Trophic Relationships of Small Nonnative Fishes in a Natural

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Trophic Relationships of Small Nonnative Fishes in a Natural Creek and Several Agricultural Drains Flowing into the Salton Sea, and Their Potential Effects on the Endangered Desert Pupfish Author(s): Barbara A. Martin* and Michael K. Saiki Source: The Southwestern Naturalist, 54(2):156-165. 2009. Published By: Southwestern Association of Naturalists DOI: 10.1894/GG-25.1 URL: http://www.bioone.org/doi/full/10.1894/GG-25.1

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. THE SOUTHWESTERN NATURALIST 54(2):156–165 JUNE 2009

TROPHIC RELATIONSHIPS OF SMALL NONNATIVE FISHES IN A NATURAL CREEK AND SEVERAL AGRICULTURAL DRAINS FLOWING INTO THE SALTON SEA, AND THEIR POTENTIAL EFFECTS ON THE ENDANGERED DESERT PUPFISH

BARBARA A. MARTIN* AND MICHAEL K. SAIKI

United States Geological Survey, Biological Resources Division, Western Fisheries Research Center-Dixon Duty Station, 6924 Tremont Road, Dixon, CA 95620 *Correspondent: [email protected]

ABSTRACT—This study was conducted to characterize trophic relationships of small nonnative fishes and to determine if predation by these fishes contributes to the decline of desert pupfish (Cyprinodon macularius), an endangered cyprinodont on the verge of extinction. We sampled 403 hybrid Mozambique tilapias (Oreochromis mossambica by O. urolepis), 107 redbelly tilapias (Tilapia zillii), 32 longjaw mudsuckers (Gillichthys mirabilis), 182 western mosquitofish (Gambusia affinis), 222 sailfin mollies (Poecilia latipinna), 63 shortfin mollies (Poecilia mexicana), and 235 porthole livebearers (Poeciliopsis gracilis) from a natural creek and four agricultural drains during September 1999– December 2001. Evidence of piscivory was in gastrointestinal contents of 14 hybrid Mozambique tilapias, 3 redbelly tilapias, 10 longjaw mudsuckers, 8 western mosquitofish, 2 sailfin mollies, and 8 porthole livebearers. Although digestion often was too advanced for identification of fishes consumed by nonnative fishes, remains of desert pupfish were in gastrointestinal contents of a longjaw mudsucker. Our findings, along with field evidence from other studies that inverse relationships exist between abundances of desert pupfish and nonnative species, are consistent with the hypothesis that predation by nonnative species is contributing to decline of desert pupfish. We suspect that competitive interactions with nonnative fishes might also adversely affect abundance of desert pupfish.

RESUMEN—Este estudio fue conducido para caracterizar las relaciones tro´ficas entre los peces exo´ticos pequenõs y para determinar si la depredacioń de estos peces contribuyo´ a la disminucioń del cachorrito del desierto (Cyprinodon macularius), un cyprinodonte en peligro de extincioń. Muestreamos un total de 403 hı´bridos de tilapia mosa´mbica (Oreochromis mossambica por O. urolepis), 107 tilapias de vientre rojo (Tilapia zillii), 32 chupalodos (Gillichthys mirabilis), 182 guayacones mosquito (Gambusia affinis), 222 topotes velo negro (Poecilia latipinna), 63 topotes del Atlańtico (Poecilia mexicana), y 235 guatopote jarocho (Poeciliopsis gracilis) en un riachuelo natural y cuatro desaguës agrıćolas desde septiembre de 1999 hasta diciembre del 2001. Evidencia de piscivorıá fue encontrada en el contenido gastrointestinal de 14 hı´bridos de tilapias mosa´mbica, 3 tilapias de vientre rojo, 10 chupalodos, 8 guayacones mosquito, 2 tapotes velo negro y 8 guatopotes jarocho. Aunque la digestioń fue frecuentemente muy avanzada para identificar las especies de peces consumidas por los peces exo´ticos, restos de cachorritos del desierto fueron observados en el contenido gastrointestinal de un chupalodo. Nuestros resultados, junto con evidencia de campo de otros estudios en los que existen relaciones inversas entre abundancias de los cachorritos del desierto y peces exo´ticos, son consistentes con la hipo´tesis de que la depredacioń causada por los peces exo´ticos esta´ contribuyendo a la disminucioń del cachorrito del desierto. Sospechamos que las interacciones competitivas con peces exo´ticos pueden afectar tambień la abundancia del cachorrito del desierto de una manera perjudicial.

