Piscivory by Non-Native Blue Tilapia (Oreochromis Aureus ) in Clark County, Nevada

UNLV Retrospective Theses & Dissertations

1-1-2007

Piscivory by non-native blue tilapia (Oreochromis aureus ) in Clark County, Nevada

Shawn C Goodchild University of Nevada, Las Vegas

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Repository Citation Goodchild, Shawn C, "Piscivory by non-native blue tilapia (Oreochromis aureus ) in Clark County, Nevada" (2007). UNLV Retrospective Theses & Dissertations. 2235. http://dx.doi.org/10.25669/sgam-v3b4

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This Thesis has been accepted for inclusion in UNLV Retrospective Theses & Dissertations by an authorized administrator of Digital Scholarship@UNLV. For more information, please contact [email protected]. PISCIVORY BY NON-NATIVE BLUE TILAPIA {OREOCHROMIS AUREUS) IN

CLARK COUNTY, NEVADA

Shawn C. Goodchild

Bachelor of Science Humboldt State University 1993

A thesis submitted in partial fulfillment of the requirements for the

Master of Science Degree in Environmental Science Department of Environmental Studies Greenspun College of Urban Affairs

Graduate College University of Nevada, Las Vegas December 2007

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Thesis Approval UNTV The Graduate College University of Nevada, Las Vegas

ft November 20;Q 7

The Thesis prepared by

SHAWN C. GOODCHILD

Entitled

PISCIVORY BY NON-NATIVE BLUE TILAPIA fOREOCHROMIS AUREUS)

IN CLARK COUNTY. NEVADA

is approved in partial fulfillment of the requirements for the degree of

M.S. ENVIRONMENTAL SCIENCE

Examination Committee Chat

Dean of the Graduate College

Ejjçmtinatforr^m^ttee Member

..i- Examinatiofn^ Committee Member

Graduate College Eaculty Representative

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

Piscivory by Non-native Blue Tilapia(Oreochromis aureus) in Clark County, Nevada

Shawn C. Goodchild

Dr. Shawn Gerstenberger, Committee Chair Associate Professor University of Nevada, Las Vegas

Fish communities that share an evolutionary history typieally have mechanisms to offset

impacts presented by other species. Fish, especially non-game species, which are

intermingled with non-native species for which they lack a shared history, are often

poorly adapted to offset these impacts. Non-native fish affect native fish through

predation, competition, displacement, and disease, affects which are often synergistic.

Native fish within the Muddy River system (Clark County, Nevada) experienced a

precipitous decline in numbers following an illegal introduetion of blue tilapia

{Oreochromis aureus) during the 1990’s. The purpose of this investigation was to

determine if tilapia were directly predating upon fish, which is a phenomenon not

substantially reported in scientific literature but possible, for example, due to

contemporary evolution. In addition, if piscivorous, various factors including gender,

health, size, and habitat were examined to ascertain influence over predation. This

information would inform management of the fisheries resources in the Muddy River and

throughout Southern Nevada. Tilapia were collected at both the Nevada Power Reid

111

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Gardner generating facility and the Muddy River, and stomach contents were

investigated. Blue tilapia were determined to be piscivorous, which was weakly related

to gender, habitat, and body length. Muddy River populations, which were

predominately male, more frequently had fish in their digestive systems than did tilapia

from the Reid Gardner ponds. Body condition of tilapia was not related to piscivory.

Due to the weakness of the relationships, additional study is warranted, including

information on other habitat variables. This investigation underscores the importance of

a tilapia removal program for waters in Southern Nevada. A management plan and

invasion framework was proposed to address the problem.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS

ABSTRACT...... iii

LIST OF FIGURES...... vii

ACKNOWLEDGEMENTS...... viii

CHAPTER 1 DITRODUCTION...... 1 History of Tilapia in Nevada...... 5 Purpose of the Study...... 6

CHAPTER 2 LITERATURE REVIEW...... 7 Overview of Effects of Non-native Fish ...... 7 Predation...... 7 Competition...... 11 Displacement...... 12 Parasites...... 12 Combination of Effects ...... 13 Reported Effects of Tilapia...... 14 Tilapia Life History...... 16 Taxonomy ...... 16 Tilapia Distribution...... 18 Ecology of Tilapia...... 19 Tilapia Anatomy Related to Feeding...... 22 Gut Morphology...... 22 Other Factors Affecting Anatomy ...... 23 Gender...... 23 Water Chemistry and Morphology ...... 24 Tilapia Dietary Considerations...... 25 Natural Diet of Tilapia...... 26 Effects of Temperature on Diet...... 26 Effects of Diet on Tilapia...... 27 Dietary Requirements and Their Importance...... 28 Body Size and Energetics ...... 28 Protein...... 30 Lipids and Carbohydrates ...... 33 Other Nutrients, Vitamins, and Minerals...... 35 Dietary Plasticity ...... 36 Food Quality and Availability ...... 37 Camivory in Tilapia...... 38

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Habitat Characteristics and Alternative Foods ...... 40 CHAPTER 3 METHODS AND MATERIALS...... 42 Site Description...... 43 Sample Acquisition...... 44 Sample Preservation and Processing...... 46 Measurements...... 47 Analysis of Data ...... 47

CHAPTER 4 RESULTS...... 50 Hypothesis 1 Piscivory by Tilapia ...... 50 Hypothesis 2 Influence of Gender on Piscivory...... 50 Hypothesis 3 Influence of Size on Piscivory...... 52 Hypothesis 4 Influence of Fitness on Piscivory...... 53 Hypothesis 5 Influence of Lentic and Lotie Environments on Piscivory ...... 53

CHAPTER 5 DISCUSSION...... 55 Hypothesis 1 Piscivory by Tilapia ...... 55 Hypothesis 2 Influence of Gender on Piscivory...... 60 Hypothesis 3 Influence of Size on Piscivory...... 63 Hypothesis 4 Influence of Fitness on Piscivory...... 66 Hypothesis 5 Influence of Lentic and Lotie Environments on Piscivory ...... 68 Conclusion...... 69

APPENDIX A INVASION AND MANAGEMENT FRAMEWORK...... 71 APPENDIX B NEVADA TILAPIA MANAGEMENT PLAN...... 77

LITERATURE CITED...... 82

VITA...... 106

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES

Table 1 Countries with blue tilapia'...... 20 Table 2 Mean total length of tilapia by habitat and gender ...... 65

Figure 1 Study area, Muddy River system, Clark County, Nevada ...... 1 Figure 2 Yearly population size of Moapa dace and Virgin River chub in the Warm Springs area of the Muddy River...... 2 Figure 3 Proportion of dietary items found in tilapia stomachs...... 51 Figure 4 Length differences of tilapia within lentic and lotie sites on the Muddy River and Reid Gardner generating station...... 54 Figure 5 Hypothetical change over time of key characteristics ...... 58 Figure 6 Hypothetical tilapia niche breadth in native habitat ...... 59 Figure 7 Hypothetical introduced tilapia niche breadth...... 60 Figure 8 Differences in frequeney of dietary items found in tilapia stomachs between genders at the Reid Gardner generating station and the Muddy River 61 Figure 9 Gender ratio of tilapia at each sampling site...... 63 Figure 10 Histograms of length frequency sorted by stomach content ...... 64 Figure 11 Fulton’s K of tilapia captured at Reid Gardner generating station...... 67

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGEMENTS

I would like to thank Nevada Power, Nevada Department of Wildlife, U.S. Geological

Survey - Biological Resources Discipline, and the U.S. Fish and Wildlife Service for

their assistance with the collection of data. I would also like to thank my committee with

their assistance in the project and development of this thesis, and my parents and family

for support.

vni

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 1

INTRODUCTION

Concurrent with an invasion of blue tilapia{Oreochromis aureus) (Actinopterygii:

Cichlidae) beginning in 1992, the native fishes of the upper Muddy River (Figure 1)

experienced a precipitous decline in numbers (Figure 2).

NEVADA UTAH

ARIZONA

M utlily Rjv«i M l 0 1 1 R iv e r

Figure 1 : Study area, Muddy River system, Clark County, Nevada.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Moapa Dace and Virgin River Chub Populations (Warm Springs, Muddy River, Clark County, Nevada)

9000

8000

7000 a I 6000

I 5000 — Dace "s I4000 I 3000

2000

1000

1994 1997 1999 2000 2001 2002 2003 2005 2007 Y e a r

Figure 2: Yearly population size of Moapa dace and Virgin River chub in the Warm Springs area of the Muddy River.

This included an endemic fish federally listed as endangered, the Moapa dace {Moapa

coriacea) (Actinopterygii: Cyprinidae), which by 1997, 75% of the entire world’s

population was extirpated. The rare Virgin River chub{Gila seminuda) (Actinopterygii:

Cyprinidae) was completely extirpated from the upper Muddy River during this invasion.

This decline was significant not only in that the Moapa dace and other native Muddy

River fish were nearly extirpated, but similar impacts may also occur to other species that

have economic or ecosystemic values where invasive fish are introduced. What remained

to be explored was the mechanism of the decline: Were tilapia causing ecosystem level

changes or affecting the native fish by direct predation. This study elucidated

relationships between the species by determining piscivory, and determined potential

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. factors important to the piscivory in order to help define solutions to guide management

of the non-native tilapia.

Non-native species present a serious threat to native ecosystems, and may radically

alter habitats and their associated biologic communities (Taylor et al. 1984; Elton 1958;

Zaret and Paine 1973; Fuller et al. 1999; Hickley 2004). Non-native fish have been

introduced into novel habitats for several reasons, including sport fishing management,

habitat or pest management, research, the aquarium hobby, aquaculture, and

unintentionally (Devoe 1992). Although a wide range of potential impacts with varying

severity may occur given introductions of exotic species (e.g. Gido et al. 2004, and

citations therein), established introduced populations of non-native fish and other aquatic

species present the probability of severe impacts to native fishes.

Behavior is subject to selective change (i.e. Alcock 1989). Species that have evolved

with fewer or different perturbations (were not exposed to these perturbations during their

evolutionary history) likely would not have evolved behaviors that minimize effects from

these novel perturbations, such as those caused to native species by introduced non-native

taxon (Meffe 1984; Hobbs and Mooney 1998; Gamradt and Kats 1996). Therefore, non

native fish in suitable habitats are typically able to displace, compete, transmit parasites,

and/or prey upon the native aquatic species with much more efficiency than species that

have a shared evolutionary history. In addition, non-native species may indirectly affect

other non-native species, such as affecting one species which influences a population of

another (i.e. removal of non-native largemouth bass increasing non-native crayfish

numbers in Japan) (Maezono and Miyashita 2004). These impacts generally decrease the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. fecundity of the native fish, and could result in decline of the native species’ population

depending on modifiers such as the environment or availability of resources.

Cox (2004) suggested that introduced species could rapidly evolve within novel

habitats to maximize fitness. Evolution in fishes could occur at a fast pace, and evolution

or hybridization may guide a lineage of fish to increase fitness (Streelman et al. 2004;

Hendry et al. 2000; Huey et al. 2000; Koskinen et al. 2002). For example, the

phenotypical and behavioral changed in Devils Hole pupfish(Cyprinodon diabolis)

(Actinopterygii: Cyprinodontidae) in artificial réfugiai habitats, where the pupfish grew

larger and are more territorial than they were within their native Devil’s Hole (Wilcox

2001). White Sands pupfish{Cyprinodon tularosa) have been shown to display adaptive

morphological variation in as little as 30 years (Collyer et al. 2005). In addition, an

introduced population of Red River pupfish{Cyprinodon rubrofluviatilis) had shown a

degree of divergence within the past 40 years based on differences of microsatellites

within mitochondrial DNA (Collyer 2004). This rapid evolution may be referred to as

contemporary evolution, or microevolution. Tilapia have also been demonstrated to

change phenotypically in introduced habitats (Barriga-Sosa et al. 2004). The

Pseudocrenilabrinid cichlid, Cynotilapia afra (Actinopterygii: Cichlidae), has been shown

to have diverged into a genetically distinct population after 20 years, and introduced fish

have been known to have evolved specific traits after 10-15 generations. Trajectories of

evolution may differ, as it has with Cynotilapia afra at differing locations within the

system where they have been introduced. Watters et al. (2003) suggest managing

phenotypic diversity, which is related to habitat characteristics of novel habitats such as

artificial refuges, which ultimately affects demographics and effective population size.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Non-native tilapia have been demonstrated to have some degree of piscivory in

habitats worldwide (i.e. Gindelberger 1981; Jimenez-Badillo and Nepita-Villanueva

2000; Scoppettone et al. 2004); however the vast majority of localities with published

dietary information do not include piscivory (e.g. Oguzie 1999; Maitipe and De Silva

1985; Spataru and Zorn 1978; Winemiller and Kelso-Winemiller 2003). One

evolutionary path that could change in a population is diet. It is possible that blue tilapia

have evolved fish eating behavior, or at least a propensity to satisfy nutrient requirements

with a slightly higher degree of piscivory, in the relatively few generations since the 1992

introduction. Another possibility is upon introduction the fish was able to exploit a wider

range of conditions than what it could have in its native habitat due to exclusion by more

niche-specialist organisms. For example, tilapia in other environments could not compete

as predators, since there were other species present that were more efficient at predation.

History of Tilapia in Nevada

Based on Nevada Department of Wildlife (NDOW) and U.S. Fish and Wildlife

Service (USFWS) records, blue tilapia were first discovered in the middle Muddy River

of southern Nevada during 1992, which was a result of an illegal introduction. By 1996,

tilapia had spread throughout the Muddy River, including the warm springs at the

headwaters. In 1994, tilapia were captured in the Virgin and Temple basins of Lake

Mead, Mohave County, Arizona, and have since been captured by NDOW throughout

Lake Mead (Jim Heinrich, NDOW, personal communication). Surveys by Federal and

State natural resource agencies for woundfin(Plagopterus argentissimus)

(Actinopterygii: Cyprinidae) on July 26, 2001, detected the presence of young-of-year

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. tilapia within the Virgin River from below the Bunkerville Irrigation Diversion

(Mesquite, Clark County, Nevada) to Halfway Wash (River Mile 42). This implied that

adult tilapia were present and had spawned in the Virgin River (Jim Heinrich, NDOW,

personal communication). This was the first time tilapia were collected in the Virgin

River. Staging young-of-year blue tilapia were collected at the mouth of the Virgin River

during July 2004, which suggested that this species could migrate upstream upon

connection with Lake Mead (Mike Golden, BIO/WEST, personal communication). As of

July 2007, drought conditions had prevented connections of the mainstem Virgin River to

Lake Mead, thereby preventing tilapia from moving upstream.

