Comparison of Nile Tilapia and Three Co-Occurring Native Centrarchids in Invaded Coastal Mississippi Watersheds

Environ Biol Fish (2006) 76:283–301 DOI 10.1007/s10641-006-9033-4

ORIGINAL PAPER

Foraging in non-native environments: comparison of Nile Tilapia and three co-occurring native centrarchids in invaded coastal Mississippi watersheds

Mark S. Peterson Æ William T. Slack Æ Gretchen L. Waggy Æ Jeremy Finley Æ Christa M. Woodley Æ Melissa L. Partyka

Received: 21 July 2005 / Accepted: 21 March 2006 / Published online: 11 May 2006 Springer Science+Business Media B.V. 2006

Abstract We examined the diet of the alien ate size class effect (Global R = 0.457, Nile tilapia and bluegill, redear sunfish, and P = 0.1%) and a strong species effect (Global largemouth bass over a two-year period in R = 0.876, P = 0.1%). Pairwise tests indicated coastal Mississippi. Nile tilapia diet was visually species fed on different components of and separated from the three natives based on locations within the environment, with bluegill, group-average linkage cluster analysis. Sequen- redear sunfish and largemouth bass (all tial two-way nested analysis of similarities R £ 0.683, P = 0.1%) having the most similar indicted there was no season effect (Global dietary components and Nile tilapia (all R = 0.026, P = 24.3%), but there was a moder- R ‡ 0.953, P = 0.1%) having the most distinct. Multivariate dispersion indicated that largemouth bass (1.425) and bluegill (1.394) had the M. S. Peterson (&) Æ J. Finley most diverse diets compared to redear sunfish Department of Coastal Sciences, The University (0.906) and Nile tilapia (0.918). Similarities of of Southern Mississippi, 703 East Beach Drive, Ocean Springs, MS 39564, USA percentages indicated that diets were separated e-mail: [email protected] based on prey: bluegill and redear sunfish consumed chironomids and insects; largemouth bass W. T. Slack consumed fish and insects; and Nile tilapia fed Mississippi Department of Wildlife, Fisheries and Parks, Mississippi Museum of Natural Science, 2148 most often on sediment resources such as nem- Riverside Drive, Jackson, MS 39202-1353, USA atodes, rotifers, bryozoans and hydrozoans. Nile tilapia had the highest frequency of mud, sand G. L. Waggy and detritus in their stomachs, suggesting they Grand Bay National Estuarine Research Reserve, 6005 Bayou Heron Road, Moss Point, MS 39562, fed directly on bottom sediments. These data USA and the fact that Nile tilapia has a 1.3–7.6 times longer intestine on average than its body length, C. M. Woodley support our contention that this alien species Department of Wildlife, Fish and Conservation Biology, University of California-Davis, Davis, feeds at the base of the food web and is well California 95616, USA adapted to survive and proliferate in non-native environments. M. L. Partyka University of North Carolina-Wilmington, Center for Marine Science, 5600 Marvin Moss Lane, Wilmington, Keywords Alien species Æ Cichlidae Æ Coastal NC 28409, USA bayou Æ Interactions Æ Invasions Æ Trophic ecology

123 284 Environ Biol Fish (2006) 76:283–301

Introduction nated by blue tilapia (later in system invasion, low diversity). The mouthbrooding Nile tilapia, Oreochromis In terms of management of aquaculture niloticus, is one of the top species used in aqua- activities, it is clear that tilapias and their hybrids culture worldwide (Costa-Pierce 2003), and this are difficult to identify, thus making informed alien species (Occhipinti-Ambrogi and Galil decisions of these widely used species more dif- 2004) has become recently established in a rela- ficult in terms of assessing which ‘strain’ is being tively small region of southeastern Mississippi cultured, their physiological and ecological and poses a significant threat to native fishes and capabilities, and consequently judging which fisheries (Peterson et al. 2004, 2005). Over a two exotic tilapia to import and where aquaculture year period in coastal freshwater and saline bayou development should be permitted (Costa-Pierce systems, we collected this species ranging from 2003). Unfortunately, little data on any alien yolk-sac to 430 mm TL, quantified spawning year- species are available in the northern Gulf of round in these coastal watersheds, and showed Mexico (GOM), in part, due to the relatively that the smallest female with mature oocytes was short or unknown history of alien species intro- 79.9 mm TL, with 50% of the females being ma- ductions (Carlton 2001). The mild temperatures ture at 113 mm TL (Peterson et al. 2004, 2005). of the northern GOM make this ecologically Finally, Peterson et al. (2005) predicted that valuable area more vulnerable to invasion by ambient environmental conditions, the presence alien species than other parts of the nation of a downstream thermal refuge from an aqua- (Fuller et al. 1999). These valuable ecosystems culture facility, and the generally low salinity of may suffer reduced biodiversity in the face of Mississippi bayous all combine to provide a increasing invasion of alien species unless a bet- quality environment for continued survival and ter understanding of the species and environ- reproduction of the released fish. mental setting which makes invasions successful Members of the Cichlidae are recognized as are wholly understood. As part of a larger study having the potential to alter aquatic communities to examine the biology and ecology of alien Nile into which they are introduced (Courtenay 1997), tilapia in coastal Mississippi watersheds (Peter- in part because they are trophic generalists son et al. 2004, 2005), the objective of this study (Trewavas 1983). This diverse array of feeding was to quantify and then compare the seasonal strategies may lead to trophic interactions be- and ontogenetic feeding habits of an established tween native and alien species. For example, alien cichlid, the Nile tilapia, Oreochromis Hendricks and Noble (1979) in Texas and Zale niloticus, and three co-occurring native centrar- and Gregory (1990) in Florida documented con- chids, bluegill, Lepomis macrochirus, redear siderable trophic overlap in young blue tilapia, sunfish, L. microlophus, and largemouth bass, Oreochromis aureus, and shad larvae, Dorosoma Micropterus salmoides. spp., in lentic habitats. Zale (1987) determined that blue tilapia survival and growth exceeded those of largemouth bass, Micropterus salmoides, Materials and methods and at a comparable age they were superior to largemouth bass in their ability to prey on zoo- Fish diet analysis was conducted only on fish col- plankton. Finally, Traxler and Murphy (1995) lected by seining, hook and line, or daytime showed that largemouth bass ( < 85 mm TL) and trammel nets in the Pascagoula and Escatawpa blue tilapia compete for food, and when blue River systems between 16 November 2000 and 18 tilapia were grown in combination with large- June 2002. We sampled monthly at two fixed mouth bass, they were significantly longer and stations that were closely associated with an heavier than blue tilapia grown alone. This sug- aquaculture facility in the Pascagoula River sys- gests that blue tilapia actually may have an tem. In addition, 14 general areas were sampled advantage in mixed assemblages (early in system periodically to determine the extent of the tilapia invasion, high diversity) relative to one domi- invasion. Fixed stations were sampled with seines