Predation is one of the most important from nonnative species causing dramatic effects ecological threats, along with competition, dis- in native fish faunas are widespread and include ease, and hybridization, posed by deliberate or invasion of the upper Great Lakes by sea lamprey inadvertent introductions of nonnative fishes (Petromyzon marinus) that virtually wiped out into habitats of native fish throughout the world populations of large fishes in ,20 years (Coble (Moyle and Cech, 1996). Examples of predation et al., 1990; Schneider et al., 1996), peacock bass June 2009 Martin and Saiki—Trophic relationships of fishes 157

(Cichla ocellaris) and largemouth bass (Micropterus the Salton Sea itself and in streams entering the salmoides) introduced into Central America, Sea (Walker et al., 1961). Both the longjaw eliminating most species of fish from large lakes mudsucker (Gillichthys mirabilis) and western (Zaret and Paine, 1973), and Nile perch (Lates mosquitofish were introduced into the Salton niloticus) introduced into Lake Victoria in Sea ca. 1930, but due to their low populations, eastern Africa, leading to extinction of nearly neither was considered a threat to desert pupfish 200 native species (e.g., Witte et al., 1992; Ogutu- (Walker et al., 1961). The orangemouth corvina Ohwayo, 1993). In the American Southwest, (Cynoscion xanthulus), bairdiella (Bairdiella icis- predation by rainbow trout (Oncorhynchus mykiss) tia), and sargo (Anisotremus davidsonii) were may be responsible for decimating the Little established in the Salton Sea in the 1950s and, Colorado spinedace (Lepidomeda vittata) in the although piscivorous, these species were not Little Colorado River system (Blinn et al., 1993), considered a threat to desert pupfish because whereas predation by western mosquitofish their habitats rarely overlapped (Walker et al., (Gambusia affinis) is likely to have eliminated 1961). However, the porthole livebearer (Poeci- the Sonoran topminnow (Poeciliopsis occidentalis) liopsis gracilis), sailfin molly, and shortfin molly from many waters in southern Arizona (Meffe et (Poecilia mexicana) were introduced into the al., 1983). Although competition from nonnative Salton Sea in the mid-1960s, and hybrid Mozam- fishes also is believed to adversely affect native bique and redbelly tilapias were introduced in fishes, such interactions are difficult to prove. the 1970s (Schoenherr, 1981a). In just a few The desert pupfish (Cyprinodon macularius)is years, the fish-species assemblage changed dra- another southwestern species whose original matically. Where the desert pupfish once was range in portions of Arizona, California, and common or abundant in the Salton Sea and its northern Mexico may have been greatly curtailed shoreline pools, sailfin molly became the dom- by proliferation of nonnative fishes, although the inant species (Black, 1980). By 1983, dominance exact ecological mechanisms are poorly docu- had shifted to hybrid Mozambique and redbelly mented. Several researchers (e.g., Schoenherr, tilapias (these two species collectively constituted 1981a; Steinhart, 1990; Moyle, 2002) have ca. 75% of 2,744 fish captured in agricultural suggested predation on eggs, juveniles, and drains), with desert pupfish accounting for only adults, and competition for food and space as five individuals (K. E. Moore, in litt.). Plummet- possible ways that the hybrid Mozambique tilapia ing size of populations of desert pupfish in the (Oreochromis mossambica by O. urolepis), redbelly Salton Sea basin, along with other losses tilapia (Tilapia zillii), sailfin molly (Poecilia throughout its historical range in the lower latipinna), and other nonnative species can Colorado River drainage, led to listing of this adversely affect populations of desert pupfish. species for federal protection as endangered The desert pupfish is a small (,75 mm total (United States Fish and Wildlife Service, 1986). length), short-lived (2-year life span) species with Although the desert pupfish increased in broad tolerance to extreme environmental con- abundance following die-offs of tilapias in the ditions (water temperatures approaching 45uC, Salton Sea during 1988–1990 (K. Nicol, pers. dissolved oxygen concentrations as low as 0.1– comm., cited by Moyle, 2002), its populations 0.4 mg/L, salinities approaching 68%; Moyle, declined again by 1996 or 1997, when the 2002). Although originally distributed through- population of the hybrid Mozambique tilapia out the lower Colorado and Gila river drainages, rebounded (S. Keeney, pers. comm.). According the desert pupfish is now present only in small, to Costa-Pierce and Riedel (2000), ca. 8,000,000 isolated populations around the Salton Sea and hybrid Mozambique tilapias died in August 1999 in the Colorado River delta (Moyle, 2002). In from stress due to overcrowding, high tempera- addition, the desert pupfish has colonized many tures, and anoxic water. Nevertheless, the gillnet agricultural drains in the Salton Sea basin. catch of adult hybrid Mozambique tilapias was Inverse relations between abundance of non- still high, averaging 20 kg or 29 fish/net/h for native fish and abundance of desert pupfish four nets set near mouths of rivers in August suggest ecological interactions consistent with 1999 (Caskey et al., 2007). In August 2000, predation, competition, or both, acting as although catch-per-unit-effort had decreased to limiting factors on desert pupfish. Prior to the ca. 10 fish/net/h, the hybrid Mozambique