Purpose of Study

Surveys in the upper Muddy River, Clark County, Nevada, correlated the presence of

blue tilapia, a species illegally introduced during 1992, to a drastic decline in the number

of the endangered Moapa dace. Virgin River chub and Moapa White River springfish

(Crenichthys baileyi moapae) (Actinopterygii; Goodeidae) (Scoppettone 1998). The

decreased numbers of native fish suggested that tilapia in some way have increased

mortality of native fish, either through predation or other factors. Piscivory in typical

diets of blue tilapia has been relatively unreported in the scientific literature.

Accordingly, piscivory of blue tilapia in southern Nevada have been investigated in this

thesis.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 2

LITERATURE REVIEW

Overview of Effects of Non-native Fish

Non-native fish can eliminate native fish populations (Elton 1958), typically through

multiple pathways (Dunham et al. 2004). For example, introduction of the Nile perch

{Lates niloticus) (Actinopterygii; Latidae) caused the extinction of 150-200 species of

endemic fish in Lake Victoria, Africa (37%-50% of the total species within the lake)

(Kitchell et al. 1997; Lowe-McConnell 1993). Unfortunately, there are many examples of

species, population, and/or community extirpation, which are supported by a vast amount

of literature. Among other impacts (i.e. hybridism, which is not an issue relative to this

thesis), non-native species may influence populations of native species through predation,

competition, displacement in living space, or by being vectors for parasites (e.g. Mack et

al. 2000). Often, several of these influences are synergistic and originate from multiple

non-native species that occur in systems. In addition, anthropogenic disturbance often

increases the damage to populations of native species from exotic organisms (e.g. Byers

2002).

Predation

Predation is the most direct and dramatic method where non-natives affect native

organisms. Predators increase their fitness by preying selectively on organisms that

Reproduced witfi permission oftfie copyrigfit owner. Furtfier reproduction profiibited witfiout permission. maximize energy intake over output (Brooks and Dodson 1965; Didonato and Lodge

1993; Ogle et al. 1996). In many cases, native fish unaccustomed to predation are the

easiest prey, since predator avoidance is an adaptive trait (Reebs 1999) and native fish

typically do not have the shared history which facilitates the evolution of this avoidance.

By focusing on easier prey, predators maximize the efficiency of their foraging (Case

1996).

Fish have a variety of techniques to avoid predation, ranging from escape behavior to

cryptic coloration and spines. Chemical cues may also be involved, such as with certain

tetras (Actinopterygii: Characidae) that hide if subjected to chemical stimuli representing

a familiar predator (Moraes et al. 2004). Not all fish generate the same response. If

presented with an unfamiliar predator stimulus, these tetras do not show as dramatic of an

avoidance response. In addition, Magurran (1990) demonstrated that guppies{Poecilia

reticulata) (Actinopterygii: Poeciliidae) are unable to avoid novel predators as efficiently

as predators with which they have evolved.

Predatory fish are often stocked as game fish with no long-term ill effects to other fish

populations, but the other fish in the stocked habitat are often non-native and have shared

evolutionary histories. The basis of traditional game fish management is developing the

ideal predator-prey relationship to maximize numbers and/or size of game fish in a

system. Habitats within southern Nevada that are affected by non-natives are typically

small and/or structurally simple, which facilitates predation (e.g. Crowder and Cooper

1982; Baras and Jobling 2002). Most of the introduced predators are unfamiliar to the

native fish, and would not likely induce a significant avoidance response that a prey

species would have developed while coevolving with a predator (Huntingford and Wright

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1992). Given limited shared history as well as limited areas for prey shelter, predators

introduced into Nevada springs are typically extremely efficient in detecting and

consuming native fishes.

Predatory fish have had substantial impacts within southern Nevada. During the

winter of 2003/2004, introduced largemouth bass {Micropterus salmoides)

(Actinopterygii: Centrarchidae) completely eradicated through predation all native fish

from the Big Springs outflow, Nye County, Nevada, including two federally endangered

fish, the Ash Meadows Amargosa pupfish{Cyprinodon mionectes nevadensis) and the

Ash Meadows speckled dace {Rhinichthys osculus nevadensis) (Actinopterygii:

Cyprinidae) (USFWS 2003 - 2007). The pupfish and dace did not evolve with predacious

fish, as did non-native Poeciliids that share the same habit, the sailfin molly {Poecilia

latipinna) and mosquitofish {Gambusia affinis) (Actinopterygii: Poeciliidae). These

Poeciliids had a shared evolutionary history with centrarchids, and maintained low

populations in spite of predation. Predation could affect native species in multiple

fashions. In Lake Mohave, non-native channel catfish {Ictalurus punctatus)

(Actinopterygii: Ictaluridae) and common carp{Cyprinus carpio) (Actinopterygii:

Cyprinidae) have been shown to prey on eggs of the endangered razorback sucker

{Xyrauchen texanus), and sunfish {Lepomis sp.) (Actinopterygii: Centrarchidae) prey on

larval razorback sucker (Minckley 1983). This predation was enhanced by the relatively

simple structure and lack of turbidity, the only structure being within cobble that was also

occupied by small sunfish. As a result of the large populations of small sunfish, no

juvenile razorback suckers have been detected and the population of suckers consists

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. solely of aged adults, which likely had a low rate of mortality from predation due to their

large size but did not successfully recruit to the population (Minckley 1983).

Throughout the world, there have been multiple examples of negative predatory

interactions between natives and introduced non-native fish. Green sunfish {Lepomis

cyanellus) in Sabino Creek, near Tucson, Arizona, completely eliminated through

predation all small Gila chub {Gila intermedia) from portions of the creek where they

came into contact, and the only Gila chuh present in reaches with green sunfish were few

large adults recruited from upstream reaches without green sunfish. (Dudley and Matter

2000). It is likely that the non-native crayfish {Procambarus clarkii) (Decapoda:

Cambaridae) also affected the chub by eating their eggs. White and Harvey (2001)

suggested that predation by the introduced Sacramento pikeminnow {Ptychocheilus

grandis) (Actinopterygii: Cyprinidae) caused a dramatic decline of sculpin{Coitus sp.)

(Actinopterygii: Cottidae) in California’s Eel River. This decline was enhanced by the

migratory nature of sculpin, which migrated through preferred pikeminnow habitat. In

New Zealand, Townsend and Crowl (1991) demonstrated that non-native brown trout

{Salmo trutta) (Actinopterygii: Salmonidae) eliminated the common river galaxias

{Galaxias vulgaris) (Actinopterygii: Osmeriformes) from all habitats accessible by the

trout, which further illustrated the drastic affect introduced predators could have on native

species. Predation during some life stage of a developing fish is a common practice;

therefore, one life stage of an introduced fish may have a predatory impact and others

may not. Cannibalism is common in larval or juvenile fishes, including fish that do not

typically include meat in their diets, as it increases the fitness of the developing young

(Sakakura and Tsukamoto 2002; Smith and Reay 1991).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Competition

Non-native species have the ability to rapidly alter populations of native species, yet

they could also affect populations in slower, less conspicuous ways that are often

synergistic. Predation on one species may decrease competition for a resource and

enhance another species (Wilbur et al. 1983), which greater numbers of that species

increase net competition against the native fish. For example, predation on pupfish

{Cyprinodon sp.) may increase numbers of sailfin mollies within a system, since mollies

are more difficult to capture and overlap dietarily with pupfish (Scoppettone et al. 1995).

The increased proportion of mollies would then have a greater impact on food items and

force the remaining pupfish to expend more energy to obtain food. In addition to

Gambusia described by Meffe (1985), competitory effects have been shown between blue

tilapia and Florida flagfish {Jordanella floridae) (Actinopterygii: Cyprinodontidae),

where flagfish were eradicated from experimental ponds due to loss of a food source that

was more efficiently exploited by tilapia (Blakesley 1975). Desert pupfish {Cyprinodon

macularis) have been extirpated from several sites in the Salton Sea due to competition

with Tilapia zilli (Actinopterygii: Cichlidae) and sailfin mollies (Schoenherr 1981).

Gophen et al. (1983) determined that after their introduction in an Israeli lake, blue tilapia

depressed populations of St. Peter’s fish{Sarotherodon galilaeus) (Actinopterygii:

Cichlidae), another species of tilapia, through competition for plankton. Zale (1987a)

found that blue tilapia would likely outcompete largemouth bass in early life stages if

zooplankton were limiting. Introduced blue tilapia have also been demonstrated to

completely outcompeteCichlasoma istlanum (Actinopterygii: Cichlidae) within a

reservoir (Rosas 1976).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Displacement

Exotic fish may displace native species, either spatially or behaviorally, to habitats of

poorer quality. Crowder and Cooper (1982) noted that predators alter habitat selectivity

of prey, causing prey to be selective of habitats that are more structurally complex.

Schlosser (1988) demonstrated that prey selected habitat that decreased probability of

predation, which limited the ability of the prey to fully utilize available habitat. This may

create avoidance behavior that forces fish into marginal habitats, which would lower

fecundity. Townsend and Crowl (1991) suggested that besides predation, brown trout

also competed with and displaced the common river galaxias. Aggression in fish is

commonplace, and could be either inter-specific or intra-specific. Aggression is usually

intended to prevent another individual from utilizing resources, such as space, mates, or

food sources, available to the aggressor (Alcock 1989; Sakakura and Tsukamoto 2002;

Smith and Reay 1991). Aggression in cichlids (Cichlidae) (both inter- and intra-

specifically) is well known in the aquarium trade, and tilapia have been shown to be

aggressive intraspecifically (Giaquinto and Volpato 1997). This aggression typically

displaces the subordinate fish to marginal habitats, which reduces feeding efficiency and

other activities. Blue tilapia, a lek-breeding species, display substantial aggression

between males during spawning, and females defend territories to guard against predation

of fry (Al-Mohsen 1998). All of these behaviors affect other species of fish, causing

avoidance behavior and exclusion of native fish from defended habitats.

Parasites

Non-native aquatic species may also be vectors for non-native parasites, such as

Asian tapeworm (Bothriocephalus acheilognathi) (Cestoda: Pseudophyllidea), which was

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. likely introduced into Southern Nevada from shipments of baitfish (Deacon 1988). Other

non-native parasites that have been introduced to native systems include white spot

disease {Ichthyophthirius sp.) (Ciliata: Ichthyophthiriidae) and anchorworm {Lernea sp.)

(Maxillopoda: Lemaedae), which represent potential threats to populations of native fish

(Warburton et al. 2002). Non-native parasites and disease could drastically alter native

populations, as demonstrated by the crayfish fungus(Aphanomyces astaci)

(Phycomycota: Saprolegniacea) introduced into Europe along with resistant North

American species, which caused severe declines of native European crayfish (Alderman

et al. 1983). In addition, some parasites may alter behavior of host species, such as

making the fish lethargic or less apt to avoid predators. In some species, this an

adaptation of the parasite to increase the probability of transmission of the parasite

between hosts, but in others it is a manifestation of a physical obstruction by the parasite.

Parasites can have serious negative consequences to non-target host species. For

example, some species of the gill flukeGyrodactylus (Trematoda: Gyrodactylidae) have

been shown to be more pathenogenic if infecting a species of fish that is not its primary

host (e.g. Peeler et al. 2004).

Combination of Effects

Compensatory or synergistic adverse impacts from non-native species are typically

the rule, such as documented with the introductions of mosquitofish in Arizona, which, in

combination with habitat alteration, completely extirpated Gila topminnows (Poeciliopsis

occidentalis) (Actinopterygii: Poeciliidae) in common habitats through competition and

predation of larval fish (Meffe 1985; McNatt 1979). Predation has a variety of effects

upon prey populations, and prey populations could be changed behaviorally as well as

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. displaced either temporally or spatially due to predation (Fraser and Cerri 1982, and

citations therein). For example. Light (2005) found non-native signal crayfish

{Pacifastacus leniusculus) (Decapoda: Astacidae) changed the behavior of the native

Paiute sculpin(Cottus beldingi), affecting habitat use, predatory risk, and foraging

success. This was facilitated by the dominance of crayfish in non-embedded substrate

that both species used for cover, which forced the sculpin out in marginal habitats.

Reported Effects of Tilapia

Tilapia have been shown to create a wide range of impacts to the ecosystem;

However, the bulk of the scientific literature suggests that this is predominately through

displacement and competition. Oreochromis, and other members of the Tilapinii, are

generalists that have the ability to rapidly colonize and dominate novel or seasonally-

disturbed habitats (Fryer and lies 1969; Merron, et al., 1993; De longh and Van Zon

1993) and cause wide-ranging changes to macrophyte and plankton populations (e.g.

Wager 1968). Blue tilapia have been heralded as a biological control tool to remove

nuisance aquatic vegetation from waterways (Schwartz et al. 1986), and a population of

introduced tilapia has the ability to become up to 90% of the biomass in a system (Faunce

and Papemo 1999). In essence, this leaves 10% of the system consisting of all other

forms of biomass, including plankton, vegetation, detritus, other fish, and invertebrates.

This efficient utilization of a system’s energy complements the use of tilapia as an

aquaculture species. Grazers have been shown to influence environmental stoichiometry

(Evans-White and Lamberti 2005), and tilapia likely have far-reaching impacts to system

chemistry that are not fully understood.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Zooplankton, an important food source for a wide variety of fish, could be negatively

impacted by non-native planktivores, such as tilapia (Drenner et al. 1984; Lehman and

Caceres 1993; Novales-Flamarique et al. 1993). Zale (1987a), and Shafland and Pestrak

(1983), described the reduction of largemouth bass production, survival, and growth due

to an introduction of blue tilapia. Gophen et al (1983) suggested that blue tilapia have

caused a dramatic decline in St. Peter’s Fish, creating a large economic drain on nearby

fishing communities. Intraspecific competition also occurs in tilapia, and juvenile tilapia

are detrimental to the growth of adults in cultured situations due to competition for feed.

