1

Parasites of native and non-native fishes of the Little Colorado River, Grand 

Canyon, Arizona. 

Anindo Choudhury1

, Timothy L. Hoffnagle2, and Rebecca A. Cole 

USGS-National Wildlife Health Center, 6006 Schroeder Road, Madison, WI 53711, 

U.S.A. 

2

Oregon Department of Fish and Wildlife, 211 Inlow Hall, Eastern Oregon University, La 

Grande, OR 97850 

Corresponding author: 

Rebecca Cole, USGS – National Wildlife Health Center, 6006 Schroeder Road, Madison, 

Wisconsin 53711, U.S.A. Phone: (608) 270 2468. E-mail: Rebecca_Cole@usgs.gov. 

1

Current address: Division of Natural Sciences, St. Norbert College, 100 Grant Street, 

DePere, Wisconsin 54115, U.S.A. 

Running Head: Fish parasites in the Little Colorado River.
 

 

2

ABSTRACT: A 2-year, seasonal, parasitological study of 1435 fish, belonging to 4 

species of native fishes and 7 species of non-native fishes from the lower Little Colorado 

River (LCR) and tributary creeks, Grand Canyon, Arizona, yielded 17 (possibly 18) 

species of parasites. These comprised 1 myxozoan (Henneguya exilis), 2 copepods 

(Ergasilus arthrosis and Lernaea cyprinacea), 1 acarine (Oribatida gen. sp.), 1 piscicolid 

leech (Myzobdella lugubris), 3 (possibly 4) monogeneans ( Gyrodactylus hoffmani, 

Gyrodactylus sp., Dactylogyrus extensus, and Ligictaluridus floridanus), 4 nematodes 

(Contracacecum sp., Eustrongylides sp. Rhabdochona sp., Truttaedacnitis truttae), 3 

cestodes (Bothriocephalus acheilognathi, Corallobothrium fimbriatum and 

Megathylacoides giganteum), and 2 trematodes (Ornithodiplostomum sp., 

Posthodiplostomum sp.). Of these, Rhabdochona sp. is the only adult parasite native to 

the LCR. Infection intensities (worm burden) of Ornithodiplostomum sp and B. 

acheilognathi were positively correlated with length of humpback chub, Gila cypha. 

Adult helminths showed a high degree of host specificity, the exception being B. 

acheilognathi, which was recovered from all fish species examined but was most 

abundant in cyprinids. Significantly higher abundance of B. acheilognathi in speckled 

dace, Rhinichthys osculus in the larger of the two creeks, Big Canyon Creek (BCC), may 

be related to higher population densities of dace. Abundance of B. acheilognathi in the 

humpback chub was highest in the fall and lowest in the summer, in both reaches of the 

LCR. This pattern was mirrored only partially by the tapeworms in speckled dace, and 

not by dace in the creeks, indicating some difference in transmission dynamics in the two 

fish hosts in different habitats. There were no major taxonomic differences in parasite 

assemblages between the two different reaches of the river (LC1 and LC2), mainly due to 

their connectivity, similar physical properties and, fish assemblages. Parasite community 

diversity was very similar in humpback chub, regardless of sampling site or time. 

Differences among sites (BCC, Salt Creek (SAC) , LC1 and LC2) can be related to the 

fish hosts present (or absent), and a result of the host specificity shown by the adult 

parasites. The parasite fauna of the LCR is numerically dominated by B. acheilognathi, 

and by the metacercariae of Ornithodiplostomum sp. The richest and most diverse 

component community occurred in a non-native species, the channel catfish, Ictalurus 

punctatus, but infracommunity species richness was highest in a native host, humpback 

chub. The generally species-poor native parasite fauna is due to the physical and 

biological characteristics of the LCR, namely the high travertine component and seasonal 

flooding. This in turn results in an invertebrate community which is low in species 

richness and diversity, as well as a species-poor native fish fauna. 

Key words: Parasites, fish, Little Colorado River, Grand Canyon, Bothriocephalus 

acheilognathi, Gila cypha. 