early 1960s, the desert pupfish was common in tilapia was still the most numerous species in 158 The Southwestern Naturalist vol. 54, no. 2 the Salton Sea (Caskey et al., 2007). Coincident Coachella valleys into the Salton Sea and generally are with the still high populations of the hybrid ,2 m deep and ,20 m wide. Salt Creek and the drains were sampled over a ca. 50-m distance extending Mozambique tilapia in 2000–2001, Martin and upstream from the mouth (see Martin and Saiki, 2005, Saiki (2005) reported that desert pupfish consti- for physicochemical characteristics of sampling sites). tuted only ca. 1% of 16,885 fish captured with Sampling sites were visited at least seasonally during minnow traps in a creek and several agricultural September 1999–December 2001, with monthly samples collected during April–October 2001 when juvenile drains. desert pupfish were most numerous. During 2002, large die-offs of fish associated At each sampling site, 10 unbaited collapsible with episodes of widespread anoxia and high minnow traps (25 cm high by 25 cm wide by 43 cm concentrations of hydrogen sulfide and ammo- long, 0.3-cm square mesh; Nylon Net Company, nia were documented in the Salton Sea, and Memphis, Tennessee) were fished for ca. 30 min. Except for desert pupfish, all captured fishes were eventually reduced the adult population of the fixed in 10% formalin for later identification and hybrid Mozambique tilapia to ca. 10% of its analysis of gastrointestinal contents. Desert pupfish former abundance (Caskey et al., 2007). In were measured for total length (nearest 1 mm) and addition, populations of the orangemouth cor- weight (nearest 1 mg), then immediately released alive near where they had been captured. vina, bairdiella, and sargo declined to the point In the laboratory, fixed fishes were identified to where gillnet surveys conducted by personnel of species, weighed, total length was measured, and the California Department of Fish and Game gastrointestinal contents were removed by dissection. have failed to capture any individuals since May Gastrointestinal contents were identified to the lowest 2003 (S. Keeney, pers. comm.). However, begin- taxonomic level possible using standard keys (e.g., Usinger, 1971; Merritt and Cummins, 1978; Pennak, ning in 2003 and continuing through the 1978), then wet biomass (nearest 0.01 mg) of each present, desert pupfish appeared with increasing forage category was recorded for individual fish. frequency in the Salton Sea itself (S. Keeney, Forage categories were combined if the percentage pers. comm.), a phenomenon not experienced of gastrointestinal tracts containing the forage catego- since the 1960s. In addition to capturing ry did not exceed 5% for any given species. Mean percentage wet biomass of each taxon consumed by relatively large numbers of desert pupfish in various species of fish was calculated by first obtaining minnow traps, a small number of adult desert the percentage of each forage category for each fish pupfish have even been caught by personnel of and then taking the mean of those percentages for the California Department of Fish and Game in each forage category for all individuals within a species. gill nets set offshore at depths $2 m (S. Keeney, Raw data were stored as Excel files, then summarized pers. comm.). using SAS software (SAS Institute, Inc., 1990). Scho- Historical changes in abundance and distribu- ener’s index was used to compare dietary overlap tion of desert pupfish and nonnative fishes in the among species: X Salton Sea basin strongly suggest that nonnative ~ { { Cxy 1 0:5 pxi pyi fishes are responsible for the decline of populations of desert pupfish. We hypothesize that where Cxy is the index value, pxi is the proportion of predation by nonnative fishes is one way that food type i used by species x, and pyi is the they adversely affect the desert pupfish. To test proportion of food type i used by species y (Bowen, 1996). A Schoener’s index value of 1 indicates this hypothesis, we characterized trophic rela- complete dietary overlap, whereas a value of 0 tionships of nonnative species in a natural creek indicates no dietary overlap between species x and and several agricultural drains where the desert y. A Kruskal-Wallis non-parametric test was used to pupfish is still present. Although not an objective determine if significant differences existed among median values for percentage biomass of various of our study, we also discuss the possibility that taxonomic categories of fish consumed by each competitive interactions may contribute to de- nonnative species. If the resulting chi-square value cline of the desert pupfish. was significant, Tukey’s studentized range test computed with ranked values was used to separate MATERIALS AND METHODS—Sampling sites were estab- taxonomic categories. lished in Salt Creek (33u269480N, 115u509560W) and four agricultural drains (Avenue 81 Drain, 33u269390N, RESULTS—Gastrointestinal contents from 403 116u029500W; Avenue 84 Drain, 33u269270N, 116u029450W; mostly juvenile hybrid Mozambique tilapias (14– County Line Drain, 33u259470N, 116u029370W; and Trifolium 20A Drain, 33u069300N, 115u459510W) that 170 mm total length; 0.05–233.20 g), 107 juve- historically supported populations of desert pupfish. These nile redbelly tilapias (17–66 mm total length; drains convey agricultural wastewater from Imperial and 0.07–4.94 g), 32 longjaw mudsuckers (48– June 2009 Martin and Saiki—Trophic relationships of fishes 159