123 Environ Biol Fish (2006) 76:283–301 285

(3 or 15 m long) and dipnets, while stations within Examination of the diets of these species was the general areas were sampled with trammel nets conducted on stomach contents only. The stom- (31 and 61 m long), hook and line, minnow traps, achs were opened longitudinally with iridectomy and plastic coated wire crab traps. Trammel nets scissors, and the contents were placed in labeled were fished as day sets or strike net sets. Detailed glass vials with a Rose Bengal/10 % formalin study site descriptions can be found in Peterson solution (Birkett and McIntyre 1971) for at least et al. (2004, 2005). All fish were measured to total 24 h. For those fish collected by hook and line, length (TL, to 0.01 mm accuracy) and grouped the most anterior 5 mm of stomach and its con- by season (Fall = October–November; Win- tents were removed to reduce any ‘bait’ bias. ter = December–February; Spring = March–May; Contents were then washed under flowing tap and Summer = June–September) according to the water for 5 minutes into a series of stacked 14 cm following outline (Table 1). Seasonal grouping of (5.5 inch) brass sieves (Market Grade Sieves Nos. months is based on best professional opinion and 20, 40, 60, 80, 120, 200 [850, 425, 250, 180, 125, the normal water temperature patterns of this re- 75 lm mesh]) (Carr and Adams 1972). The con- gion. Fish lengths were grouped into a maximum of tents retained on each sieve were washed into a 25 size classes. Fish £50 mm TL were separated labeled glass vial and stored in 70% ethanol. For into five size classes of 10 mm each (e.g., class Nile tilapia only, fish < 40 mm TL were sieved 01 = 0–10 mm TL) and fish >50 mm TL were only through the 200 sieve fraction because pre- separated into 20 size classes of 20 mm each (e.g., liminary data indicated all prey passed through 06 = 50–70 mm TL). This size class distribution the larger sieves. The contents of each sieve was used because of ontogenetic changes in mouth fraction were washed into a glass petri dish and morphology and associated increases in locomo- the components were identified with a dissecting tory ability noted in many teleost fishes (Wootton microscope. Prey items were recorded as present 1990; Gerking 1994). The number of fish examined or absent and expressed as a frequency of within each size class per season varied depending occurrence. Prey items were identified to the on the collection but was maximized at 20 indi- lowest possible taxon using available keys viduals. These selected fish represented a group (Needham and Needham 1962; Pennak 1978; pooled across months (within season) and sites. In Bland and Jaques 1978; Auer 1982; Brusca and instances when >20 fish per size class and season Brusca 1990; Holland-Bartels et al. 1990; Merritt were collected, specimens were randomly selected and Cummins 1996; Smith and Johnson 1996). for diet analysis based on a weighting technique The stomach contents for each size fraction were where the percent of fish collected at each site and then individually vacuum-filtered with a Millipore month represented the same percentage of the fish filter holder and a vacuum flask onto separate used for analysis. The total number of stomachs pre-weighted Whatman 42.5 mm diameter glass analyzed by species and season are found in microfiber filters (dried to 0.00001 g). The stom- Table 1. ach contents on the dried filter were then dried at

Table 1 Listing of the size range and the number of size classes per species, number of individuals by season, total number collected, and the number of sites specimens were collected from and percent of total individuals from the two ﬁxed sites Species Size range Fall Winter Spring Summer Total Sites (two (size classes) (season 1) (season 2) (season 3) (season 4) ﬁxed sites)

Oreochromis niloticus 7.3–430 mm TL (n = 24) 120 163 192 115 590 5 (86.72%) Lepomis macrochirus 22.1–173 mm TL (n = 10) 2 26 81 20 129 4 (55.67%) Lepomis microlophus 40.1–165 mm TL (n = 7) 8 18 1 46 73 4 (94.52%) Micropterus salmoides 13.9–557 mm TL (n = 12) 2 0 49 49 100 7 (25%) These individuals were used in the diet analyses. Fall = October and November, Winter = December, January and February, Spring = March, April and May, and Summer = June, July, August and September pooled by year

123 286 Environ Biol Fish (2006) 76:283–301

60C for 24 h, allowed to cool in a desiccator and (min TL = 4.53; max TL = 430.00) of log10 re-weighed as above. The weight difference transformed data (gender combined) based on (stomach contents and ﬁlter weight—ﬁlter 100 Nile tilapia collected from all sites and dates. weight) for each size fraction was recorded. Parametric data analysis was performed with SPSS software (version 12.0, SPSS, Inc., Chicago, Statistical analyses Ill).

Cluster analysis based on the hierarchical agglomerative method with the group-average Results linkage procedure was used to compare square root transformed mean frequency of occurrence A total of 892 fish diets were quantified ranging of food items of individual specimens ontogenet- from 7 to 24 different size classes depending upon ically, seasonally, and by species with the Bray– species and season (Table 1). Sixty-six percent of Curtis similarity coefficient. The cluster analysis the diets were from Nile tilapia, 14.5 % were from based on Bray–Curtis values was computed using bluegill, 8.2 % were from redear sunfish, and PRIMER (version 5.28; PRIMER-E Ltd, Plym- 11.2% were from largemouth bass (Table 1). outh, UK); these values range from 0 to 100% with 0% being no similarity and 100% being Oreochromis niloticus diet identical (Clarke 1993; Clarke and Warwick 2001). The cluster analysis attempts to create Nile tilapia examined for stomach contents groupings of samples (species/season/size class ranged from 7.3 to 430 mm TL (n = 590 fish in combination, n = 108 combinations) based on the 24 size classes; Fig. 1, Appendix 1). Only 4.5 % variables (prey items, n = 57) through a gener- of the Nile tilapia stomachs were empty. In ated similarity matrix. general, prey size and dry weight comparisons of We sequentially conducted two different two- the diet indicate that Nile tilapia tended to eat way nested analysis of similarities (ANOSIM) to prey that were small in all size classes, but prey test for differences in square root transformed size and overall dry weight consistently in- mean frequency of occurrence of the raw diet creased as the fish grew (Fig. 2A). Frequently data with season nested under species and then eaten prey types in all size classes were small size class nested under species. Emphasis was prey like hydrozoa, rotifers, nematodes and placed on comparing the R-stat values in the bryozoa plus various insect stages and insect output of the ANOSIM analysis. When R-stat parts (Appendix 1). Additionally microcrusta- values in pair wise comparisons between diets are ceans like cladocera, copepods, and ostracods close to 1 the compositions are very different, were consumed quite frequently as were fish whereas when they are close to 0, the composi- scales (Appendix 1). The most frequent stomach tions are very similar. Multivariate dispersion items were amorphous debris, detritus, sand (MVDISP) was used to delineate the variability grains and mud clumps (Appendix 1). The latter in the diet components among species (high val- suggests that Nile tilapia consume bottom sedi- ues equal more dispersion of the diet), while the ment directly which reflects the diverse prey similarity percentages (SIMPER) analysis was types in all fish, particularly the large individuals used to disaggregate the similarity matrix to (Appendix 1). identify which diet components were most There was a significant linear relationship be- responsible for any dissimilarity between species tween TL and intestine length (mm) for O. nil- (Clarke 1993; Clarke and Warwick 2001). oticus ranging from 4.53 to 430.0 mm TL. The Frequency of occurrence (%) of prey and dry relationship is log10 (intestine length) = )0.152 + 2 weight (g) contribution of each sieve fraction by 1.391 (log10 TL) (n = 100; r = 0.957, P < 0.001). species and size class (pooled by season) are Over this body size range, the mean intestine presented. We also developed a total length (TL, length ranged from 1.3 to 7.6 times longer than mm) vs. intestinal length (mm) linear regression the fish.