INTRODUCTION 

The closure of Glen Canyon Dam (Figure 1) in 1963 had a profound affect on the 

physical nature and ecology of the Colorado River in Grand Canyon, transforming a once 

seasonally warm, turbulent, muddy river, to one that is perennially cold and relatively 

clear. The flow of the river is now strictly regulated by the operation of the dam (National 

Academy of Sciences, 1991). There is also concern that introductions of non-native fishes 

into the system may be affecting native fish populations (Minckley, 1991; Marsh & 
 

 

3

Douglas, 1997; Fuller et al., 1999). At least 24 species of non-native fishes have been 

introduced into the Colorado River and its tributaries in Grand Canyon, and 13 have 

reproducing popluations (Valdez et al., in press). In contrast, the native fish fauna in 

Grand Canyon today is comprised of only four species: two catostomids, bluehead sucker 

(Catostomus discobolus Cope) and flannelmouth sucker (C. latipinnis Baird and Girard), 

and two cyprinids, speckled dace (Rhinichthys osculus Girard) and endangered humpback 

chub (Gila cyph Miller). 

Non-native fishes have also introduced potentially pathogenic fish parasites into 

the system. Two such parasites, the Asian fish tapeworm, Bothriocephalus acheilognathi, 

and the anchor worm, Lernaea cyprinacea, have been found in native and non-native 

fishes of the Colorado River and its tributaries in this region (Carothers et al., 1981; 

Brouder & Hoffnagle, 1997; Clarkson et al., 1997; Hoffnagle & Cole, 1999). These 

studies also indicate that the two parasites were more abundant in the Little Colorado 

River (LCR), the major, relatively unaltered, tributary of the Colorado River in Grand 

Canyon. Since the closure of Glen Canyon dam and the alteration of the Colorado River, 

the LCR has become increasingly significant in the biology of the native fishes in the 

canyon. The LCR is an important spawning and nursery site for all four native fish 

species, and the most important (and perhaps exclusive) spawning site for the endangered 

humpback chub (Robinson et al., 1996; Valdez & Ryel, 1997; Stone, 1999). In addition, 

seven non-native fish species also inhabit the LCR; This assemblage includes three 

cyprinids; common carp (Cyprinus carpio L.), fathead minnow( Pimephales promelas

Rafinesque), and red shiner (Cyprinella lutrensis, Baird and Girard); two ictalurid 

catfishes including channel catfish (Ictalurus punctatus Rafinesque) and yellow bullhead 

(Ameirus natalis Lesueur); and one cyprinodontid Fundulus zebrinus Jordan and Gilbert 

have reproducing populations. Stocked rainbow trout (Oncorhynchus mykiss Walbaum) 

from Lees Ferry reach, a 26 km tailwater immediately below Glen Canyon Dam, are not 

uncommon in the LCR. 

Although previous studies have reported the distribution and host-associations of 

B. acheilognathi and L. cyprinacea, the seasonal patterns of these pathogenic parasites as 

well as the parasite fauna of native and introduced fishes in Grand Canyon remain largely 

unknown. The importance of the LCR in sustaining the endangered humpback chub and 

at least two introduced pathogenic parasites known to parasitise it, and the presence of 

non-native fishes, made this river a natural site for a 2-year seasonal study on the parasite 

fauna. The study addresses the characteristics of the parasite fauna, host-parasite 

associations, and seasonal patterns of potentially pathogenic parasites in this ecosystem. 

MATERIALS AND METHODS 

Study Area 

The study area comprises the lower 18 km of the Little Colorado River to its confluence 

with the Colorado River at river kilometre (Rk) 98.6, within Grand Canyon, Arizona 

(Figure 1). The Little Colorado River, with headwaters in the White Mountains of 

northeastern Arizona, is the largest tributary of the Colorado River in the Grand Canyon 
 

 

4

area. It has a length of 536.3 km and a drainage area of 69,790 km2 (Oberlin et al., 1999). 

The major source of its perennial lower 22km stretch is Blue Springs and a series of 

smaller springs, which together discharge approximately 6.3m3

/s of 20oC water that is 

supersaturated with calcium carbonate and charged with free CO2. (Johnson & 

Sanderson, 1968; Cole, 1975). These carbonates give the LCR its characteristic aqua-blue 

colour during base flow periods. Deposits of carbonates (mainly CaCO3), known as 

travertine, form on the stream bottom, along stream banks, and on rocks, in turn 

encrusting vegetation and smothering the benthos. Travertine formations along the edges 

of riffles and rapids, result in low travertine ‘dams’, and impede flow. During periods of 

flooding, usually in the monsoon season (July-September) and in the Spring (FebruaryApril), the flow in the LCR can reach 3400m3

/sec (USGS www.usgs.gov/nwis/). 