Drenner (1987) and Drenner et al. (1982) demonstrated the ability of filter-feeding tilapia

to suppress large planktonic algae and animals in a lake, but increase densities of smaller

organisms that would travel through either the filtering mouthparts or the gut. This

allowed smaller organisms resistant to digestive processes to utilize nutrients within the

tilapia gut and better compete for nutrients in a water body. These studies also

demonstrated that zooplankton abundance was a negative function of fish density, where

having more fish in the lake decreased the abundance of the larger zooplankton. Vinyard

et al (1988) demonstrated that feeding rate of tilapia influenced populations of rotifers

and crustaceans, and feeding rate increased with particle size.

Tilapia have also been shown to have impacts elsewhere in the world. Introduced

Tilapia and Oreochromis have displaced native Madagascarian cichlids, resulting in their

endangerment (Vences et al. 2001). Sarotherodon introduced into the Philippines rapidly

increased in numbers and caused the local extirpation of the goby Mistichthys luzonensis

(Actinopterygii: Gobiidae) due to competition and predation (Gindelberger 1981), and

tilapia introduced to islands in Micronesia and the South Pacific, have damaged mullet

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Valamugil sp., Liza sp., and Chelon sp.)(Actinopterygii: Mugilidae), bonefish (Albula

sp.)( Actinopterygii : Albulidae), and milkfish (Chanos chanos) (Actinopterygii: Chanidae)

production (Nelson and Eldredge 1991).

Aquatic submergent macrophytes, such as eelgrass(Valisneria sp.), could be

repressed by tilapia grazing, as has been demonstrated in the Muddy River (Goodchild

personal observation; Gary Scoppettone, U.S. Geological Survey - Biological Resources

Discipline (USGS), personal communication). Upon elimination of tilapia in a tributary

of the Muddy River, eelgrass quickly returned and dominated the mud substrate,

suggesting that roots and rhizomes are not dug up and consumed by the fish. In many

systems, macrophytes provide a major source of cover for native fish, Avhich is especially

important during young life stages. Removal of macrophytes would cause reduction of

cover and a resultant increase in the risk of predation on species dependant on that cover.

Although tilapia provide critical protein to humans worldwide, in almost all instances

where the ecology of the habitat where they were introduced has been studied, tilapia

have been detrimental to native species through competition, displacement, or rarely,

predation. It is likely that introduced tilapia within the Muddy and Virgin River systems,

as well as in other waters of the Southwestern United States, would negatively affect the

native fish through these pathways.

Tilapia Life History

Taxonomv [Adapted from Trewavas (198311

The teleost blue tilapia is classified within the subfamily Tilapiinae (Tilapias), which

are members of the family Cichlidae (Cichlids), the order Perciformes (Perches and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Cichlids), and the Class Actinopterygii (Ray-finned fishes). There are ten members of the

Tilapiinae (Tribe Tilapiini), which are very similar in form and diet, and are differentiated

from other cichlids by skull morphology.

Historically, tilapiines that were considered vegetarian or planktivorous, shared

specific spine and skull morphologies, and shared chromosomal characteristics, were

considered one genus, Tilapia. Blue tilapia were considered a form of the Nile tilapia

{Tilapia niloticus), until split toT. aureus in 1962 (Spataru and Zorn 1978). This genus

was later split into three genera: Tilapia, Sarotherodon, and Oreochromis (Thys Van Den

Audenaerde 1968; Trewavas and citations therein 1983). Oreochromis and Sarotherodon

share similar traits, such as adaptations for filter feeding. These include a large

buccopharyngeal cavity shaped by a broad skull, long and similar numbers of gill rakers,

similar dentition, and elongated lower pharyngeal bones. The diets of Oreochromis and

Sarotherodon are considered or described as mdiwly Aufwuchs and plankton, whereas the

diet of Tilapia is predominately macrophytes. In addition, Tilapia form redds and are

substrate brooders, whereas Oreochromis are mouthbrooders, and redds only serve as a

site for courtship and laying eggs. These two genus names have been used

interchangeably by multiple authors. For example, the Nile tilapia is named either

Oreochromis or Sarotherodon, depending on the author’s school of thought. The

American Fisheries Society published accepted names for the United States, and

considers blue tilapia to be Oreochromis (Robins et al 1991).

Although some authors considerOreochromis a type of Sarotherodon, Oreochromis

differs from Sarotherodon by development of the genital papillae, ventral scale size and

overlap, and proportional testes weight. Oreochromis also is sexually dimorphic and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. dichromatic at spawning, whereas Sarotherodon is not. In addition, Sarotherodon are

typically biparental, whereas Oreochromis are maternal mouthbrooders (Pouyaud and

Agnese 1995). Further subdivision within Oreochromis is composed of five subgenus

and fifteen species, many which readily hybridize (Pinto and citations therein 1982). All

of these species share similar dental and skull morphology, as well as comparable

numbers of gill rakers and microbranchiospines: All characteristics that in part dictate

feeding strategies. Not surprisingly, dietary overlap is substantial amongst the tilapiines

(Winemiller and Kelso-Winemiller 2003), and Oreochromis diets are nearly identical

within the genus, allowing assumptions to be made utilizing surrogate species within the

genus. For the purpose of this thesis, tilapia and blue tilapia refer Oreochromisto aureus,

whereas Tilapia refers to the genus Tilapia. When referenced, the original name used by

the author(s) is used.

Tilapia Distribution

Source of stock from where the fish had naturalized could influence the food

consumption rates, metabolism, and growth. For example, walleye {Sander vitreus)

(Actinopterygii: Percidae) range from Arkansas to Canada, and show differences in these

characteristics depending on latitude (Galarowicz and Wahl 2003). Although tilapia are

warm water species and have been genetically modified by humans, their native location

likely has some bearing on their utilization of resources in stocked locations.

The tribe Tilapiini are riverine and lake fish (Fryer and lies 1972) that occur

throughout the fresh and brackish waters of African and Eastern Mediterranean

(Levantine) countries. Blue tilapia historically was also an African and Levantine fish,

occurring in the Senegal (Guinea, Mali, Mauritania, and Senegal), the Niger and Benue

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Cameroon, Mali and Nigeria), Shari (Central African Republic and Chad), Logone

(Cameroon and Chad), Na’Amen (Israel), Yarkon (Israel) and the Jordan (Jordan) River

basins, the Nile (Egypt and Sudan), and Lake Chad (Niger, Nigeria, Cameroon, Chad).

These basins incorporate a majority of equatorial tropical Africa, from West Africa

northeast to Israel and Jordan (Trewavas 1983). The type locality occurs in Senegal

(Trewavas 1966). All three tilapia genera were represented during the Miocene (Stewart

2001), and likely dispersed to the Levant during the Pliocene (Wemer and Mokady 2004).

Tilapia fossils have been dated to the Oligocene in Arabia (Chackrabarty 2004),

suggesting they were present during a pluvial period.

Knowledge of historical blue tilapia distribution has been confounded by its

anthropogenic distribution as a food fish, as well as structural similarities with Nile

tilapia {Oreochromis niloticd) and hybridization with other species (Trewavas 1983).

This species has initially been introduced primarily as a food fish throughout Africa and

the Middle East, as well as Florida in the United States (Trewavas 1983). Since

introduction to the United States, it has been introduced to twelve states (Fuller et al.

1999), and various production forms or hybrids of blue tilapia have been utilized by

aquaculture throughout the southern United States (Chapman 2000), Central America

(Jimenez-Badillo and Nepita-Villanueva 2000), the Caribbean, South America, and Asia

(Engle 1997) (Table 1).

Ecologv of Tilapia

Oreochromis and Sarotherodon evolved in large rivers, lakes, and estuaries. Blue

tilapia are potamodromous (migrate within rivers), and could cyclically migrate within

watersheds over one hundred kilometers per year depending on flood cycles and seasons.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Country Status Reference Antigua Barbados introduced (Lever 1996) Bahamas introduced (Chakallal 1993) Brazil introduced (Wellcome 1988) Cameroon native (Vivien 1991) Chad native (Trewavas 1983) China (Mainland) introduced (Wellcome 1988) Costa Rica introduced (FAQ 2002) Cote d'Ivoire introduced (Lever 1996) Cuba introduced (Wellcome 1988) Cypms introduced (Wellcome 1988) Dominica introduced (FAO 1997) Dominican Republic introduced (Lever 1996) Egypt native (Falk et al. 1998) El Salvador introduced (Wellcome 1988) French Polynesia introduced (FAO 2002) Guatemala introduced (Wellcome 1988) Haiti introduced (Lever 1996) Israel native (Trewavas 1983) Japan introduced (Wellcome 1988) Jordan native (Trewavas 1983) Kuwait introduced (Suresh and Lin 1992) Mali native (Trewavas 1983) Mexico introduced (Lyons et al. 1998) Netherlands Antilles introduced (Chakallal 1993) Nicaragua introduced (Wellcome 1988) Niger native (Trewavas 1983) Nigeria native (Olaosebikan and Raji 1998) Pakistan introduced (Mirza 2002) Panama introduced (Wellcome 1988) Peru introduced (Wellcome 1988) Philippines introduced (Mercene 1997) Puerto Rico introduced (Lee et al. 1983) Russian Federation introduced (Bogutskaya and Naseka 2002) Saudi Arabia native (Siddiqui and Al-Harbi 1995) Senegal native (Trewavas 1983) Singapore introduced (Ng et al. 1993) South Africa introduced (Wellcome 1988) Syria introduced (Goad 1996) Taiwan introduced (Wellcome 1988) Thailand introduced (Wellcome 1988) Turkey introduced (Innal and Erk'akan 2006) Uganda introduced (Wohharth and Hulata 1983) United Arab Emirates introduced (FAO 1997) USA introduced (Wellcome 1988) Zambia introduced (Thys Van Den Audenaerde 1994)

Table 1 ; Countries with Populations of Blue Tilapia (Froese and Pauly 2007)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Tilapia have the ability to grow and mature quickly. Schramm and Zale (1985) suggest

that this fast growth is to compensate for predation. Growth and performance of tilapia

are variable and differs depending on strain (e.g. Osure and Phelps 2006). Tilapia are

able to breed monthly and may reach sexual maturity in as little as 2 months or at 6

centimeters (Lee and Newman 1992; Brummett 1995). James and Bruton (1992) found

that in specific conditions, blue tilapia could become sexually mature at 35 millimeters

total length. Blue tilapia are an episodic (Fessehaye 2006) lek-breeding species

(Fishelson 1983) that show predictable spawning behavior due to time of day (Marshall

and Bielic 1996). Being mouth brooders, after spawning the female takes up the eggs

from the redd, departs, and establishes a territory to raise her young. Tilapia are

generalists, and could withstand a wide variety of environmental conditions. As tilapia

are warm water fish, optimum breeding temperature is between 24-29 degrees Celsius

(C°) (Egna and Boyd 1997). Zale (1987b) suggests that blue tilapia utilize habitats in part

based on temperature. Several studies have investigated temperature minima for tilapia.

Kindle and Whitmore (1986) determined that blue tilapia began to show stress between

eleven C° to twelve C°, and Shafland and Pestrack (1982) determined that they died

between six C° and seven C°. Swimming performance is poorer in cool waters, thus in

habitats with very low levels of dissolved oxygen, including warm water that has

diminished oxygen content. For example, Lee and Newman (1992) describe tilapia

withstanding oxygen levels as low as one mg/L. Blue tilapia are also able to compensate

for the suffocating effects of hypoxia or rotenone by air breathing by lying on or wedging

themselves within floating vegetation and relying on surface oxygen for an extended

period of time (Shawn Goodchild, Personal Observation).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Tilapia Anatomy Relative to Feeding

Compared to other members of the Tilapiinae and Cichlidae, the members of the

genus Oreochromis and Sarotherodon have morphological characteristics that form an

enlarged buccopharyngeal cavity that facilitates filter-feeding (Drenner et al. 1987).

Essentially, the fish expands its buccopharyngeal cavity, which sucks water and food

items into it through the mouth. It then contracts the cavity, where the mixture of water

and food is sent through a network of gill rakers and microbranchial spines, and out

through the opercular opening (Drenner et al. 1987). The mucous within this network

entraps food particles, which are then consumed. Due to this similarity, all members of

Oreochromis, and to a lesser but notable degree Sarotherodon, have similar dietary traits.

Both genuses primarily forage on phytoplankton and zooplankton, with detritus and

epiphytes associated with detritus, as a secondary part of their diet. It has been

hypothesized that this has been a result of parallel evolution between the two genus

(Trewavas 1983), or possibly the two genus diverged only recently. Tilapia are able to

detect essential amino acids by taste (smell), and could selectively forage at areas rich in

these amino acids (Yacoob et al. 2001). Gape size also affects feeding by limiting the

size of the food particle ingested, and Neil (1964) determined that in captivity Nile tilapia

were able to consume conspecifics 1/5 of their total length.

Gut Morphology

Gut length of fish reflects their diet. Fish that consume vegetative materials typically

have longer intestines and more pyloric ceca than carnivorous fish, which is due to the

need for greater surface area and residency time to digest cellulose (Walker 1987). The

tilapiinae have gut lengths that range from seven to fourteen times their total body length

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Trewavas 1983). Female Oreochromis aureus had shorter intestines than males (Wille

et al. 2002), which suggests increased vegetative processing efficiency by males. The

first quarter of the intestine is used to digest protein, and the remainder is for digestion of

non-protein amino acids found in detritus (Bowen 1980), as well as other material. Since

it is also critical for females to grow, it does not make evolutionary sense that they do not

have equal intestinal lengths unless their diet is different, is composed of other items

other than solely vegetarian, and they have adapted unique gut morphology to take

advantage of a slightly different niche than the males (resource partitioning).

Physiology may also vary. For example, Tilapia {Oreochromis) mossambica have

been demonstrated to lower the pH (increase the acidity) in their stomach to digest cell

walls found in detritus (Bowen 1981). It is logical that this adaptation is prevalent

throughout theOreochromis and Sarotherodon, and is useful for digesting macrophytes

and algae.