123 Environ Biol Fish (2006) 76:283–301 287

1 2 3 4 5

100 t111 t311 t307 t324 t301 t219 t403 t319 t317 t314 t213 t107 t407 t306 t205 t405 t210 t102 t320 t309 t409 t305 t103 t302 t208 t106 t404 t204 re207 re407 re311 re410 re107 re206 bg209 lm315 bg312 lm112 bg409 lm407 bg207 bg310 lm306 bg107 bg405 lm305 bg309 bg205 lm302 bg308 lm304 lm404 lm406 bg306 t321 t202 t402 t203 t303 t211 t322 t323 t212 t304 t110 t318 t117 t312 t308 t105 t313 t209 t310 t201 t408 t316 t104 t109 t108 t206 t406 t207 t401 t101 re411 re405 re208 re106 re409 re406 bg305 bg412 lm409 lm405 lm413 lm314 bg311 bg208 bg307 bg303 bg204 lm303 bg304 bg106 bg406 bg206 lm108 lm408 T (02-24) & BG (09) LM (05-15) BG (03-12), LM (02-05), RE (05-11), T (01) BG (09-12) RE (10-11)

Fig. 1 Plot of cluster analysis dendrogram based on Bray– at the bottom of the dendrogram reflect season and size Curtis similarity and group-average linkage of square root class codes for the group of species below the horizontal transformed species, season, and size class mean frequency line. For example, 310 = season 3 (spring) and size class 10 of occurrence diet data. The solid horizontal line is the (131.01–150 mm TL). Season codes are 1 = fall, 2 = win- 50% similarity level allowing visualization of five upper- ter, 3 = spring, and 4 = summer. LM = largemouth bass, level groupings labeled 1–5 on top of the figure. The codes T = Nile tilapia, BG = bluegill, RE = redear sunfish

Lepomis macrochirus diet Lepomis microlophus diet

Bluegill examined ranged from 22.1 to 190 mm TL Redear sunfish ranged from 40.1 to 170 mm TL (n = 129 fish in 10 size classes; Fig. 2B, Appendix (n = 73 fish in seven size classes; Fig. 2C, 2). Only 3.9% of bluegill had empty stomachs. In Appendix 3). Only 1.4% of the redear sunfish general, prey size and dry weight comparisons of stomachs were empty. In general, redear sunfish the diet indicate that bluegill ate prey that were consumed prey that were large and heavy even in large and heavy even in small size classes (Fig. 2B), the smallest size class obtained (Fig. 2C). Overall with larger fish consuming larger and heavier prey dry weight increased with redear sunfish size class (Fig. 2B, Appendix 2). Frequently eaten prey (Fig. 2C) and larger fish consumed larger and types were small dipterans (larvae and pupae), heavier prey (Fig. 2C, Appendix 3). In fact, the microcrustaceans like cladocerans, calanoid co- bulk of the diet was found in the 850 and 425 lm pepods, ostracods, and gammarid amphipods sieve fractions (Fig. 2C). Frequently eaten prey (Appendix 2). Additionally, insect parts, amor- items were small dipterans (larvae and pupae), phous debris, detritus, and sand grains were also larger insects (odonates and orthopterans), common in the diet (Appendix 2). In general, as gammarid amphipods, and molluscs (amnicolidae bluegill grew, the consumption and frequency of and shell parts) (Appendix 3). Additionally, larger insects increased. insect parts, amorphous debris, detritus, and sand

123 288 Environ Biol Fish (2006) 76:283–301

Fig. 2 Three-dimensional plot of dry sample weight (g) of selection included the smallest and largest size classes’ total stomach contents of Nile tilapia (A), bluegill (B), available plus representative ones totaling eight size redear sunﬁsh (C) and largemouth bass (D) by sieve size classes. See Table 1 for total number of size classes by fraction (lm) and ﬁsh size class (mm, TL). Size class species

grains were also common in the diet (Appendix 4). Only 4% of largemouth bass stomachs were 3). In general, the frequency of larger insects and empty. In general, largemouth bass consumed molluscs increased in the diet as redear sunfish prey that were large and heavy even in the grew. smallest size class obtained (Fig. 2D). Overall dry weight increased with largemouth bass size class Micropterus salmoides diet (Fig. 2D) and larger fish consumed larger and heavier prey (Fig. 2D, Appendix 4). Like redear Largemouth bass ranged from 13.9 to 570 mm TL sunfish, the bulk of the diet was found in the 850 (n = 100 fish in 12 size classes; Fig. 2D, Appendix and 425 lm sieve fractions (Fig. 2D). Frequently

123 Environ Biol Fish (2006) 76:283–301 289 eaten prey types were small insect larvae and mean similarity (SIMPER values) was redear pupae (dipterans), cladocerans, ostracods, cala- sunfish (70.81), Nile tilapia (69.75), bluegill noid copepods, and miscellaneous eggs (Appen- (58.72), and largemouth bass (58.33). The breadth dix 4). Beginning about 20–30 mm TL, fish of diet among species (measured by MVDISP became a frequent dietary component in large- global values) was lowest in redear sunfish mouth bass (Appendix 4). Identifiable fish in the (0.906), followed by Nile tilapia (0.918), bluegill diet were from the families Poeciliidae, Centrar- (1.394) and largemouth bass (1.425). Finally, chidae and occasionally Cichlidae (Appendix 4). pairwise comparison of these species suggested that Nile tilapia generally had the most dissimilar Trophic interactions diet compared to the other species (Table 3) followed by largemouth bass, with bluegill and red- The cluster analysis showed five higher-level ear sunfish having the least dissimilar diet clusters at the 50% similarity level (Fig. 1). The (Table 3). diets of Nile tilapia and large largemouth bass size Nile tilapia was most distinct from all three classes 05–15 (‡50 mm TL) were separated from native centrarchids (Table 2; all pairwise each other, with small largemouth bass size clas- R ‡ 0.953). Nile tilipia clearly foraged on lower ses 02–05 (10.01–50 mm TL) being linking more trophic levels (mud, sand, bryozoans, nematodes, closely with bluegill size classes 03–12 (20.01– hydrozoans and rotifers) whereas largemouth 190 mm TL) and redear sunfish size classes 05–11 bass fed on larger invertebrates and fishes (insect (40.01–170 mm TL) than to larger largemouth parts, fish scales, unidentified fish, fish parts) at bass (Fig. 1). In contrast, bluegill in size classes sizes as small as 10.01–50.01 mm TL (Table 3; 09–12 (110.01–190 mm TL) and redear sunfish in Appendices 1 and 4). Prey of bluegill (calanoid size classes 10–11 (130.01–170 mm TL) were copepods, chironomids, insect parts, sand, cla- more similar to each other than to smaller size docerans) and redear sunfish (chironomids, insect classes or to Nile tilapia (Fig. 1). parts, sand, Amnicolidae molluscs) do not overlap The results of the first 2-way nested ANOSIM to a great degree with Nile tilapia (pairwise (season nested within species) showed no season R = 0.957 and 0.953, respectively). The main effect on diet (Global R = 0.026, P = 24.3%), cause for this separation stems from the primary whereas the second two-way ANOSIM (size class foraging of Nile tilapia on the bottom resources nested within species) showed a moderate size whereas bluegill and redear sunfish forage more class effect (Global R = 0.457, P = 0.1%) and a on pelagic species in addition to epi-benthic strong species effect (Global R = 0.876, resources (Table 3; Appendices 1, 2 and 3). The P = 0.1%). All pairwise comparisons were sig- pairwise similarity in diet of the three native nificantly different with Nile tilapia being the centrarchids varied but ranged from R = 0.683 most distinct from all other species (Table 2). The between largemouth bass and redear sunfish to decreasing order of the diets with the largest R = 0.423 between bluegill and redear sunfish (Table 3).