Vegetation along the stream bank is generally sparse and consists of stands of Phragmites 

australis, Salix exigua and Tamarix chinensis. 

Three sampling reaches were initially chosen on the lower 18 km of the LCR, 

designated LC1, LC2 and LC3. The most upstream reach (LC3) is above the 

Atomizer/Chute Falls Complex which is 13.6 river kilometres (RK) upstream of the 

confluence with the Colorado River. This reach usually contains only speckled dace and 

non-native common carp and fathead minnow (Robinson et al. 1996; D. Stone, USFWS, 

personal communication), due to the waterfall barrier. This reach was only sampled once 

(Sept.1999) because river conditions did not permit helicopter landing on a regular basis. 

The middle reach (LC2, RK 10.6-11.5) is in the area of Salt Trail Canyon (RK 10.8) and 

contains all fish species that complete their life cycles in the LCR as well as occasional 

rainbow trout (Robinson & Clarkson 1992; U.S. Fish and Wildlife Service 1994). Two 

clear, saline creeks, Big Canyon Creek (BCC) in Big Canyon, Salt Creek (SAC) in Salt 

Canyon, and a saline spring (Big Canyon Springs) drain into the LCR in this reach. These 

tributaries were also sampled. The most downstream reach (LC1) is in the vicinity of 

Boulder Camp (RK 2) and ranged from RK 2.5 to the mouth (RK 0). This reach contains 

all species present in the LCR, including those that move into the LCR from the Colorado 

River, such as rainbow trout and brown trout, Salmo trutta (Robinson & Clarkson 1992; 

AZGF, 1996; Brouder & Hoffnagle 1997). Nets and other sampling gear (see below) 

were set within a 1 km stretch at each reach. 

Sampling 

 

Fish: Eleven fish species were sampled including all 4 native fishes and 7 non-native 

species (Tables I, II). The term ‘non-native’ refers to fish species that are not native to 

the Colorado River system, and consequently includes fishes that are native to other parts 

of the U.S. (channel catfish, red shiners etc.), as well as fishes that were originally 

introduced into the U.S. from Europe (e.g., common carp). Most species were caught 

using medium (45 cm) and large (91cm) hoop nets (each with 10cm mouths and 6 mm 

mesh), and minnow traps (each with 25 mm mouth and 3 mm mesh). Six hoop nets of 

each size were deployed in each reach. Minnow-traps were deployed in pods of 5 traps, 

comprising a total of 4 or 5 pods in each reach (LC1 and LC2). One or 2 pods of minnow 

traps were set in the tributary creeks (BCC, BCS and SAC) and only minnow traps were 

used at these sites. In addition, baited trot-lines were used to catch channel catfish and 
 

 

5

rainbow trout. These two species were also taken by angling. Gill nets yielded few or no 

fish and were not used after September 1999. Seines were used less frequently to catch 

very small fish and mainly when the yield from other sampling gear was low. Hand held 

sling spears and spear guns were used to capture carp trapped in shallow pools. Nets and 

traps were checked once a day and fish were brought back live to camp for necropsy 

work. In total, 1435 fish were necropsied for parasites. The relatively low numbers of the 

endangered humpback chub examined were due restrictions on both sample size and fish 

size (U.S. Fish and Wildlife Service Permit No. TE008513-0). During each trip (sampling 

period), a maximum of 10 individuals could be taken for necropsy work from each of the 

two reaches, LC1 and LC2, of the river, and sampled fish had to be less than 150 mm (i.e. 

juveniles). Two larger fish (190 mm and 232 mm) that had died during the sampling were 

also examined and included in the analysis. This quota of 20 fish (10 per reach) per trip 

was met in most cases (Table II). 

Fish were processed shortly after capture, or were held in 19 litre buckets with 

aerated water, or in live cars in SAC or in the LCR, before processing. Fish were weighed 

and measured (total lengths), and necropsied using a binocular dissecting microscope. 