Other Factors Affecting Anatomy

Gender

The gender of a fish has dramatic effects upon the energetics of the individual. The

most obvious cause of the difference between male and female fish energy budgets is

reproduction. Females produce eggs, which are much more energetically demanding than

sperm. This requires the female to utilize more protein, lipids, and other nutrients for egg

production instead of growth. Males grow faster not only due to biological or

environmental factors, but also due to genetic characteristics (Egna and Boyd 1997;

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Siddiqui et al 1997; Fryer and Iles 1972). Maies are able to better utilize protein than

females, which is a desirable trait for aquaculture.

Other gender differences occur in tilapia. Male fish are able to respond to stress more

effectively (such as during temperature minima tests) and have longer life spans, which is

likely an outcome of energetic differences (Hodgekiss and Hanson 1978; De Silva and

Chandrasoma 1980). Aggression and social hierarchy (McGinty 1985; Van Dam and

Penning de Vries 1995) also affects growth of tilapia, as dominant fish do not need to

expend as much energy to establish dominance (only to maintain dominance), and could

expend energy mainly for growth. Small, low-ranking tilapia are therefore the ones most

likely to experience nutrient deficiencies.

Water Chemistry and Morphology

Water chemistry plays a critical role in tilapia morphology. Intraspecific tilapia

anatomy can vary depending on water chemistry and biological characteristics of the

environment. Oreochromis have a wide niche breadth incorporating several foraging

strategies, and have been documented to have varied morphology depending on presence

of other members of the genus (Thys Van Den Audenaerde 1968). One example of

anatomy (and behavior) varying with environment is with Oreochromis mossambica,

which has been shown to have precocial life history traits in reservoirs with abundant

food, but in poor-quality habitats are more altricial (Arthington and Milton 1986).

Conditions for feeding, breeding, and refuge have been demonstrated by James and

Bruton (1992) to cause plasticity in age of maturity, length of spawning season, spawning

frequency, clutch size, and nesting behavior. Thermal and alkaline springs that arise

within the Great Rift Valley of Africa contain distinct forms of Oreochromis, primarily

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Oreochromis niloticus, of which the forms are considered subspecies. Compared to the

parent species, these subspecies typically have less gill rakers, and are a smaller size at

sexual maturity and adulthood. They also have smaller ventral scales, lesser number of

vertebrae, and a lesser number of fin rays. Reduced ventral scales are considered

adaptations to their epiphytic feeding (Thys Van Den Audenaerde 1968). All of these

adaptations have occurred through a considerable time of shared existence in a body of

water, and are likely designed to exploit varied niches to reduce competition. Fish size (a

factor of the environment) affects body composition of the offspring. Miliou and

Papoutsoglou (1997) found smaller females had progeny with higher protein and lower

fat carcass content than did larger females. Therefore, since the environment affects

morphology, the environment also has an indirect effect on dietary requirements.

Tilapia Dietary Considerations

There are substantial dietary shifts amongst tilapia, both in captivity and in the wild.

For example, season, and associated food availability, affected tilapia diets (Cailteux et

al. 1992; Ikomi and Jessa 2003). In addition, water quality has also been known to affect

feeding ecology. Salinity, for example, has been demonstrated to play a role in

temperature tolerances (Zale and Gregory 1989). Ribbink (1990) suggested that

mouthpart morphology changes, as well as other requirements during growth, change

dietary preferences. Njiru (1999) found that the diet ofOreochromis niloticus

substantially changed within approximately 40 years of its introduction to Lake Victoria,

Kenya, fi-om herbivory to omnivory. Knowledge of the expected diet of tilapia is

important to discern aberrant behavior.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Natural Diet of Tilapia

Blue tilapia, andOreochromis in general, are considered planktivorous and

detritivorous, and the bulk of the scientific and trade literature describes Oreochromis as

using filter feeding as a main strategy to collect phytoplankton, zooplankton, and detritus

(Gophen et al. 1983; Gu et al. 1987; McDonald 1985a; Oguzie 1999; Spataru and Zorn

1978; Winemiller and Kelso-Winemiller 2003; Zale and Gregory 1990). In addition,

tilapia consume macrophytes, including aquatic and surface plants such as duckweed

{Lemna sp.) (Liliopsida: Lemnaceae) and water hyacinth {Eichhornia crassipes)

(Liliopsida; Pontederiaceae).

Winemiller and Kelso-Winemiller (2003) described tilapiines in the upper Zambezi

River (Zimbabwe/Zambia/Mozambique) as generalists with substantial dietary overlap

amongst sizes, consuming detritus, vegetation, and insects. Benthic and allochthonous

invertebrates associated with detritus have been identified as a major source of protein

(Ikomi and Jessa 2003; Spataru and Zorn 1978), and macrophytes and detritus typically

have an epiphytic layer of microorganisms {Aufwuchs) which provide additional nutrients

(Ribbink 1990). King and Garling (1983) state that cultured tilapia could grow under a

wide range of feeds, including poor-quality natural foods such as cyanobacteria. Several

references to cannibalism in captivity exist, but this is unreported in natural systems (e.g.

Fessehaye 2006).

Effects of Temperature on Diet

Temperature has a profound effect upon feeding rates and diet. Temperature can also

affect diet-related morphology of fish, such as viscera (McManus and Travis 1998). Low

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. temperature induces a stress response and lowers metabolism, all limiting factors for

growth in tilapia (Kindle and Whitmore 1986). Shafland and Pestrack (1982)

investigated tilapia feeding and temperature. Tilapia had reduced feeding below 16 C°

and no feeding below 12 C°, with a lower lethal temperature of 6.2 C°. Egna and Boyd

(1997) suggest that the optimal temperature for growth of cultured tilapia is 27 C°, which

reduces energy utilized to deal with metabolic constraints and allows for growth. Stauffer

et al (1988) reported that tilapia could not survive in sustained temperatures less than 5

C°. However, blue tilapia appear to be the most cold tolerant of the mouth-brooding

{Oreochromis and Sarotherodon) tilapia (Zale and Gregory 1989), and variability exists

in the literature describing lethal temperature limits (Starling et al. 1995; Zale and

Gregory 1989). Based on reported variability of temperature tolerance, associated

feeding ecology is likely also different depending on the population.

Effects of Diet on Tilapia

Fish assimilate and allocate energy into growth, energy storage, gonadal development,

and metabolism (Adams et al. 1982). Growth rate, body size, and fecundity in the

Tilapiines show a great deal of plasticity depending on environmental conditions (Fryer

and lies 1969). Gender, body condition, prey availability, temperature, and season are

critical influences that guide this plasticity (Adams 1982). For example, an abundance of

food in spring may facilitate increased gonadal development, while an abundance of food

in summer may facilitate increased growth, or an abundance of food in summer for a

stunted population of fish within an alkaline spring system may facilitate increased lipid

deposition. Environmental conditions may influence metabolism through physical

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. factors, such as consistent high temperatures, salinities, or extreme pH. De Silva and

Perera (1985) found thatOreochromis niloticus grew the best in 10 parts per thousand

(ppt) salinities, however with a high protein diet (>30%) the fish grew best in 0 ppt

salinities. The limits to growth were attributed to the energy cost of osmoregulation. Due

to the constraints imposed by environmental conditions on fish metabolism, the

individual may need to vary the normal diet to avoid deficiencies. Environmental

conditions may also influence available food items, whether bacteria, detritus, algae,

plankton, macrophytes, or fish. Tilapia diet is the basis that equates available food items

with requirements placed on the individual due to physical conditions, and regulates the

overall fecundity of the individual. For example, individuals at warmer temperatures may

have a higher metabolism, and would require a diet higher in nutrients to maximize

fecundity than would fish at lower temperatures. Literature has shown that cannibalistic

fish maximize traits beneficial to tilapia, such as growth rate, development and fecundity,

and fitness (Fessehaye 2006, and citations therein); however cannibalism has only been

reported with captive tilapia where the escape behavior of prey is curtailed by space

constraints.

Dietary Requirements and Their Importance

Bodv size and Energetics

Body size plays an important role in growth and energy use in fish, and typically

relative growth rate decreases with larger body sizes (Jobling 1994; Steffens 1989). Xie

et al. (1997a) and Al-Hafedh (1999) suggest this is due to decrease in relative food intake,

and protein utilization efficiency is reduced with larger body sizes. Ration size, or

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. amount of food, typically (but not always) affects growth in a non-linear fashion (Jobling

1994). The larger fish grows slower as there is more mass to support relative to

ingestion. Typically, fish respond to this inequality by increasing prey, or portion, size

based on increased gape or other morphology as described above. More food, depending

on protein quality, is translated to more mass (Siddiqui et al. 1997).

There is also a point of maximum efficiency, where higher ration size does not benefit

the fish in the form of growth as feed efficiency of the digestive system is maximized.

This was found to be 2% of the tilapia’s body mass utilizing formulated feed (Xie et al.

1997b). Increased rates of ingestion have been found to be responses to nutrient (i.e.

protein) deficiencies (Bowen et al. 1995). In addition to ration size, feeding frequency,

and time of residency in gut have direct effects on feed efficiency and growth (Riche et al.

2004). Normal variations in ingestion because of social, environmental, and

physiological factors regularly occur within fish (Jobling 1994), thus these factors all

have the ability to affect growth and ultimately fecundity.

In addition, the phenomenon of compensatory growth, where a fish rapidly grows

after fasting, could affect body size, especially after periods of low food availability.

Several factors influence compensatory growth, including duration of fasting, age,

previous nutritional health, population levels, and gender (Barreto et al. 2003).

Compensatory growth may present additional nutritional constraints on the individual and

create a protein or lipid sink in the fish.

Fish bioenergetics is governed by quality of diet (Jobling 1994), and lack of nutrients

could have deleterious effects on fish, which is especially evident in hatchery situations.

Nutrients are essential components for the functioning of the fish’s body. A useful model

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of fish bioenergetics was developed by Hewitt and Johnson (1992; Crowl et al. 2000),

where:

C = (R + G) /1 - (E + F + SDA)*

Nutrients are obtained from consumption, incorporated into growth, and utilized by

respiration. Nutrients are the building blocks of enzymes and structural components of

the fish, and are critical for maintaining the growth, reproduction, and all other functions.

If a specific food item is limiting of a nutrient, then to avoid a deficiency the individual

must either eat more (an excess) or vary the diet to include other food sources that have

that specific nutrient. For example, nutrient deficiencies have been linked to increased

cannibalism in captive fish (Baras and Jobling 2002). There are five main types of

nutrients: Protein, lipids, carbohydrates, vitamins, and minerals.

Protein

Protein, a substance comprised of amino acids and usually provided in commercial

fish diets by inclusion of fishmeal (De Silva and Anderson 1995), is a major source of

energy, has a variety of effects on tilapia, and is critical to tilapia fecundity and growth

(Garling and Wilson 1976; Steffins 1989; Al-Hafedh 1999; Bowen 1980). Protein is a

large molecule composed of up to 20 or more major amino acids. Ten amino acids are

critical to obtain in the diet; since animals cannot create them. Proteins are digested into

base amino acids, which are absorbed and utilized to build tissues (SWFN 1983).

* C = Consumption, R = Respiration, G = Growth, E = Excretion, F = Egestion, and SDA = Specific Dynamic Action

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Not all proteins have the same nutritive value, and protein quality is based on the

types and amount of amino acids in the protein molecule. Fish would need to eat more or

vary the diet if they eat predominately low-quality protein. Plant-based protein

supplements have only recently been developed for the rearing of tilapia, and legume

protein concentrates have been one of the few non-fish protein sources used to

successfully grow tilapia, however, plant-based proteins can result in nutrient deficiencies

(Olvera-Novoa et al. 1997) or lower growth rates (Davis and Stickney 1978; Alceste

2000; Olvera-Novoa et al. 1998). Algae, such asSpirulina sp. (Cyanophyceae:

Oscellatoriaceae)(01vera-Novoa et al. 1998) and duckweed (Fasakin et al. 1999),

typically are composed of poor quality protein. Plant-based proteins have different ratios

of amino acids, and in protein deficient diets, arginine, and lysine were likely the limiting

amino acids (Davis and Stickney 1978). Plants, as well as their periphyton, that are low

in protein may be a large portion of a tilapia’s diet, and large quantities must be

consumed to obtain suitable levels of protein (primarily arginine and lysine) for growth.

In food-limited environments, such as after tilapia consume all aquatic vegetation or there

is limited plankton, reproduction or growth may be sacrificed, which ultimately affects

fecundity. For example, Gunasekera et al. (1996) found protein-deficient diets over time

caused low female body weight, suggesting energy was being channeled to maximize

reproductive capabilities instead of growth.

In order to maximize fecundity, female tilapia should theoretically maximize protein

intake. Proteins, as well as other nutritional requirements of fish such as lipids, have

been shown to affect frequency of spawning in tilapia (Santiago and Reyes 1993).

Protein intake has been demonstrated to be linked to spawning performance and ovarian

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. recrudescence within Oreochromis niloticus, where low protein diets reduced spawning

frequency and clutch size (Gunasekera et al. 1996; Gunasekera and Lam 1997; El-Sayed

et al. 2003), and high protein decreased age of puberty (Gunasekera et al. 1995). El-

Sayed et al. (2003) demonstrated that increased protein in tilapia diets increased size of

fish at maturation, egg hatchability, number of eggs per spawn, larval weight, and fry

growth, especially in adverse salinities. El-Sayed et al. (2003) also reported decreased

hatch time for tilapia raised on high-protein diets. Gunasekera and Lam (1997) also

determined protein intake affected oocyte growth, with a chronically protein-deficient

diet, delaying recrudescence and creating smaller mature oocytes. Cerda et al. (1994) also

demonstrated that protein levels directly affected oocyte growth in other species, with

deficiencies translated over to delayed development. Love (1980) demonstrated that

protein is directly utilized to produce ATP, which supplies metabolism with energy,

during fasting.

Protein has been shown to improve overall condition of tilapia (Gunasekera and Lam

1997), which is a function of body size. As a fish grows, the protein requirements lessen

(Wilson 1989), suggesting that there is a sufficient reserve of protein in the body to

provide for necessary functions. Bowen (1979) suggested that the detritivorous Nile

tilapia {Sarotherodon mossambica) in Lake Sibaya, South Afiica, derived enough protein

during juvenile stages for growth, stages that were likely in part particle-feeding

zooplankton (albeit the author stated that the tilapia were exclusively detritivorest), yet

t Food sources that supply more energy per unit effort would be selected over food with poor nutrient content. Food availability has been shown to modify fish diet (Wooton 1990; Maitipe and DeSilva 1985), as well as the diet of Nile tilapia, which has been

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. became protein deficient during adult stages and experienced stunting. Detritus nutrient

content in Lake Sibaya was derived mainly from microorganisms, such as bacteria, which

contain protein. Fish are also a major potential source of protein and lipids (Steffens

1989), whieh may be eause for piscivory in tilapia.