Table 2 Pairwise R-stat values of square root transformed mean diet frequency of occurrence by species after a two- way nested ANOSIM (size class nested within species; Discussion global R = 0.876, P = 0.1%) Species Alien Nile tilapia in our low salinity bayou systems do not appear to directly compete for food Bluegill Largemouth Nile resources with three native co-occurring centrar- bass tilapia chids. Their diet at all size classes of mostly lower Largemouth bass 0.620 trophic level items (mud, sand, bryozoans, nem- Nile tilapia 0.957 0.956 atodes, hydrozoans and rotifers) was most distinct Redear sunfish 0.423 0.683 0.953 from largemouth bass (apex predator), which fed All pairwise values are significant at P = 0.1% on larger invertebrates and fishes (insect parts,

123 290 Environ Biol Fish (2006) 76:283–301

Table 3 Mean pairwise abundance of important diet components of the four ﬁsh species from the Pascagoula and Escatawpa River watersheds based on SIMPER analysis Prey items Pairs Mean Mean Mean Mean Contribution abundance abundance dissimilarity dissimilarity/SD (%)

BG versus RE BG RE 43.62 Insect parts 0.55 0.22 4.39 1.49 10.07 Sand 0.45 0.90 3.66 1.13 8.39 Cladocera 0.33 0.00 3.41 1.12 7.83 Chironomidae 0.56 0.92 3.10 0.93 7.10 Calanoida 0.25 0.08 2.92 0.99 6.69 Ostracods 0.26 0.08 2.50 0.84 5.73 Amnicolidae 0.00 0.33 2.26 0.69 5.18 Gammaridae 0.19 0.08 2.25 0.73 5.16 Eggs 0.21 0.00 2.14 0.72 4.90 Nematoda 0.13 0.07 2.04 0.97 4.68 Ceratopogonidae 0.09 0.10 1.70 0.66 3.89 Diatoms 0.01 0.17 1.43 0.49 3.27 72.90 BG versus LMB BG LMB 51.08 Scales 0.01 0.52 4.80 1.32 9.39 Chironomidae 0.56 0.17 4.46 1.30 8.73 Fish parts 0.00 0.41 3.92 1.13 7.68 Insect parts 0.55 0.30 3.82 1.26 7.48 Sand 0.45 0.27 3.73 1.20 7.31 Cladocera 0.33 0.21 3.59 1.17 7.03 Unid. Fish 0.00 0.34 3.41 0.99 6.67 Calanoida 0.25 0.14 2.98 1.04 5.84 Eggs 0.21 0.18 2.78 0.92 5.44 Ostracods 0.26 0.03 2.44 0.89 4.78 70.34 BG versus T BG T 55.20 Mud 0.00 1.00 6.93 3.40 12.55 Chironomidae 0.56 0.05 4.18 1.47 7.58 Insect parts 0.55 0.15 3.69 1.46 6.68 Bryozoa 0.01 0.40 3.34 1.26 6.05 Sand 0.45 0.99 3.21 1.16 5.81 Cladocera 0.33 0.10 2.98 1.19 5.40 Rotifera 0.06 0.31 2.93 1.31 5.31 Hydrozoa 0.00 0.30 2.87 1.23 5.19 Nematoda 0.13 0.31 2.81 1.27 5.09 Calanoida 0.25 0.00 2.45 0.94 4.44 Ostracods 0.26 0.12 2.39 0.93 4.33 Scales 0.01 0.18 2.06 0.93 3.73 72.15 RE versus LMB RE LMB 51.87 Chironomidae 0.92 0.17 6.68 1.62 12.88 Sand 0.90 0.27 5.68 1.34 10.95 Scales 0.00 0.52 5.32 1.31 10.26 Fish parts 0.00 0.41 4.27 1.11 8.24 Unid. Fish 0.00 0.34 3.71 0.98 7.16 Insect parts 0.22 0.30 3.68 1.08 7.10 Amnicolidae 0.33 0.00 2.42 0.68 4.67 Calanoida 0.08 0.14 1.88 0.69 3.62 Cladocera 0.00 0.21 1.78 0.56 3.44 Nematoda 0.07 0.04 1.74 0.84 3.35 71.67

123 Environ Biol Fish (2006) 76:283–301 291

Table 3 Continued Prey items Pairs Mean Mean Mean Mean Contribution abundance abundance dissimilarity dissimilarity/SD (%)

RE versus T RE T 50.70 Mud 0.00 1.00 7.48 3.27 14.75 Chironomidae 0.92 0.05 6.48 2.16 12.78 Bryozoa 0.00 0.40 3.64 1.24 7.18 Rotifera 0.09 0.31 3.26 1.32 6.43 Hydrozoa 0.00 0.30 3.08 1.22 6.07 Nematoda 0.07 0.31 2.82 1.33 5.56 Insect parts 0.22 0.15 2.50 1.10 4.93 Scales 0.00 0.18 2.21 1.04 4.36 Amnicolidae 0.33 0.00 2.16 0.68 4.25 Tiplidae 0.00 0.18 1.95 0.89 3.85 70.15 LMB versus T LMB T 56.57 Mud 0.00 1.00 7.46 3.27 13.19 Sand 0.27 0.99 4.99 1.46 8.82 Scales 0.52 0.18 3.82 1.24 6.75 Fish parts 0.41 0.00 3.69 1.12 6.52 Bryozoa 0.00 0.40 3.60 1.24 6.36 Unid. Fish 0.34 0.00 3.23 0.98 5.71 Rotifera 0.02 0.31 3.16 1.31 5.59 Nematoda 0.04 0.31 3.12 1.31 5.51 Hydrozoa 0.00 0.30 3.07 1.23 5.43 Insect parts 0.30 0.15 3.06 1.07 5.41 Cladocera 0.21 0.10 2.17 0.78 3.84 73.14

Prey items are listed in order of their contribution to the mean dissimilarity between pairs of fish species (column five), with a cutoff when the cumulative percent contribution to mean dissimilarity approaches about 70%. BG = Bluegill; RE = Redear sunfish; LMB = Largemouth bass; T = Nile tilapia. SD = standard deviation

fish scales, unidentified fish, fish parts) at sizes as tom resources whereas bluegill and redear sunfish small as 20–30 mm TL. Nile tilapia appears to forage more on pelagic species in addition to epi- feed mainly on bottom sediments and extract benthic resources. McCrary et al. (2001) found energy from accompanying organisms in the mud, fine sand, algae and phytoplankton in the sediments as well as some epibenthic prey. Al- stomach of introduced Nile tilapia in Laguna de though prey size and dry weight did increased Apoyo, Nicaragua, and McBay (1961) noted that slowly in Nile tilapia, diet was quite similar across Nile tilapia >6–9 inches (152–228 mm TL) fed on size classes, as prey on all sieve size fractions were bottom algae whereas smaller fish feed on zoo- represented throughout the entire size range plankton in ponds in Alabama. This again sug- examined, reflecting their habits of consuming gests a generalist feeding strategy in Nile tilapia in sediments and their contents. The extremely long non-native environments. intestinal tract of Nile tilapia reflects this adap- It is also clear that Nile tilapia throughout their tation which has been reported in numerous native range is adapted to feed on all trophic detritivorous (Stevens and Hume 1995) and levels. For example, Beveridge et al. (1989), marine herbivorous species (Horn 1989). In con- Robinson et al. (1990), and Richter et al. (1999) trast, bluegill diets (calanoid copepods, chirono- indicated these diurnal feeders (Moriarty and mids, insect parts, cladocerans) and redear sunfish Moriarty 1973a) ingest suspended bacteria and diets (chironomids, insect parts, Amnicolidae planktonic algae as well as periphyton (Dempster molluscs) do not overlap to a great degree with et al. 1993). In Nile tilapia >179 mm standard Nile tilapia because Nile tilapia feed on the bot- length (SL), macrophytes were important with

