects (primarily odonates and hemipterans), algae, and detritus. Fishes made up 75-98% of gut volume in F. grandis collected below Red Bluff Reservoir in the Permian Basin region of Texas. At our northernmost site with F. grandis present (near Malaga, New Mexico), aquatic invertebrates composed the highest proportion (65%) of gut volume. Although not documented in gut contents analysis, we observed a large adult F. grandis consuming a swallow (Hirundinidae) nestling that had apparently fallen from a bridge over the river near Sheffield, Texas. In laboratory aquaria, F. grandis consumed up to nine prey fish (20-32 mm TL, maximum total mass of 1.1 g) during 30-min feeding trials. Adult F. grandis >100 mm TL consumed the greatest number of prey fish in feeding trials (Fig. 1).

Stomach contents analysis and laboratory feeding trials revealed that nonnative F. grandis readily consumed small fish prey. Similarly, Blake et al. (2014) found that F. grandis from a nonnative Brazos River population consumed largespring gambusia (Gambusia geiseri) in laboratory aquaria. We found that large F. grandis adults (>100 mm TL), which were common in the Lower Pecos, were highly piscivorous. Whereas occasional fish consumption has been observed in field settings for native F. grandis populations (e.g., Harrington and Harrington 1961; Ley et al., 1994), such high volumes and frequency of fish prey in stomach contents have not been reported, suggesting that their feeding ecology might be different in this inland ecosystem. Consumption of high proportions of fish prey by F. grandis may be a reflection of the low diversity of other prey resources, such as aquatic insect larvae, in these saline reaches. East (2015) reported lower benthic macroinvertebrate diversity in the Lower Pecos within the Permian Basin region as compared with sites below the confluence with Independence Creek in Texas. Our observations of piscivory suggest that F. grandis occupies a unique trophic niche in assemblages of high-salinity reaches of the Lower Pecos, where native piscivores such as Micropterus salmoides and Lepisosteus osseus have not been observed in recent surveys (Cheek and Taylor, 2015; East, 2015). It is possible that the absence of larger piscivorous fishes intolerant of the high salinity in this region has promoted the high abundance of F. grandis.

Interactions with nonnative fishes have been implicated in the declines of many native fish species in southwestern rivers (Minckley and Marsh, 2009). Harmful trophic interactions with nonnatives include competition for food or habitat resources and direct predation (Ross, 1991). The feeding ecology of adult F. grandis in the Pecos River suggests that predation might potentially have greater impacts on species such as F. zebrinus than competition for food resources as suggested by Cheek and Taylor (2015). Our observations of consumption of Cyprinodon species indicate that predation could threaten remaining nonhybrid populations of C. pecosensis if the distribution of nonnative F. grandis expands farther north on the Pecos. In summary, our results suggest that predation impacts of F. grandis could be significant in the Pecos River and other inland habitats. To our knowledge, this is the first study to examine the ecology of this increasingly common nonnative species in inland systems. Additional research is needed for more detailed information on resource availability and feeding preferences, and to investigate habitat use and life history of F. grandis in inland habitats outside their range.

[FIGURE 1 OMITTED]

We thank Texas Tech University and the Center for Active Learning and Undergraduate Engagement at Texas Tech University for funding this research. C. Wilcut, D. Marquez, J. Calvert, A. Howe, andJ. Pease provided assistance in data collection. G. Wilde provided advice for designing feeding trials. M. Castillo assisted with Spanish translation. Work was carried out under Texas Tech University Animal Care and Use protocol 13035-04 and 14070-10. Permits for field collection of fishes were provided by New Mexico Department of Game and Fish and Texas Parks and Wildlife Department. We thank The Nature Conservancy for allowing river access at the Independence Creek Preserve.

LITERATURE CITED

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Submitted 7 June 2015.

Acceptance recommended by Associate Editor, Mark Pyron, 16 October 2015.

Cassie M. Vaughan, Jared H. Breaux, Jessica L. East, Allison A. Pease *

Department of Natural Resources Management, Texas Tech University, Lubbock, TX 79409

* Correspondent: allison.pease@ttu.edu
Table 1--Prey items consumed by Fundulus grandis collected
in the Pecos River (n = 66, 55-123 mm standard length) by
percent volume and percent frequency of occurrence in
stomach contents.

                      Volume (%)   Occurrence (%)

Fishes                77.8         57.6
Gastropods            0.7          1.5
Crustaceans           0.3          4.5
Aquatic insects       2.9          27.3
Terrestrial insects   0.5          4.5
Algae                 9.9          30.3
Detritus/sediment     8.2          10.6
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Title Annotation:NOTES
Author:Vaughan, Cassie M.; Breaux, Jared H.; East, Jessica L.; Pease, Allison A.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1U7TX
Date:Mar 1, 2016
Words:2435
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