117 mm total length; 1.26–23.35 g), 182 western DISCUSSION—Proliferation and spread of non- mosquitofish (9–57 mm total length; 0.01– native species generally are assumed to be mostly 2.55 g), 222 sailfin mollies (11–53 mm total responsible for the decline or extinction of many length; 0.03–3.22 g), 63 shortfin mollies (22– native species in the southwestern United States 61 mm total length; 0.14 to 3.00 g), and 235 (Minckley and Deacon, 1968; Schoenherr, porthole livebearers (11–60 mm total length; 1981a; Miller et al., 1989; Scoppettone et al., 0.01–2.40 g) were examined during this study. 2005). Several investigators have argued that Empty gastrointestinal tracts ranged from 2% (8 competition for limited resources contributed to fish) in hybrid Mozambique tilapia to 22% (14 the decline of native species in the lower Color- fish) in shortfin molly (Table 1). ado River basin, which includes the Salton Sea Unidentifiable organic matter (possibly ani- (Schoenherr, 1981a; Greger and Deacon, 1988; mal tissues in advanced stages of digestion, Mills et al., 2004). However, other investigators decaying plant detritus, or both) was the primary have argued that predation is a more likely forage item in gastrointestinal contents of five of mechanism whereby nonnative fishes eliminated seven species (Table 1). It accounted for .87% native species (Meffe, 1985; Marsh and Douglas, of all foods consumed by hybrid Mozambique 1997; Minckley et al., 2003). Regardless of cause, tilapia, redbelly tilapia, sailfin molly, shortfin desert fishes may be especially vulnerable to molly, and porthole livebearer. By comparison, nonnative invaders because they typically evolved the most abundant forage item in the longjaw in species-poor systems with few or no compet- mudsucker was fishes, comprising .47% of itors or predators (Soltz and Naiman, 1978). gastrointestinal contents, whereas the most During our study, nonnative species fed abundant forage item in the western mosquito- primarily on unidentifiable organic matter that fish was insects, comprising .46% of gastroin- presumably consisted of detrital aggregates. testinal contents. Although detritus seemingly was plentiful, it According to Schoener’s index, the longjaw may not have been the most nutritious food mudsucker exhibited the lowest overlap in diet available. Other researchers (Persson, 1983; among the seven species, whereas the western Bowen, 1984; Hayes and Rutledge, 1991) report- mosquitofish exhibited moderate overlap with ed detritus to be an inferior food resource that the five remaining species (Table 2). Hybrid often leads to fish with poor condition factors. Mozambique tilapia, redbelly tilapia, sailfin According to Bowen (1979), detrital aggregates molly, shortfin molly, and porthole livebearer in different portions of Lake Sibaya in southern exhibited high dietary overlap with each other Africa varied in nutritional value, with those (values $0.94). The high values of overlap were from shallow areas being more nutritious than due to these species mostly consuming uniden- those from deeper waters. These observations led tifiable organic matter (detritus). Bowen (1979) to conclude that the nutritional Except for shortfin molly, all species exhibit- value of detritus is influenced by its composition, ed evidence of piscivory (Table 1). Fishes which can depend on where it is located within a occurred in gastrointestinal contents of 3% of lake. Many researchers report detritus to be a hybrid Mozambique tilapias, 3% of redbelly significant source of food for tilapias (Bowen, tilapias, 31% of longjaw mudsuckers, 4% of 1979; Spataru et al., 1983; Bowen, 1984; Muchiri western mosquitofish, 1% of sailfin mollies, and et al., 1995), sailfin mollies (Breden and Bird, 3% of porthole livebearers. On average, the 1988; Meffe and Snelson, 1989), and western longjaw mudsucker was the most piscivorous mosquitofish (Meffe and Snelson, 1989; Hayes species, followed distantly by western mosquito- and Rutledge, 1991), and attribute this to the fish and redbelly tilapias, and lastly by the abundance and ease of obtaining detritus and remaining species (Table 3). Although fishes the lack of more nutritious foods. When inver- typically were too digested for identification to tebrates are available, they serve as the primary species, gastrointestinal contents of longjaw food of western mosquitofish (Meffe and Snel- mudsuckers included porthole livebearers, hy- son, 1989; Hayes and Rutledge, 1991; Daniels brid Mozambique tilapias, and desert pupfish. and Felley, 1992; Gophen et al., 1998; West et al., In addition, fry of western mosquitofish were in 2003). By comparison, the sailfin molly feeds gastrointestinal contents of adult western mos- primarily on vascular plants even when inverte- quitofish. brates are available (Meffe and Snelson, 1989). 160