Lipids and Carbohvdrates

Fatty acids, non-protein amino acids, lipids, and carbohydrates have also been shown

to have effects on tilapia well-being. Lipids are essential for energy and growth, and are

used to construct cell membranes, to absorb vitamins, and for other metabolic functions.

Lipids are critical to fish, and at low temperatures, reproduetive capability may be

sacrificed to conserve lipids in the mesenteries and liver (McManus and Travis 1998).

Lipids are also used to increase palatability of formulated feed (SWFN 1983), and fish

favor formulated foods with increased lipids. The aquaculture industry typically utilizes

fish oil as a supplement within feeds, in part to supply fatty acids (Liu et al. 2004), and as

a primary sources of lipids (Wille et al. 2002). Lipid requirements in tilapia are greater as

juveniles, when they require 10% of their diet to be lipids. As the fish grow, they

eventually require as low as 6% of their diet (Aleeste 2000). McKenzie et al. (1996)

demonstrated that at increased temperatures, tilapia fed unsaturated fatty aeids from a

fish-based meal physiologically handled exercise better than did fish fed a plant-based

saturated fatty acid. This suggests that tilapia which consume fish could better cope with

exercise in warm, flowing waters than strictly vegetarian tilapia. However, lipids have

been shown to decrease weight gain and protein uptake efficiency in the Nile tilapia

demonstrated to change from suspension to detritivory depending on abundance of phytoplankton.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Meurer et al. 2002), which would require additional proteins to make up for the

deficiency.

Lipids are also essential for providing energy reserves for tilapia (Halver 1972), and

fat levels in tilapia carcass and weight gain are proportionate to lipids included in diet

(Wille et al. 2002). High lipid diets also enhance conversion of food sources to energy,

and are connected very closely with protein utilization (Hanley 1991). Females typically

have higher lipid requirements due to egg production, which limits availability of energy

for growth (Mair et al. 1995). In addition, non-protein amino acids associated with

detritus have been shown to stimulate growth in tilapia within some habitats, but the

content of non-protein amino acids is low in many systems (Bowen 1980).

Carbohydrates are generally poorly utilized by fish digestive systems, and diets high

in carbohydrates generally result in impaired growth. Fiber, in part, could increase

carbohydrate utilization by increasing residence time in the digestive system (Shiau

1997). However, lower levels of carbohydrates may assist the fish in utilizing protein and

the subsequent amino acids (SWFN 1983). Another compound that impaired growth was

cellulose (Anderson et al. 1984), a primary component of plant materials and a source of

fiber. Tilapia that ingest increased levels of cellulose may require additional protein to

maintain growth in order to remain competitive. Depending on vegetative surface area of

grazed macrophyte and environmental conditions, amount of epiphytic bacteria supplying

protein could significantly vary to where low numbers cause protein deficiencies in plant-

eating fish.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Other Nutrients, Vitamins, and Minerals

Different nutrients and/or substances could have cumulative effects, either benefiting

or negating, on the physiological utilization of food items. Therefore, a wide range of

compounds and elements are necessary for weight gain, and ultimately the fecundity of

the individual fish. Vitamins, minerals, and other trace compounds are necessary for

proper growth and have a variety of specialized functions. Fat-soluble vitamins. A, D, E,

and K, are absorbed in the intestine and could be stored if ingested in excess. Vitamin E

is important for proper functioning of reproductive organs, and has been shown to

enhance ovarian growth, hatching success, and survivorship of larvae (Emata et al. 2000).

Water-soluble vitamins (most of the other vitamins) cannot be stored and must be

regularly consumed to avoid deficiency. Vitamins in general may be of varying degrees

of importance relative to the stage of development of the fish. Vitamin C is important for

the brain and gonads, and is the leading micronutrient for the functioning of reproductive

tissue, including the production of hormones. Vitamin C has been demonstrated to

increase egg viability, hatching success, and survivability (Emata et al 2000). Tissue

levels of Vitamin C in the brain are the slowest to decline during deficiency, suggesting

that reserves in the brain are highly important (Dabrowski and Ciereszko 2001). Vitamin

C deficiencies prevent iron uptake within the intestine, thus creating anemia, as iron is not

present for use in the circulatory system. It is an antioxidant, and deficiencies may cause

kidney and liver damage (Adham et al. 2000).

Minerals could be ingested or absorbed, and may be stored in bones or scales, such as

phosphorus and calcium. Minerals also have specialized purposes, and deficiencies result

in poor growth or developmental disorders. For example, lack of iodine is generally

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. known to cause thyroid disorders. Another example is a deficiency in zinc, an essential

nutrient for enzyme activity and protein synthesis, could lower immune response or body

weights (Vinicius do Carmo e Sa 2004). Tied to zinc, the enzyme phytase increases

protein utilization and availability of phosphorus and calcium (McMullen 2001). This

supports greater growth, and increases calcium, magnesium, and phosphorus in bones

and/or blood (Portz and Liebert 2004). Sodium (NaCf), an important mineral for

osmoregulation as well as the nervous system, when introduced into feed has been

demonstrated to increase growth in freshwater tilapia, but decrease growth at high or low

levels (Shiau and Lu 2004).

Limitations to these nutrients can lower the condition of the individual, ultimately

affecting its fecundity. Some compounds, such as phytase, are already limited in

availability, through either the diet or the metabolism of the fish. The number of these

mineral or chemical requirements is large, however most of these nutrients could be

obtained from herbivory, detritivory, or omnivory, and deficiencies are typically only seen

in hatchery-reared fish fed artificial diets. Therefore, these nutrients and minerals are not

likely to be negatively influencing tilapia in Nevada.

Dietary Plasticity

Blue tilapia are a tropical, warm water species that are widely distributed. Species

that are widely distributed typically are generalists and euryphagous. Tropical species

that employ this strategy may have a range of diets depending on habitat, for example, the

African fish. Alestes macropthalmus (Characiformes: Alestiidae) consumes vegetation in

swamps but is carnivorous in lakes (Lowe-McConnell 1975). Crowder and Cooper

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (1982) state that fish diets are generally plastic, and fish are able to modify feeding

strategies to maximize their energy intake per unit effort.

Drenner et al. (1982) suggest that the size of tilapia dictate method of foraging and as

the fish grows, feeding strategies are shifted. In this case, small tilapia {Sarotherodon

galilaeum) particle feed on individual prey items until they grow to over approximately

60 millimeters total length, and then become obligatory filter feeders. This changes food

preference as the fish matures, which limits intraspecific competition and allows the

population to exploit a wider range of resources (Ikoma and Jessa 2003), which is

consistent with the generalist dietary ecology of the tilapia. Drenner et al. (1982) also

suggested that smaller fish have a period of overlap where they are both particle and filter

feeders. Studies have shown that diet, or diet and genetics, influences morphology (e.g.

Cichlasoma minckleyi, Astatoreochromis alluaudi, and Gila bicolor), which allows the

fish to coexist in greater numbers, utilizing differing niches and the respective diets

(Trapani 2004; Galat and Vucinich 1983). Taste has been demonstrated to stimulate food

finding and ingestion. Nile tilapia have been demonstrated to be sensitive to specific

amino acids, and utilize taste and smell to selectively forage in sites that maximize intake

of essential amino acids (Yacoob et al. 2001), which may facilitate camivory.

Food Quality and Availability

Food quality could potentially cause tilapia to alter diet. Nutrient quality of foods can

vary due to many factors. For example, McDonald (1985b), found carbon content of

algae widely varies, and some species are more nutritious than others. Nutrient content

and/or palatability of plants have been demonstrated to affect food choices of Tilapia zilli

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Saeed and Ziebell 1986). Food sources that supply more energy per unit effort would be

selected over food with poor nutrient content. For example, tilapia may shift from

planktonic algae to epiphytic food sources depending on seasonal nutrient quality of

plankton.

Food availability has been shovm to modify fish diet (Wooton 1990; Maitipe and

DeSilva 1985), and Nile tilapia has been demonstrated to change from filter feeding to

detritivory depending on abundance of phytoplankton. Ribbink (1990) suggests that

periphyton-feeding cichlids change food preference depending on availability of other

sources, including insects and fish. This change was likely due to the ontological

development of feeding morphology and/or nutritional requirements, and can occur over

several temporal scales. Spataru and Zom (1978) suggest that diet changes from

zooplankton to phytoplankton depend on seasonal fluctuations of prey populations. La

Mesa et al. (2000) described dietary plasticity in a planktivorous Arctic fish, Trematomus

newnesi (Actinopterygii: Nototheniidae), which is based on environmental conditions and

prey availability (or diversity). Gu et al. (1997) determined that blue tilapia were able to

alter feeding strategies, changing foraging from phytoplankton to detritus depending on

food resource availability, and were able to consume a wide variety of food types. This

feeding plasticity potentially allows for the utilization of fish in the diet as a source of

protein and fatty acids.

Camivory in Tilapia

The use of animals larger than zooplankton, including macroinvertebrates, terrestrial

insects, or vertebrates, by tilapia as prey is rarely documented outside of captivity, which

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. is usually the artificially elevated population densities of aquaculture. Although gut

contents were predominately detritus, vegetation, and phytoplankton, Jimenez-Badillo

and Nepita-Villanueva (2000) found 6.9% of blue tilapia predated on inseets and fish in a

Mexican lake. Bowen (1979) found fish in digestive tracts of Nile tilapia, where four

juveniles and three adults of 1,262 individuals sampled contained fish, which was 0.5%

of the total sampled. Njiru (1999) found fish and insects as important food items for

introduced Oreochromis niloticus in Lake Victoria, Kenya, and laboratory experiments

have demonstrated eannibalization in the Nile tilapia (Neil 1964; Fessehaye 2006).

Whitton et al. (1987) state that Oreochromis mossambica predates on fish and mussel

larvae, in addition to vegetation, and likely contributed to extirpations of native fish in

Indonesia. Gut contents of blue tilapia within the Muddy River also eontained fish

(Scoppettone et al. 1998; Scoppettone 2004). Seoppettone (2004) suggested that prey

fish size correlated with tilapia size, which is consistent with other piscivorous fish where

larger fish could mechanically process larger prey.

Although it must be noted that Gaye-Siessegger et al. (2004) found that several

confounding factors influence interpolation of trophic levels using stable isotopes in

tilapia, Gu et al. (1997) suggested that some small blue tilapia analyzed for stable

isotopes were entirely carnivorous (likely utilizing benthic invertebrates), though diet

became varied as the fish grew. This study demonstrates the promise of stable isotopes to

be used to determine diet of tilapia, which could be used to detect historic consumption of

fish regardless if they were present in the gut during sampling.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Habitat Characteristics and Alternate foods

Aquatic food webs are driven energetically by allochthonous and autochthonous

materials. The majority of energy is derived from the allochthonous materials that blow,

wash, or drop into the stream, which are processed by shredding invertebrates,

detritivores, and nitrogen-fixing organisms such as bacteria. In tropical ecosystems where

tilapia have evolved, these processes form the base of the detritus and periphyton upon

which they feed. In addition, in the larger rivers where they have evolved, much of the

flows are driven by nutrient-rich runoff, which elevates primary productivity and there is

a great deal of suspended foodstuff due to the nutrient supply. The habitats within the

Muddy River and the rest of Southern Nevada differ in the sense that they are typically

comprised of base spring outflows with very little runoff. Spring outflows are typically

plankton-poor, and primary productivity is typically in the form of algae mats or

periphyton on rocks. In addition, the Warm Springs area of the Muddy River is severely

impacted by the non-native fan palm {Washingtonia filifera) (Liliopsida: Arecaceae),

which comprise most of the riparian overstory. These palms are evergreen (do not drop

leaves to provide allochthonous material), shade the stream (prevent photosynthesis and

primary productivity), and send networks of roots into the stream (likely filtering out

nutrients, as well as excluding gravel-based invertebrates and microorganisms).

Macrophytes, such as Potamogeton sp. (Liliopsida: Potamogetonacea), tend to be sparse

in the Muddy River, and typically occur in fast-moving water where they are difficult to

graze. As a result, it is likely that the Muddy River, especially the Upper Warm Springs,

is a food limiting system in respect to planktivorous or detritivorous tilapia.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Tilapia populations are able to rapidly grow, and quickly dominate an ecosystem

(Faunce and Papemo 1999). As the population grows, there are less standard food

resources available per individual. Since these systems are limiting in food resources, in

order for a tilapia to maximize fitness it would need to conduct alternate dietary strategies

to acquire essential amino acids and other nutritional requirements discussed above.

Fish are excellent sources of a variety of amino acids, especially essential amino acids

that are poorly represented in vegetation, as well as lipids and other nutrients. In addition,

the native fish are naïve to predation by tilapia, therefore do not provide as much of an

energy drain to capture as would a fish that coevolved with blue tilapia. Given these

factors, it is likely that fish are predated to a degree to supplement the tilapia’s diet in this

system, especially for younger tilapia where growth is paramount. In addition, factors

that likely affect predation include gender, size, fitness, and habitat characteristics.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 3

MATERIALS AND METHODS

Several hypotheses were investigated. Hypotheses 2-5 were contingent upon

Hypothesis 1 being supported. These hypotheses were:

• Null Hypothesis (Hq): Tilapia are not carnivorous, and only consume

plankton, vegetation, and/or detritus.

Hypothesis 1 : Tilapia consume fish as diet items.

Hypothesis 2: Tilapia gender influences piscivory.

Hypothesis 3 : Size influences piscivory.

Hypothesis 4: Tilapia fitness influences piscivory.

Hypothesis 5: Tilapia piscivory varies between lentic and lotie

environments.