Parasites: Parasites were collected and first briefly washed in saline or clear LCR water 

(naturally saline). Procedures for killing and preserving parasites were conducted as 

outlined by Van Cleave and Mueller (1932) and Pritchard and Kruse (1982). Briefly, 

parasites were killed and simultaneously fixed in steaming 10% buffered (or nonbuffered) formalin (for platyhelminths and occasionally nematodes) or hot 70% ethanol 

(for nematodes only). Hot fixatives were used to fix and collect enough material for 

taxonomic work, but once the fauna was known, hot fixation was discontinued and 

parasites were fixed in unheated fixatives. When monogeneans were numerous, the gillarches were separated and placed in dilute (1%) formalin for 6-12 hours, causing 

dissociation of the epithelia along with the monogeneans. The monogeneans, mostly free, 

were collected from the dissociated epithelial debris. Copepods and myxozoan cysts were 

collected in 70% ethanol. Platyhelminths were stained in acetocarmine or Ehrlich’s 

haematoxylin, dehydrated, cleared in xylene or methyl salicylate, and permanently 

mounted on slides, in balsam. Nematodes were cleared in a solution of 5% glycerine in 

70% ethanol by evaporation of ethanol and water. Copepods were initially cleared in hot 

lactophenol and temporarily mounted on slides and later washed in 70% ethanol, stained 

in acetocarmine, and permanently mounted in balsam, on slides. Parasites were identified 

using Hoffman (1999) and museum specimens for comparison. The following species 

(accession numbers are in parentheses) are being deposited in the U.S. National Parasite 

Collection (USNPC), Beltsville, Maryland and Harold W. Manter Laboratory (HWML) 

collection, University of Nebraska, Lincoln, Nebraska: Henneguya exilis (USNPC 

XXXX), Ergasilus arthrosis (USNPC XXXX), Lernaea cyprinacea (USNPC XXXX), 

Oribatida gen. sp.(USNPC XXXX, HWML XXXX), Myzobdella lugubris (USNPC 

XXXX), Gyrodactylus hoffmani (USNPC XXXX, HWML XXXX), Gyrodactylus

sp.(from SPD) (USNPC XXXX), Dactylogyrus extensus (USNPC XXXX), 

Ligictaluridus floridanus (USNPC XXXX, HWML XXXX), Contracacecum sp. 

(USNPC XXXX, HWML XXXX), Eustrongylides sp.(USNPC XXXX, HWML XXXX), 

Rhabdochona sp. (USNPC XXXX, HWML XXXX), Truttaedacnitis truttae (USNPC 
 

 

6

XXXX, HWML XXXX), Bothriocephalus acheilognathi (USNPC XXXX, HWML 

XXXX), Corallobothrium fimbriatum (USNPC XXXX, HWML XXXX), 

Megathylacoides giganteum (USNPC XXXX, HWML XXXX), Ornithodiplostomum sp. 

(USNPC XXXX, HWML XXXX) and Posthodiplostomum sp. (USNPC XXXX). 

Temperature recording 

Water temperature was recorded with programmable stowaway Hobo® Temp 

temperature data loggers (Onset Computer Corporation, Bourne, Massachusetts) in 

submersible waterproof, polycarbonate cases. Rocks were used as anchors to ensure the 

encased data loggers remained submerged at all times. Data loggers were programmed to 

record temperatures every 6 hours or every 12 hours (shorter intervals for longer 

recording duration, since this affects the memory capacity of the loggers), and deployed 

in SAC and BCC to record temperatures continuously between September 27, 2000 and 

June 6, 2001. Data loggers were retrieved during each sampling trip and new ones were 

deployed in their place. The BoxCar Pro 4.0 Programme (for Windows) (Onset Computer 

Corporation) was used to programme and activate the Hobo Temp data loggers and to 

download data from them. Raw data were subsequently exported to a Microsoft Excel 

spreadsheet. Temperature data loggers were not deployed in the LCR between sampling 

trips since periodic flooding events would have them washed away. Water temperature in 

the LCR from 1998 and 2001 was recorded by the USGS temperature gauge 

approximately 1 km upstream from the confluence with the Colorado River (William 

Vernieu, USGS Grand Canyon Monitoring Research Center, Flagstaff, Arizona, 

unpublished data). 

Analyses: The terms abundance, intensity, and prevalence follow that of Margolis et al., 

(1982). Species richness refers to the number of species in an assemblage or community. 