TABLE 1—Relative importance of various food items in gastrointestinal tracts of fishes in southern California as indicated by their mean-percentage contribution to total mass of gastrointestinal contents (M) and the percentage of gastrointestinal tracts in which they occurred (O): n 5 number of fish examined and n0 is number of fish with empty gastrointestinal tracts.

Redbelly Longjaw Western Sailfin Shortfin Porthole Mozambique tilapia mudsucker mosquitofish molly molly livebearer tilapia n 5 403, n 5 107, n 5 32, n 5 182, n 5 222, n 5 63, n 5 235, n0 5 8 n0 5 4 n0 5 5 n0 5 11 n0 5 11 n0 5 14 n0 5 16 Food item MOMOMOMOMOMOMO Plants (total) 4.5 6.3 0.8 7.2 2.6 0.5 3.0

Vascular plants 2.9 43.4 6.1 66.4 0.8 9.4 6.7 28.0 1.0 12.6 0.5 12.7 2.5 31.1 Naturalist Southwestern The Algae 1.6 25.1 0.2 2.8 0 0 0.5 2.2 1.1 24.3 0 1.6 0.5 8.1 Insects (total) 3.1 2.2 14.5 47.09 1.0 0 8.7 Diptera 1.4 12.4 0.5 3.7 0.3 6.3 1.1 6.0 0.4 3.6 0 0 2.0 11.16 Hemiptera 0.2 1.5 ,0.1 1.9 0.1 3.1 15.7 26.4 0 0 0 0 ,0.1 0.4 Other aquatic insects 1.3 21.8 1.5 17.8 14.0 34.4 23.5 44.0 0.6 4.5 0 0 6.5 20.9 Winged or terrestrial insects 0.2 3.5 0.2 1.9 0 0 6.7 15.9 0 0 0 0 0.2 1.3 Other non-insect invertebrates (total) 0.6 1.8 11.5 3.5 0.5 0.2 0.3 Gastropoda 0.1 0.3 1.2 3.7 0.2 6.3 1.5 2.8 0 0 0 0 ,0.1 0.9 Oligochaeta 0 0 0 0 9.2 9.4 0.5 0.6 0.2 0.5 0 0 0 0 Other invertebrates 0.5 7.0 0.5 2.8 2.0 6.3 1.5 5.0 0.2 3.2 0.2 1.6 0.3 2.1 Fishes (total) 0.2 1.2 47.7 3.6 0.1 0 0.2 Western mosquitofish 0 0 0 0 0 0 0.9 1.1 0 0 0 0 0 0 Porthole livebearer 0 0 0 0 13.4 6.3 0 0 0 0 0 0 0 0 Mozambique tilapia 0 0 0 0 6.9 3.1 0 0 0 0 0 0 0 0 Desert pupfish 0 0 0 0 6.7 3.1 0 0 0 0 0 0 0 0 Unidentifiable remains of fish 0.2 3.5 1.2 2.8 20.7 18.8 2.7 3.3 0.1 0.9 0 0 0.2 3.4 Unidentifiable organic matter (detritus) 91.7 96.5 88.6 94.4 25.5 62.5 38.8 46.7 95.9 95.1 99.3 77.8 87.8 88.1 o.5,n.2 no. 54, vol. June 2009 Martin and Saiki—Trophic relationships of fishes 161

TABLE 2—Schoener’s indices of overlap in diet of fishes in southern California. Values approaching zero indicate dissimilar diets, whereas values approaching 1.00 indicate similar diets.

Mozambique Redbelly Longjaw Western Sailfin Shortfin Porthole Species tilapia tilapia mudsucker mosquitofish molly molly livebearer Mozambique tilapia 1.00 0.97 0.10 0.68 0.96 0.98 0.97 Redbelly tilapia 1.00 0.12 0.71 0.98 0.95 0.97 Longjaw mudsucker 1.00 0.28 0.10 0.09 0.13 Western mosquitofish 1.00 0.70 0.66 0.72 Sailfin molly 1.00 0.94 0.96 Shortfin molly 1.00 0.94 Porthole livebearer 1.00