123 292 Environ Biol Fish (2006) 76:283–301 diatoms being common only in winter months opportunistic foragers and used both planktonic (Khallaf and Alne-na-ei 1987). Finally, Moriarty and benthic food resources. and Moriarty (1973b) determined that the diet of Redear sunfish, in contrast, frequently fed on Nile tilapia fry in Lake George, Uganda, Africa small dipteran larvae and pupae, larger insects consisted of algae, Aufwuchs, macrophytic detri- (odonates and orthopterans), gammarid tus, rotifers, zooplankton, insect larvae, and water amphipods, and molluscs (amnicolidae and shell mites. Small fish (30–60 mm TL) consumed more parts). In general, as redear sunfish grew, the phytoplankton than fry, and not much zooplank- consumption and frequency of larger insects and ton. Large fish (>60 mm TL) fed upon phyto- molluscs increased. These prey items are similar plankton, occasionally some detritus, and a few to those reported in different habitats. For rotifers. While this feeding flexibility makes them example, Desselle et al. (1978) noted that redear ideal aquaculture species, it also makes them sunfish were opportunistic feeders but fed mainly highly adaptive toward colonizing areas outside on mud crabs in an estuarine lake in Louisiana. their native range if they escape. Clearly, as Vanderkooy et al. (2000) noted that small redear Lowe-McConnell (1987) points out, Nile tilapia in sunfish fed on zooplankton whereas larger fish African lakes have a varied diet feeding on shifted to benthic macrofauna, and redear sunfish periphyton in some lakes but worms and insects in frequently used sediment-associated prey. Finally, other nearby lakes, illustrating their generalist Huckins (1997) and Huckins et al. (2000) noted feeding habits in their native environments. that redear sunfish are specialized molluscivores Diets of the three co-occurring native cen- in their natural habitat, and shift from soft body trarchids we examined did not appear to vary invertebrates to molluscs as they grow. Clearly, from what is typical of the species and size range redear sunfish in our study area forage opportu- examined in other regions within their native nistically and generally use benthic food range. For example, in coastal Mississippi resources, including molluscs as they grow. drainages bluegill frequently preyed on dipteran Largemouth bass consumed prey that was large larvae and pupae, microcrustaceans like cladoc- and heavy even in the smallest size class obtained. erans, calanoid copepods, ostracods, and gamm- Overall, dry weight increased with largemouth arid amphipods. Insect parts, amorphous debris, bass size and larger fish consumed larger and detritus and sand grains were also common in heavier prey. In fact, the bulk of the diet was the diet. In general, as bluegill grew, the con- found in the largest (850 and 425 lm) sieve frac- sumption and frequency of larger insects in- tions. Frequently eaten prey were small diptera creased. These prey items suggest bluegill fed larvae and pupae, cladocerans, ostracods, cala- both in the water column, in structural habitat noid copepods, and miscellaneous eggs. Begin- like logs, and possibly epibenthically. In Vir- ning about 20–30 mm TL, fish became a frequent ginia, Flemer and Woolcott (1966) found that dietary component with identifiable prey were bluegill fed on unidentified insects parts, from the families Poeciliidae, Centrarchidae and Hemiptera, copepods, and detritus. Young (age occasionally Cichlidae. These data mirror the 0–1, 32–44 mm SL) fish fed more often on mi- results of other studies. For example, McLane crocrustaceans and dipteran larvae while older (1947–1948) in Florida and Keast (1985) in Can- fish consumed great percentages of larger insects ada noted that largemouth bass shift from feeding like coleopterans and hymenopterans. In an on zooplankton and small invertebrates to large estuarine lake in Louisiana, Desselle et al. (1978) invertebrates (crayfish) and fish as they grow. noted that bluegill fed mainly on barnacle cirri, Piscivory begins as early as 23–35 mm TL (Keast amphipods and small blue crabs; these authors 1985). Colle et al. (1976) noted that age 0–II (95– indicated bluegill were opportunistic foragers. 266 mm TL) largemouth bass feed on fish and Finally, Vanderkooy et al. (2000) determined freshwater Palaemonetes spp. whereas fish ~ age 3 that small bluegill fed on zooplankton whereas (~267 mm TL) contained predominately fish. larger fish shifted to benthic macrofauna. It is Finally, Traxler and Murphy (1995) determined clear that bluegill in our study sites were that largemouth bass feed on chironomid larvae

123 Environ Biol Fish (2006) 76:283–301 293 and pupae, and odonates at sizes between 25 and et al. 1995) by interfering with spawning by na- 40 mm TL. tive nest-building species like centrarchids. Spe- In contrast to the centrarchids examined in this cialized tilapias, Oreochromis zilli and study, the sediment feeding strategy of Nile tila- Oreochromis aurea, introduced to other regions pia of all size classes is similar to detritivorous of the world that have been shown to feed on species such as striped mullet (Odum 1970) and eggs and fry of native clupeids and centrarchids gizzard shad (Smoot and Findlay 2000). Each has (Crutchfield 1995), thus having a direct impact an elongated intestinal tract to increase surface on native species. Similar direct impacts are area and gut residency time and thus the oppor- found in other alien species like the Mayan tunity for digestion and assimilation. Species that cichlid, Cichlosoma uropthalmus, in south Flor- utilize this trophic strategy also appear to influ- ida which exhibits nest predation on native ence function in freshwater systems by affecting centrarchids (Trexler et al. 2000) and may con- phytoplankton biomass, productivity and com- tribute to decreases in centrarchid reproduction munity structure (Schaus et al. 1997; Schaus and and changes in population dynamics. Clearly, the Vanni 2000) via excretion of sediment resources Nile tilapia’s generalist feeding strategy is one of to the water column. This may occur in our many adaptive capabilities when colonizing new coastal drainages if Nile tilapia expand their dis- areas. In fact, Myrick (2002) in his review noted tribution and increase in population size over that omnivorous- or generalist-cultured species time. of tilapia (like Nile tilapia) may have an Multiple factors couple to increase survival advantage over more specialized wild species and proliferation of alien species in non-native because of their ability to exploit a wide variety environments. Physiological, ecological, and ad- of food resources. vanced reproductive capabilities of Nile tilapia There was no direct food resource competition make them excellent aquaculture species, but between Nile tilapia and the three native cen- these same capabilities make them successful trarchids. The fact that Nile tilapia feeds at the invaders (Peterson et al. 2004, 2005). Coupled base of the food web, has great physiological with these capabilities, habitat alteration in a capabilities (Lowe-McConnell 1987; Costa-Pierce number of forms has been shown to support the 2003), and an advanced reproductive strategy proliferation of alien species (Moyle et al. 2003; (Peterson et al. 2004, 2005), indicate it will do well Occhipinti-Ambrogi and Savini 2003), and as in coastal drainages of the north-central Gulf of human population increases and urban develop- Mexico. Managers should consider reducing or ment spreads, problems caused by aquatic alien eliminating aquaculture of tilapias in general in species will also increase. Alien aquatic species coastal watersheds as natural disasters like that have become established have been shown flooding and hurricanes can cause tilapias to enter to have direct and indirect impacts in non-native and distribute (or redistribute) into other habitats environments and the communities living within and drainages thus exacerbating the invasion. them (Crutchfield 1995; McKaye et al. 1995; Finally, practices by aquaculture facilities need to Courtenay 1997). For example, Oreochromis be incorporated into management plans that will spp. can literally occupy all available habitats minimize escape, regardless of species, particu- with their spawning sites which can have severe larly in coastal areas which are prone to flooding consequences on native fish fauna (McKaye in response to natural disasters.