Infracommunity refers to the community of parasite species in an individual host, while 

component community refers to the assemblage of parasites recovered from a sample of a 

host species. A compound community is the assemblage of parasites in all host species at 

a locality (Sousa, 1994). Species richness of gut helminth communities have also been 

calculated separately because it provides a basis for comparison of parasite community 

patterns as they relate to trophic-web dynamics, and because parasite assemblages in the 

gut are due to a common process (ingestion). The terms richness and diversity follow 

usage in Magurran (1988) and Peet (1974). Regression analyses and Pearson’s 

correlation coeffecient were employed to examine relationships between fish length, 

parasite burden (total number of parasites in an individual fish), and infracommunity 

parasite species richness . Parasite community parameters examined include total 

component community richness, component community diversity (Shannon-Wiener’s 

index) and mean (infracommunity) richness. Comparisons of richness were made using 

the Mann-Whitney U-Test and correlations were examined using Pearson’s correlation 

and Spearman’s rank correlation (Zar, 1996). Results of all tests were considered 

significant at P < 0.05. 
 

 

7

RESULTS 

Fish 

In total, 1435 fish belonging to 11 species were examined in this study (Table I). Of 

these, the 4 native fishes made up 67.4% of the total sample. Speckled dace comprised 

43.9% of the total sample. All but one rainbow trout were caught from the LCR (Table 

II). Similarly, humpback chub were rarely caught from sites other than the LCR (LC1 and 

LC2). Big Canyon Creek and Salt Creek provided mainly speckled dace and occasionally 

a few other smaller species. Big Canyon Springs yielded mainly plains killifish and 

speckled dace. In general, the two reaches of the LCR (LC1 and LC2) consistently 

yielded a major proportion of the samples (Figure 2) as well as the richest assemblage of 

fish species throughout the study (Figure 3). High turbidity during the September 1999 

sampling made collection of fish difficult. A sudden flooding event while sampling LC1 

forced an early termination of sampling. This is reflected in the poor returns from 

sampling in the LCR during that time. 

Most species were sampled over a considerable size range (Table I). However, 

most (> 90%) of the flannelmouth suckers examined were < 100 mm long. Similarly, 

most of the bluehead suckers were also immature individuals. The majority of carp 

samples were concentrated in one sampling period (June 2000) (Table II) and consisted 

primarily of small immature individuals. Other fish species, including most of the 

channel catfish examined, were taken as older juveniles and adults (see lengths and 

weights in Table II). 

Some fish were not caught in each reach but rather were collected predominately 

at specific reaches. Rainbow trout were caught mostly at the downstream reach, LC1 

(Table II). Species such as the red shiner, yellow bullhead, and common carp were 

caught more sporadically. 

Parasites 

A total of 17 species of parasites was recovered from fishes in this study (Tables III, IV). 

The species of monogenean found in speckled dace resembles closely the species found 

in fathead minnow, and may be conspecific with it, but has been treated separately due to 

condition of samples. Eleven of the 16 metazoan parasites were adults. Of these, 

Rhabdochona sp. was the only adult parasite native to the LCR. All other adult parasite 

species were most likely introduced with their fish hosts. Parasites found as larval or 

juvenile stages mature in fish-eating birds (i.e., 2 nematodes, Contracacecum sp., 

Eustrongylides sp, and 2 trematodes, Ornithodiplostomum sp., Posthodiplostomum sp.), 

in channel catfish (i.e., plerocercoids of Corallobothriinae), or in the aquatic environment 

as free living adults (i.e. juvenile mites on gills). 

The degree of host specificity varied but was highest in most of the adult parasites 

(Tables III, IV). The monogeneans were specific for their fish hosts. The nematodes, 

Truttaedacnitis truttae and Rhabdochona sp were specific for rainbow trout and speckled 

dace respectively. The cestodes Corallobtohrium fimbriatum and Megathylacoides 

giganteum, the myxozoan Henneguya exilis, and the leech Myzobdella lugubris, were 
 

 

8

found only in channel catfish. Bothriocephalus acheilognathi was recovered in all fish 

species examined, but was rare in the catostomids, rainbow trout and ictalurids (channel 

catfish and yellow bullhead). The species of Rhabdochona from speckled dace appears to 

be previously unknown and is being described elsewhere. Gravid females of this 

nematode were not found in any other fish host in the LCR. 

Component community richness was highest in channel catfish (7 species) but 

infracommunity richness was highest in humpback chub (1.86) and channel catfish (1.23) 

(Figure 4). There was no common pattern of seasonal change in infra-community 

richness in the different fish species examined (Figure 5), except that both humpback 

chub and speckled dace showed lowest infra-community richness values in the summer 

(June) sampling periods in both 1999 and 2000. The component and infra-communities 

of the two native sucker species were consistently species poor (Table III, Figures 4, 5). 