During our study, western mosquitofish con- mostly detritus and, to a much lesser extent, sumed mostly invertebrates or detritus, depend- insects, invertebrates, and fishes. Tilapias are ing on time of year that samples were collected, omnivorous, feeding on detritus and plant with invertebrates being more important during materials, but also including some animal matter June and July when they were presumably in (Spataru et al., 1983; Trewavas, 1983; Gophen et greatest abundance. al., 1998). Other investigators described poeci- We were not allowed to sacrifice desert pupfish liids as being mostly omnivorous, feeding on for analysis of gastrointestinal contents; however, terrestrial and aquatic invertebrates, detritus, this species is described as omnivorous, prefer- algae, and vascular plants (Meffe and Snelson, ring to feed on invertebrates, but consuming 1989), with diet of western mosquitofish consist- algae and detritus when invertebrates are scarce ing mostly of invertebrates (Hayes and Rutledge, (Bunnell, 1970; Cox, 1972; Naiman, 1979; Moyle, 1991; Gophen et al., 1998). Judging from the 2002). Although our data indicated that the collective observations, the desert pupfish is hybrid Mozambique tilapia, redbelly tilapia, likely to exhibit a significant overlap in diet with sailfin molly, shortfin molly, and porthole western mosquitofish, and moderate overlaps livebearer exhibited low overlap in diet with with tilapias, mollies, and porthole livebearers. the longjaw mudsucker and moderate overlap However, as defined by Larkin (1956) and with western mosquitofish, these five species others, competition is the demand, typically at exhibited the greatest overlaps in diet among the same time, of more than one organism for each other (Table 2), collectively consuming the same resources of the environment in excess

TABLE 3—Relative contribution of fish in gastrointestinal contents of fishes in southern California. Values are arcsine-transformed means expressed as percentage of the total biomass of gastrointestinal contents. Judging from results of Kruskal-Wallis tests, overall variation among means was significant (x2 5 91.29, df 5 6, P , 0.001). Within a column, means followed by the same letter are not significantly different(P . 0.05) according to Tukey’s studentized range test computed from ranked data.