123 294 123 Appendix

Appendix 1 Summary of the mean Nile tilapia prey frequency of occurrence by size class pooled by sieve fraction and season of ﬁsh collected in the Pascagoula and Escatawpa River watersheds. Values in parentheses are sample size

Size classes (mm)

Prey 0–10 10.01–20 20.01–30 30.01–40 40.01–50 50.01–70 70.01–90 90.01–110 110.01–130 130.01–150 150.01–170 170.01–190 category (19) (57) (60) (54) (59) (62) (57) (55) (43) (39) (16) (7)

Hydrozoa 14 31.7 55.6 47.6 61.3 33.3 36.4 48.8 38.5 43.7 57.1 Rotifera 5.3 12.3 15 27.8 44.1 59.7 59.6 58.2 67.4 25.6 46.1 42.8 Nematoda 8.8 30 18.5 32.2 25.8 17.5 25.4 55.8 20.5 43.7 57.1 Bryozoa 1.7 10 20.4 25.4 48.4 50.9 61.8 83.7 76.9 56.2 85.7

Acari 1.7 1.6 3.6 5.1 Insects Collembola Unid. larvae 1.8 Coleoptera Unid. species 1.7 3.2 Tricoptera Unid. larvae Diptera Dixidae larvae 1.7 1.6 8.8 12.7 9.3 7.7 7.7 Tipulidae larvae 3.5 10 5.6 11.9 16.1 8.8 12.7 11.6 5.1 Chironomidae 6.7 11.1 5.1 4.8 5.3 12.7 larvae Unid. Diptera 5.3 3.3 3.7 5.1 4.6 Ephemeroptera Unid. species Crustaceans Cladocera 5 3.7 3.4 5.1

Copepoda 3.5 6.7 1.8 3.4 6.4 1.8 2.3 2.6 76:283–301 (2006) Fish Biol Environ Ostracoda 1.8 4.8 2.3 10.2 Amphipoda 1.7 Annelida Oligochaeta Lumbricidae 10.2 Miscellaneous Insects parts 1.7 1.7 1.8 32.2 24.2 7 18.2 7 10.2 14.3 Fish scales 8.8 13.3 9.3 22.0 16.1 22.8 9.1 32.6 5.1 15.4 Fish eggs

Oreochromis sp. 1.8 Fish parts 2.3 2.6 Gambusia sp. Amorphous debris 68.4 100 98.3 100 100 100 100 100 100 97.4 87.5 100 Detritus 94.7 98.2 96.7 100 100 100 100 100 100 97.4 87.5 100 nio ilFs 20)76:283–301 (2006) Fish Biol Environ Mud clumps 36.8 82.4 96.7 100 100 100 100 100 100 97.4 87.5 100 Sand 52.6 80.7 95 100 100 100 100 100 100 97.4 87.5 100 Empty (%) 21 3.5 1.8 5.1 1.6 3.5 5.4 7 12.5

Prey category 190.01–210 210.01–230 230.01–250 250.01–270 270.01–290 290.01–310 310.01–330 330.01–350 350.01–370 370.01–390 390.01–410 410.01–430 (10) (1) (1) (1) (16) (1) (6) (5) (5) (12) (3) (1)

Hydrozoa 30 50 25 30 33.3 Rotifera 16.7 50 50 20 Nematoda 40 100 100 100 25 50 66.7 100 Bryozoa 70 100 25 75 20

Acari 100 83.3 50 75 60 100 Insects Collembola Unid. larvae Coleoptera Unid. species Tricoptera Unid. larvae 25 Diptera Dixidae larvae 100 100 100 25 30 33.3 Tipulidae larvae 20 100 100 100 50 50 60 100 Chironomidae larvae Unid. Diptera Ephemeroptera Unid. species 25 Crustaceans Cladocera 83.3 100 75 60 100 Copepoda 25 10 Ostracoda 10 100 100 75 75 60 33.3 100 Amphipoda Annelida Oligochaeta Lumbricidae Miscellaneous Insects parts 10 100 50 20 Fish scales 30 25 10 100 Fish eggs 10 100 100 10 Oreochromis sp. Fish parts Gambusia sp. 10 123 Amorphous debris 100 100 100 100 100 83.3 100 100 100 100 100 Detritus 100 100 100 100 100 83.3 100 100 100 100 100

Mud clumps 100 100 100 100 100 83.3 100 100 100 100 100 295 Sand 100 100 100 100 100 83.3 100 100 100 100 100 Empty (%) 10 100 16.7 20 20 16.7 296 123 Appendix 2 Summary of the mean bluegill prey frequency of occurrence by size class pooled by sieve fraction and season of ﬁsh collected in the Pascagoula and Escatawpa River watersheds. Values in parentheses are sample size Size classes (mm) Prey category 20.01–30 30.01–40 40.01–50 50.01–70 70.01–90 90.01–110 110.01–130 130.01–150 150.01–170 170.01–190 (6) (20) (29) (34) (19) (6) (3) (4) (5) (2)

Diatoms 6.9 33.3 Rotifera 16.7 3.5 47.4 33.3 Nematoda 24.1 11.8 47.4 33.3 Bryozoa 3.5 5.9 33.3 Acari 7 2.9 15.8 Insects Odonata Coenagriidae 16.7 adult Hemiptera Cicadellidae 20 adult Notonectidae 15.8 20 adult Orthoptera Acrididae 50 adult Coleoptera Coleoptera Adult/larvae 2.9 66.7 40 50 Trichoptera Hydroptilidae 15.8 16.7 adult Trichoptera 2.9 larvae 76:283–301 (2006) Fish Biol Environ Lepidoptera Lepidoptera 20 larvae Diptera Ceratopogonidae 2.9 16.7 33.3 20 50 Chironomidae 6.7 5 41.4 55.9 63.1 83.3 66.7 100 50 larvae Diptera 16.7 50 adult/pupae Hymenoptera Formicidae 16.7 33.3 33.3 nio ilFs 20)76:283–301 (2006) Fish Biol Environ

Crustaceans Cladocera 83.3 75 55.2 76.5 5.2 33.3 33.3 33.3 Copepoda Calanoida 10 31.0 47 5.2 16.7 33.3 Harpacticoidae 13.8 Ostracoda 55 41.4 32.3 78.9 66.7 33.3 Mysidacea 16.7 10 Isopoda 3.5 33.3 Amphipoda Gammaridae 15 17.2 5.2 83.3 33.3 50 Mollusca Polyplacophora Ancylidae 33.3 33.3 Gastropoda 33.3 Bivalvia 33.3 25 Miscellaneous Insect parts 20 34.5 35.3 73.7 50 100 100 100 Eggs 3.5 5.2 33.3 Fish scales 20 Amorphous debris 100 100 100 100 100 100 100 100 100 Detritus 100 100 100 100 100 100 100 100 100 Sand 67 25 41.4 50 68.4 50 33.3 Empty (%) 5 3.5 2.9 25 20 123 297 298 123 Appendix 3 Summary of the mean redear prey frequency of occurrence by size class pooled by sieve fraction and season of ﬁsh collected in the Pascagoula and Escatawpa River watersheds. Values in parentheses are sample size Size classes (mm) Prey category 40.01–50 50.01–70 70.01–90 90.01–110 110.01–130 130.01–150 150.01–170 (15) (17) (31) (6) (1) (1) (2)