Methods selected to investigate these hypotheses were developed to utilize existing

data or existing samples from ongoing governmental resource management projects or

programs. All fish collected would have otherwise been disposed of. Other methods to

determine piscivory would be applicable, such as stable isotope analysis or parasite

surveys, which would provide additional clues on tilapia diet. The methods used did not

require additional use of governmental funds, or acquisition of funds to collect the data.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. It also did not require significant additional efforts to capture tilapia, which would cause

stress to the remaining native fish. Appropriate University of Nevada, Las Vegas, animal

use and care protocols were submitted and approved to support this project (UNLV

Protocol #R993-0502-177).

Site Description

The study area (Figure 1) is within the Mojave Desert physiographic region in

southern Nevada, and includes the Muddy and Virgin River watersheds. Warm Springs,

in the upper Moapa Valley approximately 100 kilometers east of Las Vegas, northeastern

Clark County, Nevada, includes a spring complex that constitutes the headwaters of the

upper Muddy River and the terminal flow of the White River Groundwater Flow System

(Eakin and Lamke 1966). It is a major discharge point for a vast regional carbonate

ground water flow system stretching more than 450 kilometers to the north, as well as

multiple shallow basin-fill aquifers associated with mountain ranges (Eakin and Lamke

1966; Planert and Williams 1995). The water-bearing stratum comes to the surface in

multiple seeps and springs that provide a complex variety of habitats, which contain

several endemic species. The Muddy River was historically a tributary to the Virgin

River, but currently flows into Lake Mead because of the impoundment created by

Hoover Dam (Holden et al. 2005).

The upper valley is relatively flat, with some hummocks at the periphery and

drainages throughout, and is surrounded by xeric foothills. The valley has a perennial

supply of water from springs, and is influenced by periodic floods arising from the

surrounding desert watershed. The stream water in the upper Moapa Valley is typically

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. warm and clear. The Muddy River downstream of the Warm Springs Road bridge is

primarily cool, fluvial and relatively turbid. Most of the stream courses have been altered

from their pre-existing condition through channelization, incision, diversion,

sedimentation, and livestock grazing (e.g. Cross 1976).

The vegetation within the study area is typical to the northern Mojave Desert and

associated riparian areas. Dominant trees or arborescent shrubs in riparian sites include

willows {Salix spp.) and the non-native salt cedar(Tamarix ramosissima). The Warm

Springs area of the Muddy River is dominated by the non-native California fan palm

{Washingtonia filifera). Riparian understory is predominately arrowweed {Pluchea

sericea), saltbush {Atriplex sp.) seepwillow(Baccaris sp.), as well as various forbs.

Emergent vegetation in marshes is primarily cattail {Typha sp.). Native submergent

vegetation is sparse and typically confined to slow moving stream edges or pools. This

vegetation included naiad (Najas sp.) and pondweed(Potamogeton sp.). Warm spring

outflows were typically dominated by non-native eelgrass. During periods of low

turbidity, there was abundant algal/bacterial growth on rock substrates, stream edges, and

in pools.

Sample Acquisition

Tilapia were captured using rotenone, electroshocking, spearing, and nets. Most

tilapia were collected with rotenone. Electroshocking, spearing, seining, and gill or

trammel nets were used opportunistically. All work was conducted in daylight hours.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The collection of tilapia throughout the Muddy River was conducted by the USGS during

the winter of 1998 and fall of 2000, to investigate declines in the native fish population.

The USGS collected data on these fish and provided it to the investigator. The collection

of tilapia at Nevada Power’s Reid Gardner generating station corresponded with a tilapia

removal program by NDOW during the spring of 2003 and 2004. The tilapia removed by

NDOW were salvaged by the investigator and used for this analysis.

Rotenone is a naturally occurring substance derived from plants, and has been used as

a traditional method to capture fish by South American tribes. Rotenone has been used as

a fisheries management tool since 1934, and has a long history of successful applications

(Finlayson et al. 2000). Rotenone is a non-systemic inhibitor of cellular respiration in

animals, and is most toxic when taken into the body through absorption into the blood

across gill membranes. Due to this route of exposure, it is selective for animals that

breathe through gills, or absorb dissolved oxygen in water for respiration. Concentrations

between 0.5 to 10 parts per million (ppm) of rotenone are typically used for fisheries

applications (Finlayson et al. 2000). Rotenone is commonly utilized by fisheries

managers to eliminate undesirable fish within systems where mechanical means are not

efficient. Examples of this include elimination of competitory fish in trophy fisheries and

removal of harmful non-native fish in systems where native fish are preferred (Finlayson

et al. 2000).

As specified by the pesticide labeling, rotenone was applied to flowing water and

pools at a standard rate of less than 5 ppm. Since rotenone loses effectiveness as it is

naturally detoxified by sediments or particulates, booster stations were established at

locations as necessary to maintain a concentration of less than 5 ppm throughout the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. treatment area. The number and placement of these locations were determined based on

information derived from pretreatment surveys, flow characteristics, and susceptibility of

sentinel fish. Backpack sprayers, gasoline-powered pumps, and boats rigged with drip

systems were used to deliver rotenone to standing water, where drip stations were not

effective at distributing rotenone. Application of rotenone occurred for at least 8 hours,

with treatment time adjusted relative to flow characteristics and response of sentinel fish.

During treatment, crews collected all fish found dead, which were used for stomach

analysis.

Gill or trammel nets were placed across or within sites. Mesh size ranged from 16-

inch to 2-inch standard. Nets were regularly monitored so fish did not remain trapped

and digest their stomach content. Cast nets were also employed at sites where it was not

possible to place a passive net and the turbidity of the water was high.

Sample Preservation and Processing

All fish collected were immersed in ice water to slow digestive processes. Fish were

either processed immediately or frozen. All fish were weighed and measured to total

length (length from snout to tip of tail). Digestive tract contents were removed, described

to lowest taxonomic level, enumerated, and if noteworthy, placed individually in

containers with either 10% Ethyl Alcohol or fixed in formalin for preservation and

labeled with associated source data.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Measurements and Other Analyses

Fulton’s condition factor was developed for each sample utilizing the formula K =

(w/L^) (10^) Î (Murphy and Willis 1996). This was used to correlate body condition with

diet. Stomach contents were numerically analyzed, obtaining frequency of occurrence

(proportion of population that feeds on particular food item).

Analysis of Data

Paired data derived to test hypotheses were analyzed using Chi-squares and logistic

regression (Zar 2004). Logistical regression is a robust test that involves fewer violations

of assumptions than other tests, such as discriminate function analysis, which requires

independent variables to be normally distributed, similar group sized, and linear relations

(Garson 2005). SPSS (2005) Statistical Software was used to analyze data. All data sets

were analyzed using standard descriptive statistics and tests for normality.

Existing samples were enumerated to determine appropriate error rate. Sample sizes

were determined using information derived from pilot study, where;

Sample Size = n = (z^pq)/(e^)§

Stomach content was classified to type (fish material present, vegetation only,

unidentified material, or empty) and enumerated. The data obtained from the USGS

Î K = Condition Factor; w = weight of sample; L = total length, 100,000 = metric scaling constant. § z = z statistic @ a = 0.95; p = proportion positive (e.g. fish detected in sample); q = proportion negative (e.g. fish not detected); s = allowable error (set at 3.4% probability )

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. contained classes of bread and invertebrate material. These were filtered by classifying

according to most dominant stomach content other than these two materials.

Relationships between gender, length, and piscivory were determined using linear

regression. Other variables included in the regression were location and/or length. The

Wald Chi-Square was used to determine level of significance.

Relationship between Fulton’s K and stomach contents was modeled using simple

linear regression, and analyzed using a one-way ANOVA. Only fish captured from Reid

Gardner generating station were used for K analysis, since weight data was unavailable in

the USGS data set. Levene’s test was used to determine equality of variances. Stomach

content data were filtered to include only vegetation and fish contents. Empty and

unknown stomach content data were rejected, since these fish could be either piscivorous

or herbivorous and the addition of these variables confounded data analysis. Both

Kolmogorov-Smimov and Shapiro-Wilk tests were used to test normality of overall

Fulton’s K and Fulton’s K per the stomach categories vegetation and fish present;

however the Kolmogorov-Smimov test was principle due to n = 217 (except for the

Fulton’s K/fish present category which had n=15). Standard SPSS (2005) Explore

function was used on all data to develop descriptive statistics, histograms, and Q-Q plots.

SPSS Curve Fit function were used to determine model and parameter estimates. One

outlier datum with an extremely high Fulton’s K was present, and was discarded, as it

was likely an error in measurement.

Relationships between lentic and lotie environments and stomach content were

modeled using multinomial logistic regression (using Nagelkerke’s R-Square (Nagelkerke

1991)). Predicted vs. observed values were also determined. Stomach content data were

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. also filtered to include only vegetation and fish contents, and empty and unknown

stomach content data were rejected. The labeling of a site as lentic or lotie was

determined if the sampling site was in a stream or a pond environment.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 4

RESULTS

Hypothesis 1: Piscivory in Tilapia

Of the 725 tilapia sampled, 126 individual samples contained fish material,

comprising 17.4% of the total (Figure 2). Using data fi-om the Reid Gardner ponds only,

potential error rate was determined to be 0.034**, thus there is a 3.4 percent chance of

error that 216 samples would provide a value within a 95% confidence level. By adding

USGS data, potential error was reduced to 2.6 percenttî. The Chi Square was 1.64 (6

d.f, a = 0.95), and the Pearson (chi square) (SPSS 2005) was 15.34 (642.1, p = 0.00,

with USGS data).

Hypothesis 2: Gender Influences Piscivory

Stepped forward selection of logistic regression suggested gender and location as the first

and second significant factors in length, resulting in a Chi-square of 25.86 and 10.77.

Using all data, the error was 6 percent when the sample size of individuals with fish in the

** N = (z^pq)/(6^) = (1.96)^(0.07)(0.93)/0.034 = 216

tt N = (z^pq)/(s^) = (1.96)^(0.174)(0.826)/0.026 = 726

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Stomach ConWats O Rah O V«cftt.«t»ii a Stoi»*ch E»q>ty ■ OtWr

mm##;

Figure 3: Proportion of dietary items found in tilapia stomachs.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. gut was 126 (23 females and 92 males containing fish), which excluded 11 individuals

that contained fish in the gut but were not identifiable to genderThe Chi Square =

1.64 (6 d.f, a = 0.95) and Pearson (chi square) (SPSS 2005) = 23.98.

The non-parametric Kruskal-Wallis Test was significant, accepting piscivory differed

by gender, resulting in a Chi-Square of 8.9, with two degrees of freedom and a

significance of 0.011. Females ranked slightly higher than the males with a mean rank of

109.35 versus 109.9. Fish with gender unknown, typically smaller fish, ranked at 138.02.

Kolmogorov-Smimov test for normality showed data of all stomach contents being

normal, and Levene statistic at a.os showed variances are equal.

The Wald statistic was significant for gender when all locations were pooled, and the

standard error of the intercept (B) was precise. Location and length were not significant.

Percentage correct of predicted variables was 93.5 percent, and the data was not

homoscedacic. In lentic-only systems, gender was not significant.

Hypothesis 3; Size influences Piscivory

The results for the Wald test for all systems was not significant (p = 0.835); however

it was significant for lentic-only systems (a < 0.01, p = 0.006), which was ranked a

secondary significant factor.

M N = (z^pq)/(E^) = (1.96)^(0.18)(0.73)/0.06 = 126

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Hypothesis 4: Tilapia fitness influences piscivory.

Using a simple linear regression model, stomach content was poorly predicted by

Fulton’s K, with a significant of 0.056 (p = 0.000). The one-way ANOVA resulted in

a significant similarity between stomach types (F = 5.1; df = 3; p = 0.002). Levene’s test

(F=2.69; p=0.10) weakly suggested variances were not equal. Both Kolmogorov-

Smimov and Shapiro-Wilk tests of Fulton’s K were not significant (p = 0.2 and 0.3

respectively), thus adequately accepting normality of the data, and a Q-Q plot of Fulton’s

K appeared linear. Skewness and kurtosis were 0.28 and 0.17 respective, suggesting a

relatively bell-shaped curve of Fulton’s K values. Fulton’s K within both stomach

content categories was also normal using the aforementioned tests.

Hypothesis 5: Tilapia piscivory in lentic and lotie environments.

Using all data, the sample size of tilapia containing fish in their gut was 126, and the

error rate regarding the difference of piscivory depending on water movement was

determined to be 0.08 (8%)§§.

Using a multinomial regression model, stomach content had a Pseudo R-Square (Cox

and Snell) of 0.096. Relationships between still water and stomach content, length, and

gender in the final regression model were significant (p = 0.04. 0.00, and 0.15

respectively) as classification for still water was 63.6% and flowing water 64.4%. Nearly

equal samples were collected in flowing and standing water: 362 and 364 respectively.

N = (z^pq)/(sQ = (1.96)^(0.4)(0.6)/0.08 = 126

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E & 2 0 0 - î

1 0 0 -

0 -

still water flowing water Lentic vs. Lotie

Figure 4: Length differences of tilapia within Lentic and Lotie sites on the Muddy River and Reid Gardner generating station.

Descriptive statistics indicated fish were larger in still water {x =131 mm, SE = 2.5)

than in flowing water (x =115 mm, SE = 2.0) (Figure 3). A t-test between the lentic

and lotie groups testing a difference in length was significant (p < 0.001).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 5

DISCUSSION

This thesis attempts to show that tilapia are piscivorous, and test several hypotheses

that may contribute information to reasons behind this piscivory. If a clear difference is

detected, such as a gender difference, then targeted management may be able to address

one vulnerable life stage or habitat requirement of the invasive species that would depress

the numbers of fish that fit that variable (e.g. use nets to target specific size of fish).

Variables examined relative to dietary differences were gender, size, and fitness of the

tilapia, as well as occurrence in lentic or lotie systems.