Species Whole fish or fragments in gastrointestinal contents (%) Mozambique tilapia 0.16 C Redbelly tilapia 1.19 BC Longjaw mudsucker 47.73 A Western mosquitofish 3.58 B Sailfin molly 0.07 C Shortfin molly 0.00 C Porthole livebearer 0.20 C 162 The Southwestern Naturalist vol. 54, no. 2 of immediate supply. Without information on western mosquitofish, White River springfish whether any of the consumed foods were in short (Crenichthys baileyi), and Moapa dace (Moapa supply, we cannot easily invoke competition as coriacea) after aquatic vegetation was depleted an ecological consequence of overlapping diets. in the Muddy River system of southeastern Nevertheless, nonnative fish were especially Nevada. Moreover, under aquarium conditions, numerous during summer and early autumn in Scoppettone (1993) observed shortfin mollies our study area (Martin and Saiki, 2005), raising feeding on their own young and on larvae of the possibility of insufficient food resources White River springfish. Poecillids are well known during those months. for cannibalizing their newborn young (Meffe The longjaw mudsucker mainly was carnivo- and Crump, 1987; Meffe and Snelson, 1989). In rous and exhibited little overlap in diet with the addition, the western mosquitofish preys on eggs other nonnative species (Table 2). During our and young of other species, resulting in high study, this species was especially piscivorous mortality and, in some instances, eventually (48% of total diet), consuming desert pupfish, eliminating cohabiting species (Myers, 1965; tilapias, porthole livebearers, and unidentifiable Meffe, 1982, 1985; Scoppettone, 1993). Although fish remains, but also eating aquatic inverte- relying on circumstantial evidence, Deacon and brates (26%). Other investigators have reported Minckley (1974) suggested that the western longjaw mudsuckers foraging on desert pupfish mosquitofish was responsible for eliminating (Walker et al., 1961) and California killifish the desert pupfish throughout most of its (Fundulus parvipinnis; West and Zedler, 2000), historical range in Arizona. although Barry et al. (1996) indicated that Although fishes were not a significant compo- longjaw mudsuckers in Elkhorn Slough fed nent of gastrointestinal contents for six of the mainly on aquatic invertebrates. Moyle (2002) seven nonnative species examined, our results reported that the longjaw mudsucker feeds on might under-estimate negative effects of pisciv- invertebrates and small fish about in proportion ory on populations of desert pupfish. Winkleman to their availability. and Aho (1993) examined diet of eastern In addition to piscivory by the longjaw mosquitofish (Gambusia holbrooki) and indicated mudsucker, we discovered that tilapias, western that data on gastrointestinal contents probably mosquitofish, sailfin mollies, and porthole live- misrepresents actual importance of cannibalism bearers preyed on some fish. Moyle (2002) noted because small fish could be digested more that both the Mozambique tilapia and redbelly rapidly than other food items. Meffe (1985) tilapia occasionally will feed on fish. Even within determined that consumed fish were recogniz- their native range in Africa, these tilapias include able for ,4 h after ingestion by predator fish. fish in their diets (Ben-Tubia, 1960; Bowen, Furthermore, Meffe (1985) calculated that an 1979). A. A. Schoenherr (unpublished data, investigator is able to detect no