Diatoms 100 Nematoda 13.3 9.7 16.7 Insects Odonata 16.7 Linellulidae nymph 100 Orthoptera Gryllidae 100 100 Diptera Ceratopogonidae larvae 16.7 Chironomidae larvae/pupae 100 100 100 100 100 100 100 Diptera larvae 3.2 16.7 Arthropoda Araneae 100 Crustaceans Amphipoda Gammaridae 16.7 50 Copepoda Calanoida 100 Ostracoda 100 Mollusca Amnicolidae 100 100 Shell parts 100 100

Annelida 76:283–301 (2006) Fish Biol Environ Oligochaeta 100 100 Miscellaneous Insects parts 26.7 16.7 100 50 Amorphous debris 100 100 100 96.7 100 100 100 Detritus 100 100 100 96.7 100 100 100 Sand 100 100 100 96.7 100 100 100 Empty (%) 3.2 Appendix 4 Summary of the mean largemouth bass prey frequency of occurrence by size class pooled by sieve fraction and season of ﬁsh collected in the 76:283–301 (2006) Fish Biol Environ Pascagoula and Escatawpa River watersheds. Values in parentheses are sample size Size classes (mm) Prey category 10.01–20 20.01–30 30.01–40 40.01–50 50.01–70 70.01–90 90.01–110 110.01–130 170.01–190 210.01–230 410.01–430 550.01–570 (1) (16) (15) (30) (16) (11) (5) (2) (1) (1) (1) (1)

Rotifera 10 Bryozoa 3.3 Insects Hemiptera Unid. adult 1 6.2 Homoptera Aphidae 6.2 Diptera Chironomidae larvae/pupae 26.7 20 30 62.5 50 100 Unid. adult 6.2 Crustaceans Cladocera 86.7 93.3 36.7 Copepoda Calanoida 53.3 26.7 26.7 Ostracoda 13.3 16.7 Amphipoda Gammaridae 10 Astacidae 6.2 Pisces Poecillidae 6.7 12.5 30 Gambusia sp. 6.2 10 Centrarchidae 6.7 Lepomis sp. 6.7 13.3 20 Cichlidae Oreochromis sp. 25 Cyprinidae 25 Unid. ﬁsh 33.3 6.7 20 37.5 20 100 Fish bones 13.3 20 12.5 30 100 100 100 100 Fish scales 6.7 30 25 60 75 100 100 100 100 Miscellaneous Misc. eggs 46.7 73.3 36.7 123 Insect parts 6.7 20 26.7 25 30 100 50 Amorphous debris 100 100 100 100 100 100 100 100 100 100 100 100

Detritus 100 93.3 100 100 100 100 50 100 100 100 100 100 299 Sand 20 40 30 12.5 10 50 100 Empty (%) 6.2 6.7 9.1 300 Environ Biol Fish (2006) 76:283–301

Acknowledgements Field and laboratory assistance Courtenay WR Jr (1997) Tilapias as non-indigenous spe- was provided by C. Vervaeke, B. Lezina, and J. cies in the Americas: environmental, regulatory and Brookins. Brian Lezina checked all databases. Richard legal issues. In: Costa-Pierce BA, Rakocy JE (eds) and Grady Scott of Moss Point, Mississippi allowed Tilapia aquaculture in the Americas, Volume 1. access to their property for sampling. James D. Wil- World Aquaculture Society, Baton Rouge, LA, liams of the U.S. Geological Survey, Florida Caribbean pp 18–33 Science Center in Gainesville, Florida verified tilapia Crutchfield JU Jr (1995) Establishment and expansion of specimens. The Jackson County Port Authority allowed redbelly tilapia and blue tilapia in a power plant access and provided assistance with our sampling on the cooling reservoir. Am Fish Soc Symp 15:452–461 Black Creek Cooling Ponds facility. Lastly, The Mis- Dempster PW, Beveridge MCM, Baird DJ (1993) sissippi Department of Wildlife, Fisheries and Parks Herbivory in the tilapia Oreochromis niloticus:a funded this project to MSP and WTS through grant comparison of feeding rates on phytoplankton and F-129. periphyton. J Fish Biol 43:385–392 Desselle WJ, Poirrier MA, Rogers JS, Cashner RC (1978) A discriminant functions analysis of sunfish (Lepomis) food habits and feeding niche segregation in the Lake References Pontchartrain, Louisiana estuary. Trans Am Fish Soc 107:713–719 Auer NA (ed) (1982) Identification of larval fishes of the Flemer DA, Woolcott WW (1966) Food habits and dis- Great Lakes Basin with emphasis on the Lake Mich- tribution of the fishes of Tuckahoe Creek, Virginia, igan Drainage. Great Lakes Fisheries Commission, with special emphasis on the bluegill, Lepomis m. Ann Arbor, Michigan. Special Publication 82-3. 744 macrochirus Rafinesque. Chesapeake Sci 7:75–89 pp Fuller PL, Nico LC, Williams JD (1999) Nonindigenous Beveridge MCM, Begum M, Frerichs GM, Millar S (1989) fishes introduced into Inland Waters of the United The ingestion of bacteria in suspension by the tilapia States. American Fisheries Society, Special Publica- Oreochromis niloticus. Aquaculture 81:373–378 tion 27, Bethesda, Maryland 613 pp Birkett L, McIntyre AD (1971) Treatment and sorting of Gerking SD (1994) Feeding ecology of fish. Academic samples, pp 156–158. In: Holme NA, McIntyre AD Press, San Diego California 416 pp (eds) Methods for the study of marine Benthos, IBP Hendricks MK, Noble RL (1979) Feeding interactions of Handbook No. 16, Blackwell Scientific Publications, three planktivorous fishes in Trinidad Lake, Texas. Oxford. 344 pp Proc Annu Southeastern Conf Fish Wildlife Agencies Bland RG, Jaques HS (1978) How to know the insects, 3rd 33:324–330 edn. WCB McGraw-Hill, Boston, Massachuetts Holland-Bartels LE, Littlejohn SK, Huston ML (1990) A 409 pp guide to larval fishes of the Upper Mississippi River. Brusca RC, Brusca GJ (1990) Invertebrates, Sinauer U.S. Fish and Wildlife Service, LaCrosse, Wisconsin Associates, Inc., Sunderland, MA 922 pp 107 pp Carlton JT (2001) Introduced species in U.S. coastal Horn MH (1989) Biology of marine herbivorous fishes. waters: environmental impacts and management pri- Oceanogr Mar Biol Annu Rev 27:167–272 orities. Pew Oceans Commission, Arlington, VA, Huckins CJF (1997) Functional linkages among morphol- USA 28 pp ogy, feeding performance, diet, and competitive abil- Carr WES, Adams CA (1972) Food habits of juvenile ity in molluscivorous sunfish. Ecology 78:2401–2414 marine fishes: evidence of the cleaning habit in the Huckins CJF, Osenberg CW, Mittlebach GG (2000) Spe- leatherjacket, Oligoplites saurus, and the spottail cies introductions and their ecological consequences: pinfish, Diplodus holbrooki. U.S. Fish Bull 70:1111– an example with congeneric sunfish. Ecol Monogr 1120 10:612–625 Clarke KR (1993) Non-parametric multivariate analyses of Keast A (1985) The piscivore feeding guild of fishes in changes in community structure. Aus J Ecol 18:117– small freshwater ecosystems. Environ Biol Fishes 143 12:119–129 Clarke KR, Warwick RM (2001) Change in Marine Khallaf EA, Alne-na-ei AA (1987) Feeding ecology of Communities: an approach to statistical analysis and Oreochromis niloticus (Linnaeus) & Tilapia zillii interpretation, 2nd edn. PRIMER-E: Plymouth (Gervias) in a Nile canal. Hydrobiologia 146:57–62 Marine Lab., UK Lowe-McConnell RH (1987) Ecological studies of tropical Colle DE, Shireman JV, Manuel DK (1976) Age, fish communities. Cambridge University Press, Cam- growth and food habits of largemouth bass collected bridge 382 pp from a Louisiana coastal freshwater marsh. Proc McBay LG (1961) The biology of Tilapia nilotica Linna- Annu Southeastern Conf Fish Wildlife Agencies eus. Proc Annu Conf Southeastern Game Fish Comm 30:259–268 15:208–218 Costa-Pierce BA (2003) Rapid evolution of an established McCrary JK, van den Berghe EPEP, McKaye KR, Lopez feral tilapia (Oreochromis spp.): the need to incor- Perez LJ (2001) El cultivo de tilapias: una amenaza a porate invasion science into regulatory structures. las especies icticas natives en Nicaragua. Encuentro Biol Invas 5:71–84 33:9–19