Hypothesis 1: Tilapia are Piscivorous

Blue tilapia in the Muddy River were clearly piscivorous, and differences in stomach

content occurred based on location and gender. A Chi-square of 642.1 was highly

significant rejecting Hq. For the pond-only population, the calculated Chi-square of 15.34

was greater than the critical value of 1.64, thus the Ho specific to the Reid Gardner

generating station ponds is also rejected. This suggests that piscivory by tilapia occurs

and consumption of fish is not by chance. Approximately 7% of the tilapia within the

Reid Gardner pond samples contained fish, many of which had multiple fish in the

sample. Approximately 68% of the Muddy River USGS samples contained fish. Given

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the short residency time of a recognizable fish in the gut, it is likely that the percent of

samples with fish under represents piscivory. This would especially be true if peak

piscivory occurred during times other than when sampling took place, such as early

morning, evening, or nighttime. Other times of the year or weather conditions would also

influence feeding. It is also possible that rates of digestion may differ, or during

sampling, some fish may have regurgitated stomach contents, increasing percentage of

empty stomach contents. Stable isotope analysis would be a better method to determine

true proportion of piscivory in tilapia, and is a logical next step to determine composition

of fish in tilapia diet.

It is not directly apparent why tilapia in the Muddy River system are highly

piscivorous. The published reports from the few other locations have shown that fish are

minor portions of the diet in specific locations, but not to the extent of the Muddy River

tilapia. Captive fish that demonstrate cannibalism, as well as other species, exhibit

greater growth than non-cannibalistic individuals (e.g. Fessehaye 2006, and citations

therein). This indicates that there is an advantage to cannibalism; however, tilapia are

only able to benefit from this if they are in close confines with potential prey, limiting

escape response.

There are several potential explanations why tilapia in the Muddy River are

piscivorous. One possible explanation regarding the Muddy River piscivory is that tilapia

were a result of a relatively recent invasion, and it involved prey fish that have existed

without cichlid or centrarchid predators. This does not explain the presence ofGambusia

and mollies in the gut contents of tilapia from the Reid Gardner generating station, both

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species which have a shared evolutionary history with predatory centrarchids and cichlids,

and are present in other habitats where tilapia are not piscivorous. It is possible that these

populations have lost some of their predator avoidance ability due to many generations

away from these predators and from domestication.

Predation may also be facilitated by the tilapia removing vegetation used by the non

native Poeciliids, such as Gambusia, for cover. If tilapia prefer foraging on vegetation,

they will do so until a point where it is difficult to find and not energetically prudent to

forage. This lack of cover would increase vulnerability of predation to fish that use that

cover, especially springfish, mollies, and Gambusia, and species naïve to predators would

be the first to be exploited. This may help explain the difference in piscivory between the

Muddy River and the Reid Gardner generating station populations, there was still

sufficient vegetation at Reid Gardner for cover (i.e. Figure 5).

Another compelling explanation could involve the complex predator-prey

relationships between different age classes of Virgin River chub and Moapa dace. In

general, adult dace and chub occupy prime locations in the stream current where eddies

facilitates drift feeding and capture of other food, such as invertebrates and fish. It is

likely that smaller dace and chub were relegated to the fringes of this habitat to avoid the

predaceous adult chub, which consists of slower water and where the tilapia would

congregate. Unreported NDOW data (including Arizona Game and Fish data) collected

on the Virgin River suggest that this habitat partitioning took place with similar species to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Tiiuf ul'R-jiii (iauiaci S,iiii|’iaiL' I liac iit'MuvkIv R;‘. ci S.iiaf'aii: I I

I i'ics Knti Nuinbci

t—

Figure 5: Hypothetical change in relative amount of key characteristics over time, including approximate stage where sampling occurred.

dace and chub; however, tilapia did not yet occur. Also, when tilapia did occur in the

Virgin River, they congregated in this type of habitat (Shawn Goodchild, USFWS,

personal observation). This interaction could explain the rapid extirpation of the Virgin

River chub, as tilapia predated upon the young age classes and converted much of the

Muddy River’s biomass to make it unavailable to adult chub.

A third possible explanation could be a niche release theory. Tilapia in their native

habitats, such as in Africa, are likely bound to specific niche characteristics by other

species that are better at exploiting portions of the habitat. For example, one species may

be a very good predator, some others are more efficient omnivore, and another a more

efficient planktivore (Figure 6). With the other species being more efficient than tilapia

at a certain aspect of a resource, the tilapia are restricted to a specific type of herbivory,

planktivory, or detritivory that the other species do not utilize, as it is not energetically

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. advantageous for the tilapia to compete with the other species. When removed from this

situation and put in a foreign habitat, the tilapia is not bound by interactions with these

Aliif.i Species 1 Al'ticii Species 2 Omnivore Carnivore

Niche (irenvllh à

Species 0

Plaiiklivdic lleihivorv Caiiiivoiv

DIET

Figure 6: Hypothetical Tilapia Niche Breadth in Native Habitat.

species, and is able to expand its diet accordingly (Figure 7). In this situation, it is only

bound by the ability of the fish in the new system, such as Moapa dace, to compete,

which in the Muddy River have narrowly specialized niche requirements.

Being a recent invasion of tilapia (less than 15 years old), it is likely that the

ecosystem is still in the process of balancing, and the relationship of vegetative cover and

predation is fluctuating in proportion. More investigation needs to be conducted to

determine if other published accounts of tilapia diets occur in stable populations or if they

are also relatively new at the time of sampling.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. iiiiiiMiucfil Tilapus Nil naliic cOinpclildM

DUT

Figure 7: Hypothetical Introduced Tilapia Niche Breadth.

Hypothesis 2: Gender Influences Piscivory

The calculated Chi-square of 23.98 was greater than the critical value of 1.64, thus Ho

is rejected. This suggests that the rate of piscivory by tilapia is different between genders.

Although females ranked slightly higher than males, male tilapia were more likely to

predate other fish than were females (17% vs. 2.6%). Based on the samples, there was

not a great difference in the proportion of samples with or without fish between the two

genders at the Reid Gardner ponds, which suggests that piscivory was important for both

genders. It was also confounded by fish whose gender could not be identified and were

eliminated from analysis, which were mostly small. This was especially relevant for the

samples derived from the Muddy River (Figure 8), where 31% of the samples were

unidentified to gender. This also had consequences for determining gender ratio, where

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the Reid Gardner pond fish were nearly equal, the Muddy River fish were

overwhelmingly male (Figure 9). For this reason, additional representative samples

should be analyzed using dissecting scopes to determine gender of small fish.

As discussed in the introduction, both genders would have a need to maximize

growth, and it could be that at the time of sampling male tilapia needed a more protein-

rich and fatty diet. Given the similar ratio, it is likely that the gender-specific rate of

piscivory changes trajectory over time of year or for other environmental conditions.

Stomach Content ■ Vegetation Q Fish □ Empty

Gender (Muddy River)

Figure 8: Differences in Frequency of Dietary Items found in Tilapia Stomachs between Genders at the Reid Gardner Ponds and the Muddy River.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. stomach Content 100- ■ vegetation S fish □ empty ■ unknown

60' C 3 ÜO

Male Unknown Gender (Reid Gardner Ponds)

Figure 8 (cent.): Differences in Frequency of Dietary Items found in Tilapia Stomachs between Genders at the Reid Gardner Ponds and the Muddy River.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 8

Gender (Reid Gardner Ponds)

Gender (Muddy River)

Figure 9: Gender Ratio of Tilapia at Each Sampling Site.

Hypothesis 3; Tilapia Size affects Piscivory

Length was significant only in the lentic models. Overall, there was not substantial

influence of size over piscivory (Figure 10). Flowing water is poorer tilapia habitat

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200 Length (mm)

Figure 10; Histograms of Length-Frequency based on stomach content.

than lentic due to increased hydraulic drag and lower food availability. Lentic systems,

with lesser hydraulic energy influencing substrate, allow for increased accumulation of

detritus, and associated aufwuchs. They also allow for a greater amount of pelagic

plankton due to the standing water. Another benefit of lentic water is the lack of flow

allowing tilapia to expend less energy to maintain place. In general, the tilapia were

smaller in lentic systems than lotie (Table 2). Larger, dominate tilapia would exclude

smaller fish from the lentic site, and lotie systems would contain tilapia that are smaller

and have a low social status. These smaller tilapia would generally need to maximize

their growth, and may exploit additional resources than would the tilapia in lentic sites.

The smaller tilapia likely avoid the main current in lotie environments, hut would be

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. present in increased numbers between the lentic/lotic boundaries and would be able to

utilize prey species at either location.

Size (mm) (Mean) Male Lentic 144 Male Lotie 128 Female Lentic 150 Female Lotie 127 Unknown Lentic 119 Unknown Lotie 81 Overall Lentic 144 Overall Lotie 114

Table 2: Mean Total Length of Tilapia within Lentic and Lotie Systems Separated by Gender.

Surveys suggest lentic systems in the Muddy River generally have a greater number of

potential prey fish. Adult native fish, such as the speckled dace(Rhinichthys osculus

moapae), Moapa dace, and Virgin River chub, prefer lotie habitat, and White River

springfish can occur in both (though they utilize the slow microhabitats in lotie systems).

Slower water surrounding the fiinges of lotie portions generally contain the subadult fish,

whereas younger juvenile fish tend to utilize lentic sites. Juveniles of native fish such as

dace or chub tend to occur in the open where they can feed on planktonic drift, whereas

non-native Poeciliids are often associated with cover. Due to gape size of tilapia, it is

likely that tilapia prey on smaller fish (Baras and Johling 2002), which tend to occur in

lentic systems within the Muddy River system (S. Goodchild, personal observation).

Therefore, the results are also likely influenced by fewer naïve fish present at the time in

lentic environments due to the non-breeding season.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Hypothesis 4; Tilapia fitness influences piscivory.

Fitness of the individual was not related to piscivory, and the Ho failed to be rejected.

Stomach content was poorly predicted by Fulton’s K, with a value of 0.056.

Approaching the value of one, R^ is closer to supporting the hypothesis that Fulton’s K

affects piscivory. A value of 0.056, which is approaching zero, the lowest value in the

range, suggests that this hypothesis is false, and a fish with a specific Fulton’s K are not

differentially piscivorous. This was supported by ANOVA, which showed a significant

similarity of Fulton’s K between the groups. The data was normal and fit a relatively

classic bell curve (Figure 11), had a mean of 1.79 (S.D. = 0.233), a mode of 1.64, a

variance of 0.05, and a minima of not less than 1.2; suggesting that all populations within

the Reid Gardner ponds were healthy (as defined as a generality of K < 1 being

suboptimal health). A fish that is unhealthy due to a dietary deficiency would have a

lower Fulton’s K, since it would have a low body weight relative to its length. A fish

with a deficiency would also be inclined to obtain nutrients, of which other fish are a

potential source. Given these data, it is likely that all nutritional requirements are being

met by the diet of tilapia, through herbivory planktivory, detritivory, or piscivory.

Another suggestion is that parasitism, hy affecting the nutritional needs or foraging

behavior of the tilapia, would affect piscivory. Although no specific data was collected

on parasite load, parasitism by nematodes was common at Reid Gardner, and in some

individuals collected, the mesenteric parasite loads were very heavy. This did not appear

to cause tilapia to experience poor condition as with other species infected with helminth

parasites (Aloo 2002). Mesenteric nematodes are typically larval forms obtained from

invertebrate secondary hosts (Hoffman 1999), therefore are not likely indications of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. piscivory. No intestinal macroparasites, which could have resulted from a fish

intermediate host, were observed during processing. This suggests that parasites were not

altering prey species behavior, causing increased susceptibility to predation.

Tilapia K Factor

40 nj 3 35 ■o 30 ; -• h,' > ? ■a 25 k ' c 20 $ & 15 0) f i . . n 10 r E 5 3 . P ' • 0 1- 1 1 II II—11—1

Figure 11; Fulton’s K of tilapia captured at Reid Gardner generating station.

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Mean = 1.8057 Std. Dev. = 0.25099 N = 218 1 00 1.50 2 00 2.50 3.00 3.50 Fultons K

Figure 11 (cont): Distribution of Fulton’s K with Normal Curve.

Hypothesis 5 : Piscivoiy differs between lentic (still) and lotie (flowing) systems

Stomach contents were explained very weakly given the low Pseudo R-Square,

suggesting approximately 10% of the variability was explained by this model. Albeit

given this weak degree of explanation, stomach content, gender, and length were

significantly related to water movement. The same arguments as Hypothesis 3, where

size and dominance drives fish distribution and piscivory, applies to Hypothesis 5. As

expected, size of tilapia was different in flowing vs. still water. The faster the movement

of the water, as well as the increased size of a fish, the more energy the fish needs to

utilize to maintain its physical position. This is especially so in the case of tilapia, who

have a morphology that suits slow moving or still water. Skewness of lengths suggests

asymmetrical distributions, and a t-test indicates the lentic and lotie groups are

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. statistically different. Albeit, methods differed in capture of fish between lentic and lotie

systems, and seining in lotie systems tend to capture smaller fish due to increased escape

ability of adults. This may have influenced the results.

Conclusion

Tilapia in the Muddy River system are highly piscivory. The frequency of piscivory

differed between fish obtained from the Muddy River and the Reid Gardner generating

station ponds, primarily lotie vs. lentic system. Piscivory also differed by gender, with

males showing a greater frequency of predation. Fish health was not a factor in degree of

piscivory. Other than the fact that tilapia were piscivorous, other factors should be

examined in more detail, specifically collecting more data and at different times of year

and day. Time of year likely plays a role in diet, based on developmental needs of the

individual as well as the ecology of the predator/prey relationship. Time of day likely

influences feeding rate, and presence of samples in the stomach depend on the difference

of time of consumption and time of digestion. As discussed, stable isotope analysis

would eliminate this bias.

Additional studies should also focus on habitat analysis. Examining spatial

distribution of tilapia based on habitat and distribution of prey species would especially

be illuminating. Vegetation cover maps could also be developed to monitor change in

cover relative to piscivory, and distribution of Poeciliids or native fish relative to the

cover would provide additional clues to why tilapia are piscivorous.

Another potential beneficial study would be a parasite survey of tilapia. Parasites

could potentially have wide-ranging impacts on the native fish in the system. If tilapia

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. harbor abnormal levels of mesenteric nematodes, and those tilapia were predated by a

definitive host such as an egret, native fish would be exposed to a greater number of

larval nematodes than normal. This exposure could increase chances that morbidity

would result in native fishes and they would be at greater risk to predation, as well as

have a lower fecundity. Identifying the parasites in the tilapia would provide more

information on their life cycle and potential threats to native fish.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX A

Invasion and Management Framework

Tilapia have been cultured since at least 4,000 years ago in Egypt (Lee and Newman,

1992), and elsewhere throughout temperate and tropical regions worldwide. This has

facilitated spread of the species into novel ecosystems, including Nevada. Chadderton

(2007) outlined a process of invasion by alien species (headers below), which was based

on Lodge et al. (2006). To facilitate management of these invasive species, actions

should address each appropriate stage of these processes.