more than ca. cited by Varela-Romero et al., 2002) reported 25% of prey by using analysis of gastrointestinal that juvenile redbelly tilapias consumed eggs of contents. Meffe (1985) also noted that the desert pupfish, whereas Nichols (pers. comm., probability can be low for finding an already cited by Black, 1980) determined that nearly rare fish in the gastrointestinal tracts of abun- 25% of the diet of adult redbelly tilapias from an dant predators, with likelihood of such a agricultural drain at the Salton Sea consisted of discovery decreasing even more given that unidentified fish and fish eggs. During our study, digestion can make prey items unrecognizable primarily juvenile tilapias were sampled, and this after just a few hours. Meffe (1985) argued that life stage might not have been as piscivorous as even when rate of predation is low, its cumulative adults. Piscivory in Mozambique and redbelly impact on a rare prey species still can be high if tilapias probably occurs after aquatic vegetation potential predators are abundant, as was the case and other food sources are depleted, as reported for our study where desert pupfish comprised by Scoppettone et al. (2005) for the blue tilapia only 1% of the catch (see Martin and Saiki, 2005, (Oreochromis aureus), a close relative of the hybrid for relative abundances of desert pupfish and Mozambique tilapia. According to Scoppettone nonnative fishes captured at sampling sites). et al. (2005), herbivorous blue tilapias measuring In addition to preying on nearly all life stages ca. 50–160 mm standard length switched to a (embryos to adults) of the desert pupfish predominantly piscine diet that included the (Loiselle, 1980; Schoenherr, 1981b; M. Matsui, June 2009 Martin and Saiki—Trophic relationships of fishes 163 pers. comm., cited by Schoenherr, 1988), We thank the California Department of Fish and nonnative fishes can adversely affect desert Game for logistical support during this study. We also pupfish in other ways. For example, aggressive thank S. Keeney for assisting with selection of sites, K. behavior exhibited by breeding males guarding English, M. Farinha, R. Hager, A. Hitch, and S. Keeney for assisting with field or laboratory work, K. English, their territories uses energy needed for other M. Farinha, and R. Hager for creating computerized reproductive activities, such as courtship and datasets, G. Garrett, S. Hurlbert, S. Keeney, F. Mejia, P. spawning (Schoenherr, 1988). As populations Rissler, G. Scoppettone, and two anonymous reviewers of nonnative fishes increase in breeding areas of for their thoughtful comments and suggestions, and F. the desert pupfish, such encounters will occur Mejia for translating the abstract into Spanish. more often. Other species of pupfish (e.g., Red River pupfish, Cyprinodon rubrofluviatilis,Leon LITERATURE CITED Springs pupfish, Cyprinodon bovinus,andAsh Meadows pupfish, Cyprinodon nevadensis mio- BARRY, J. P., M. M. YOKLAVICH,G.M.CAILLIET,D.A. nectes) reportedly experience similar reproduc- AMBROSE, AND B. S. ANTRIM. 1996. Trophic ecology of tive interference from nonnative fishes (Echelle the dominant fishes in Elkhorn Slough, California, et al., 1972; Soltz, 1974; Kennedy, 1977). 1974–1980. Estuaries 19:115–138. BEN-TUBIA, A. 1960. The biology of the cichlid fishes of Moreover, Loiselle (1980) determined that lake Tiberias and Huleh. 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