123 Environ Biol Fish (2006) 76:283–301 301

McKaye KR, Ryan JD, Stauffer JR Jr, Lopez Perez LJ, cus in coastal Mississippi watersheds. Copeia Vega GI, van den Berghe EP (1995) African tilapia in 2004:842–849 Lake Nicaragua—ecosystem in transition. BioScience Richter H, Focken U, Becker K, Santiago CB, Afuang WB 45:406–411 (1999) Analysing the diel feeding patterns and daily McLane WM (1947–1948) The seasonal food of the ration of Nile tilapia, Oreochromis niloticus (L.), in largemouth black bass, Micropterus salmoides florid- Laguna de Bay, Phillippines. J Appl Ichthyol 15:165– anus (Lacepede), in the St. Johns River, Welaka, 170 Florida. The Quart J Florida Acad Sci 10:103–138 Robinson RL, Turner GF, Grimm AS, Pitcher TJ (1990) A Merritt RW, Cummins KW (eds) (1996) An introduction comparison of the ingestion rates of three tilapia to the aquatic insects of North America, 3rd edn. species fed on a small planktonic alga. J Fish Biol Kendall/Hunt Publishing Co., Dubuque, Iowa 862 pp 36:269–270 Moriarty CM, Moriarty DJW (1973a) The assimilation of Schaus MH, Vanni MJ (2000) Effects of gizzard shad on carbon from phytoplankton by two herbivorous fishes: phytoplankton and nutrient dynamics: role of sedi- Tilapia niloticus and Haplochromis nigripinnis. ment feeding and fish size. Ecology 81:1701–1729 J Zool, London 171:41–55 Schaus MH, Vanni MJ, Wissing TE, Bremigan MT, Moriarty CM, Moriarty DJW (1973b) Quantitative esti- Garvey JE, Stein RA, (1997) Nitrogen and phospho- mation of the daily ingestion of phytoplankton by rus excretion by detritivorous gizzard shad in a res- Tilapia nilotica and Haplochromis nigripinnis in Lake ervoir ecosystem. Limnol Oceanogr 42:1386–1397 George, Uganda. J Zool, London 171:15–23 Smith DL, Johnson KB (1996) A guide to marine coastal Moyle PB, Crain PK, Whitener K, Mount JF (2003) Alien plankton and marine invertebrate larvae, 2nd edn. fishes in natural streams: fish distribution, assemblage Kendall/Hunt Publishing Co., Dubuque, Iowa 211 pp structure, and conservation in the Cosumnes River, Smoot JC, Findlay RH (2000) Digestive enzyme and gut California, U.S.A. Environ Biol Fishes 68:143–162 surfactant activity of detritivorous gizzard shad Myrick CA (2002) Ecological impacts of escaped organ- (Dorosoma cepedianum). Can J Aquat Fish Sci isms. In: Tomasso JR (ed) Aquaculture and the 57:1113–1119 environment in the United States, U.S. Aquaculture Stevens CE, Hume I (1995) Comparative physiology of the Society, Baton Rouge, Louisiana, pp 225–245 vertebrate digestive system. (2nd edn), Cambridge Needham JG, Needham PR (1962) A guide to the study of University Press, Cambridge, U.K 400 pp fresh-water biology. Holden-Day, Inc., San Francisco, Trewavas E (1983) Tilapiine fishes of the genera Saroth- California 108 pp erodon, Oreochromis and Danakilia. British Museum Occhipinti-Ambrogi A, Savini D (2003) Biological inva- (Natural History), London 583 pp sions as a component of global change in stressed Traxler SL, Murphy B (1995) Experimental trophic ecol- marine ecosystems. Mar Pollut Bull 46:542–551 ogy of juvenile largemouth bass, Micropterus salmo- Occhipinti-Ambrogi A, Galil BS (2004) A uniform ter- ides, and blue tilapia, Oreochromis aureus. Environ minology on bioinvasions: a chimera or an operative Biol Fishes 42:201–211 tool? Mar Pollut Bull 49:688–694 Trexler JC, Loftus WF, Jordan F, Lorenz JJ, Chick JH, Odum WE (1970) Utilization of the direct frazing and Kobza RM (2000) Empirical assessment of fish plant detritus food chains by the striped mullet Mugil introductions in a subtropical wetland: an evaluation cephalus. In: Steele JH (eds) Marine food chains. of contrasting views. Biol Invas 2:265–277 University of California Press, Berkeley, California, VanderKooy KE, Rakocinski CF, Heard RW (2000) pp 222–240 Trophic relationships of three sunfishes (Lepomis Pennak RW (1978) Fresh-water invertebrates of the spp.) in an estuarine bayou. Estuaries 23:621–632 United States, 2nd edn. Wiley-Interscience Publ., Wootton RJ (1990) Ecology of teleost fishes. Chapman New York, New York 803 pp and Hall, Fish and Fisheries Series 1, London 404 pp Peterson MS, Slack WT, Woodley CM (2005) The occur- Zale AV (1987) Growth, survival, and foraging abilities of rence of non-indigenous Nile Tilapia, Oreochromis early life history of blue tilapia,Oreochromis aureus, niloticus (Linnaeus) in coastal Mississippi: ties to and largemouth bass, Micropterus salmoides. Environ aquaculture and thermal effluent. Wetlands 25:112– Biol Fishes 20:113–128 121 Zale AV, Gregory RW (1990) Food selection by early life Peterson MS, Slack WT, Brown-Peterson NJ, McDonald stages of blue tilapia, Oreochromis aureus, in Lake JL (2004) Reproduction in non-native environments: George, Florida: overlap with sympatric shad larvae. establishment of the Nile Tilapia Oreochromis niloti- Florida Sci 53:123–129

123