Invasion Process

Present in Native Range (Pre-border)

Presence in native range is a factor dependant upon distribution and abundance of the

species in its native range, as well as its value in trade. For example, a species such as

zebra mussel {Dreissena polymorpha) would have a high risk of transport since it is

abundant and there is a greater risk of it being transported in ballast water. Species, such

as some cichlids that may have high value to aquarists and are accessible, may also have a

higher risk of being transported. This segment of the invasion process highly supports

movement of fish, as tilapia are abundant and used extensively for aquaculture. Specific

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. to tilapia and this invasion criterion, waters in the southeastern United States could be

considered ‘native’.

Species Transported to New Location (Post-border)

Two factors involve the probability of tilapia being transported into Nevada, their

ease of access and value as a food fish. Tilapia are readily available, and could be

purchased from fish farms, private individuals (i.e. fi-om the internet), or in live food

markets. They have several functions to which are beneficial to the buyer, ranging fi-om

cleaning vegetation from water systems to being a food fish. Nevada Administrative

Code (NAC) 503.110, Nevada Revised Statutes 501.105, 510.181, 503.597, and 504.295

prohibit importation and possession of live tilapia(Sarotherodon or Tilapia) or their

gametes. This effectively limits importation; however, it is not a complete control for

people who either intentionally or unintentionally break the law.

Species Introduced to New Site

Intentional stocking of fish is common in southern Nevada, mostly due to the

aquarium trade. Most stockings are assumed to be unwanted pets; however some

evidence points to stocking of fish species in order to harvest later, such as cichlids

(various species of the family Cichlidae) and giant gourami (Osphronemus goramy) at

Rogers Spring, Lake Mead National Recreation Area, Clark County, Nevada. Crayfish

are another example of a species stocked for later consumption; however, these are also

stocked to clean ponds and to provide forage for game fish. It is unlikely that tilapia are

stocked in the wild for any other reason than later consumption; however, they may also

be stocked illegally to clean ponds on private property. Given NAC 503.110, it would be

illegal to possess a tilapia in order to stock it.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Establishes Self-sustaining Population at New Site

This criterion involves requirement for stocking of enough fish to reproduce and

establish a self-sustaining population. This also requires a suitable gender ratio and

enough fish to prevent deleterious genetic bottlenecks based on effective population sizes.

In smaller environments, or with fish that are not actively predated on and school, fewer

fish may be required. In larger environments where fish are more dispersed, it would be

more difficult for fish to congregate to spawn, and there is less inherent risk. Tilapia tend

to congregate in suitable habitat during spawning, which increases reproductive

opportunities. This ultimately causes populations of tilapia to occur around these sites.

Although a generalization since the Muddy River is a small habitat, initially the tilapia

within the Muddy River were found in specific slow water habitats, where they

established self-sustaining populations.

Consolidation and Expansion of Range

Typically, successfully established introduced fish would establish in one area, then

spreading once reaching a specific density, presumably to lessen competition. Spread

may be fast or slow (i.e. Kolar and Lodge 2002) depending on environmental and life

history characteristics of the fish. The small scale of the Muddy River and the

potamodromous nature of tilapia facilitate spread of the species thoughout and beyond the

river. As density increases, more movement would occur, further expanding their range.

Impacts

Impacts occur throughout the invasion process; however, severity depends on the

species and the habitat. For example, introduction of a mosquitofish(Gambusia affinis)

would have less severity than largemouth bass in a pond, but more severity in a small

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. intermittent stream. Kolar and Lodge (2002) define two levels of impacts: Nuisance and

Non-nuisance. This distinction is useful in a predictive model; however, in actuality

there is a scale of impacts ranging fi-om slight to major. Introductions of some species,

such as invasive terrestrial weeds, may have imperceptible impacts, such as changing

allochthonous carbon, which could shift population dynamics. Major impacts are

noticeable, such as tilapia depressing numbers of native fish denuding stream vegetation.

Management Process

Prevention

Tilapia prevention is mandated by NAC 503.110, which removes the pathway of legal

tilapia escaping into the environment. Two types of illegal pathways occur: Intentional

and unintentional. It is likely most occurrences of tilapia in the State of Nevada are a

result of unintentional illegal activities by parties who do not know tilapia are prohibited

species. Prevention of this aspect, including all prohibited species, could involve

education of markets who sell live fish, as well as pet stores and pond supply retailers.

This education would need to occur at a regular basis to accommodate changing staff.

This would leave the only unintentional vectors individuals who buy tilapia from

individual breeders out of State. Controlling import of tilapia is more problematic, and is

limited by staff and funding relative to the relatively unlimited tilapia businesses

worldwide. Education campaigns and partnerships could be pursued with fish farming

and other commercial operations; however, the main deterrent in this case would be law

enforcement. It would be assumed that all possession of live tilapia after the initiation of

an education campaign would be intentional and law enforcement would provide a

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. deterrent. Fully investigating the chain of custody and movement of the fish, as well as

coordinating with other State and Federal agencies responsible for interstate commerce,

to fully prosecute perpetrators would help prevent illegal stocking.

Earlv Detection, Rapid Response, and Eradication

Early detection involves comprehensive fish surveys in suitable habitat to find initial

populations of tilapia or other invasive fish. Given the distribution of native fish in

Nevada, this is already occurring during normal activities by fisheries biologists.

Additional effort should be expended at sites that are easily accessible by the public, are

near or connected to ponds on private property, or are at sites near other infested areas.

Early detection would also involve rapid identification of the species, as well as

identification of the potential threats.

After detection of the species, it is critical to undergo a rapid response to the situation

(Anderson 2005). A multidisciplinary team should be identified to address the detection,

either an existing interagency management team or a new team consisting of relevant

stakeholders and appropriate science advisors. From this, a science-based response plan

would be developed based on consensus of the team. This plan would also involve

criteria for success. Some topics that may be included in the plan are control barriers,

pesticides, mechanical control, and survey methodology. By selecting relevant

stakeholders, funding would be facilitated to implement the plan. Anderson (personal

communication) suggested major factors in success of a rapid response and eradication of

Caulerpa taxifolia in California was communication and a mutually supportive

environment of the stakeholder team. This allowed the team to effectively collaborate in

obtaining grants and other funding to implement the plan.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Control and Slow Spread

One failure regarding tilapia management in the Muddy River was not controlling the

spread. This would have involved coordinating with local authorities, such as with the

Moapa Band of Paiutes or the Moapa Town Board, to install and/or manage barriers to

prevent movement of tilapia. Provided early detection of tilapia, in addition to rapid

response and eradication efforts should be underway to install barriers to prevent or slow

movement.

In addition to prevention of movement, limitation of breeding is also a strategy to

slow spread. Since tilapia are lek-based breeders, they require a relatively slow current to

m inim ize energy expenditure. Control methods could include removal of slack water

areas through hydraulic control. This would involve various structures to force water,

such as revetments.

Site-based Management

Site-based management is directed management to protect specific sites and/or

sensitive species. This is almost exclusively construction of barriers to prevent species

from accessing sensitive habitats. One example of this is construction of several barriers

on two tributaries of the Muddy River to prevent spread of tilapia into sensitive sites

containing Moapa dace. Another option is targeted removal at the selected site. This has

occurred in several tributaries of the upper Muddy River using the piscicide rotenone.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX B

Nevada Tilapia Management Plan

Development of a management plan to reduce or eliminate tilapia in Nevada is

problematic due to their widespread presence in Lake Mead. It is likely that tilapia would

pass through Hoover Dam, spreading into Lake Mohave and the rest of the lower

Colorado River. Other fish have been shown to pass through local dams, specifically

razorback suckers through Davis Dam at the tail of Lake Mohave (Gordon Mueller,

USGS, personal communication). This creates a large reservoir of the species where

control methods are unfeasible due to the nature of tilapia (i.e. difficult for anglers to

catch, actively avoid nets, huge area where they are distributed, etc...), as well as the lack

of staff and funding to carry out specific control methods. Therefore, the core of a

management plan should be isolation of these lakes and prevention of spread into new

habitats. It should also include targeted removal of tilapia from tributaries and other

manageable waters where they are known to occur.

Coordination

Anderson (2005) recommended as a first action in response to an infestation is to

develop a multidisciplinary team to deal with it. Currently endangered species Recovery

Implementation Teams take the lead for managing tilapia in specific river system.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Members are often in several teams, and are able to transfer knowledge from one team to

another. The core team dealing with tilapia is the U.S. Fish and Wildlife Service, U.S.

Geological Survey - Biological Resources Discipline, Nevada Department of Wildlife,

and the Southern Nevada Water Authority. Informing the process are collaborations with

Arizona Game and Fish Department, Utah Department of Natural Resources, and the

Washington County Water District, groups that have significant experience with

invasions and removal of red shiner (Cyprinella lutrensis) in the Virgin River. In

addition, efforts on the lower Virgin River have included the National Park Service, and

on the Muddy River, Nevada Power. Additional partnerships should be developed,

including the other municipal water agencies, the U.S. Department of Agriculture -

Wildlife Resources, and State water quality departments. State of Nevada Department of

Agriculture and Cooperative Extension Units likely field questions regarding tilapia, and

should be informed regarding current activities.

Barriers

Virgin River

Several impediments to tilapia movement already occur in the Virgin River, mainly

the irrigation diversion dams at Bunkerville and Mesquite. These ditches have return

flows that typically drop in elevation, forming a barrier; however, there are still locations

where these structures could facilitate swim-through systems for tilapia. Drop-structures

with concrete aprons should be constructed at all sites that do not prevent upstream

movement of fish. These structures should be developed as far outside of the floodplain

as possible to prevent erosion during floods and potential failure.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. In addition, mainstem barriers should be constructed consisting of twin low-head

dams in the lower portion of the Virgin River. This would create a small middle area

which could be regularly surveyed for fish, and if tilapia are discovered it would be easily

treated. It would also create insurance that if one barrier fails, the other one may not.

Muddv River

As with the Virgin River, several impediments and barriers already exist on the

Muddy River, albeit several are temporary. Currently, a permanent barrier is located on

the Moapa Band of Paiute reservation. Tilapia breached this barrier during maintenance

to remove sediment; however, the barrier itself prevents movement of fish. Two concrete

structures act as impediments to fish: One recently constructed barrier on Bureau of Land

Management property near the upper Muddy River, and the Nevada Power diversion dam

near the Warm Springs Road Bridge. These two structures act as barriers during normal

flow; however likely allow fish passage during storm events and higher flows. Two

smaller barriers currently sit on the upper Muddy River tributaries, and are designed to be

removed after they are not needed.

Management should include developing several barriers to prevent upstream

movement in the upper tributaries. After this is accomplished, rapid series of rotenone

treatments could be conducted to push tilapia downstream. This will be discussed below.

The morphology of the Muddy River in the Logandale/Overton area is not known, and

should be ascertained. Several barriers could be developed in this portion of the river

taking advantage of current irrigation structures (i.e. Bowman Reservoir diversion) or

erosion control stmctures. As with the Virgin River, a system of twin low-head dams that

are regularly monitored would be preferred.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Las Vegas Wash

No sensitive resources that could be affected by tilapia occur in the Las Vegas Wash;

however, it could function as a source population. In addition, tilapia may accumulate

and transport contaminants into Lake Mead from Las Vegas Wash. If management of

tilapia in Lake Mead is attempted, then Las Vegas Wash needs to be free of tilapia. If this

is determined to be a goal, then temporary barriers could be developed in its tributaries, as

well as a permanent barrier at the mouth of the Las Vegas Wash.

Treatments

Treatments using rotenone would complement barrier development. Treatment

protocol would depend on treatment plan developed based on specific site characteristics

at the time of treatment, as well as constraints identified during compliance with Federal

and State environmental permitting. If other chemicals are determined to be superior to

rotenone, and are labeled for fisheries management in waters containing food fish, then

those shall be used. Winter is the ideal time to treat, since they congregate in warmer

waters (Zale, 1987b). In addition, rotenone loses effectiveness in warmer waters. Kutty

and Sukumaran (1975) suggest that tilapia lose swimming ability with biocides, but could

recover immediately. This also is evident during temperature trials, where at low water

temperatures they lose swimming ability. Combined low temperatures and biocide would

have additional stress on tilapia.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Legislative

Current legislation regarding tilapia restrict possession and establish an unlimited bag

limit for number of tilapia in possession by anglers. This is already the ideal situation.

Additional legislation could increase penalties for possession and movement of live

tilapia, as well as fund additional law enforcement personnel. In addition, the NAC

should be revised to clearly state all genera in the tilapia family are prohibited, accounting

for future taxonomic revisions.

Education

Education is a critical step to prevent unintentional illegal possession of tilapia. At

the very minimum, pamphlets or fliers outlining regulations should be developed that

include contact information of the Nevada Department of Wildlife for additional

information. One pathway is to create an invasive species coordinator and team for

southern Nevada. This coordinator would develop a team to address aquatic invasive

species, primarily modeled upon the successful Southern Nevada Restoration Team. This

would create staff who would distribute information to the public. Additional resources

could be developed, including web pages, press releases, information videos, and

podcasts. Addition to the printed fishing regulation booklet could include incentives to

fish for tilapia, such as recipes.

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. VITA

Graduate College University of Nevada, Las Vegas

Shawn Christopher Goodchild

Home Address: 6132 Moonlight Dr Las Vegas, Nevada 89130

Degrees: Bachelor of Science, Zoology, 1993 Humboldt State University, Areata, California

Bachelor of Science, Wildlife Management, 1993 Humboldt State University, Areata, California

Thesis Title: Piscivory by Non-Native Blue Tilapia {Oreochromis aureus) in Clark County, Nevada

Thesis Examination Committee: Chairperson, Dr. Shawn Gerstenberger, Ph. D. Committee Member, Dr. Chad Cross, Ph. D. Committee Member, Dr. Lloyd Stark, Ph. D. Committee Member, Dr. Jim Deacon, Ph. D.

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