Diversity of parasite component communities was remarkably uniform in humpback chub 

over the study period (Table V), compared to assemblages in speckled dace and channel 

catfish. Furthermore, the overall diversity of chub parasite communities in LC1 and LC2 

were nearly identical (Table VI). 

Bothriocephalus acheilognathi reached its highest abundance in humpback chub 

(Table III, Figure 6). Abundance of B. acheilognathi showed a clear seasonality in 

humpback chub, and was significantly lower in the summers than in any other time in this 

study (Figure 7). Abundance values of the tapeworm were also consistently (and in most 

sampling periods significantly) higher at LC2 than at LC1 (Figure 7). Except for 

abundance values of B. acheilognathi in chub from LC1 during April 2001, the two 

reaches of the river (LC2 and LC1) showed similar seasonal patterns (Figure 7). This 

pattern was not mirrored by the infections of B. acheilognathi in speckled dace from any 

of the sampling sites (Figure 8). Abundance of B. acheilognathi infections in speckled 

dace was significantly higher in Big Canyon Creek throughout the study than in any other 

location (Figure 9). Of the two creeks, a seasonal pattern of tapeworm abundance was 

only observed in Big Canyon Creek, where abundance values of the tapeworm were 

significantly higher in the spring and lower in the fall and summer (Figure 9). In total, 

3930 individuals of B. acheilognathi were recovered in this study. Of these, 2130 (or 

54.1%) were found in humpback chub. Regression analyses showed that, over all, there 

was a positive correlation between length of humpback chub and tapeworm burden (R2

 = 

0.12), but R2 values varied from as low as 0 (Sept.1999) to 0.19 (April 2000). 

Ornithodiplostomum sp. occurred consistently, and also followed trends in 

humpback chub similar to those seen with B. acheilognathi (Figure 10). 

Ornithodiplostomum sp. also shows significantly higher abundance values in Big Canyon 

Creek than elsewhere (Figure 11). Regression analyses indicated that infections (worm 

burden) of Ornithodiplostomum sp. were positively and significantly correlated with 

body size of humpback chub (R2

 = 0.28). The R2 values varied between a low of 0.03 

(Sept. 1999) and a maximum of 0.75 (Sept 2000) indicating this relationship fluctuates 

through time. 
 

 

9

Temperature 

Temperature profiles were generated from the temperature data recorded by the Hobo 

Temp data loggers for BCC and SAC (Figure 12), and for the LCR from the data 

recorded by the USGS temperature data logger (Figure 13). The sharp decrease in 

temperatures in both SAC and BCC near the end of October (Figure 12) was possibly due 

to a flooding event in Salt Canyon and Big Canyon. 

DISCUSSION 

Unlike most other investigations of fish parasite communities, this study provided 

us with a dataset of the entire fish parasite community from one river, and allowed us to 

address questions relating to parasite community structure, as well as historical and 

contemporary processes affecting parasite community richness and diversity. 

Fifteen of the 17 species of parasites identified in this study (Tables III, IV) are 

first published records for the LCR and Colorado River in Grand Canyon. Only 

Bothriocephalus acheilognathi and L. cyprinacea have been previously reported from the 

LCR and other sites in the Grand Canyon (Carothers et al., 1981; Brouder & Hoffnagle, 

1997; Clarkson et al., 1997; Hoffnagle & Cole, 1999). The parasite assemblage is species 

poor and unique in having only one species of native adult helminth (i.e., the ‘new’ 

species of Rhabdochona in speckled dace). The parasite assemblage is numerically 

dominated by parasites (B. acheilognathi) that have been presumbably introduced with 

non-native fish, or by larval parasites (Ornithodiplostomum sp.) of fish eating birds. The 

host specificity and preferences of the parasite species observed in this study follow 

patterns of host-associations elsewhere (Hoffman, 1999). Although B. acheilognathi was 

found in all fish species examined, it clearly has a predilection for cyprinids. This is in 

keeping with its host preferences (Bauer, 1991; Kennedy, 1991; Scholz, 1997, 1999; 

Hoffman, 1999), and is not surprising since it is originally a parasite of cyprinids in 

northeast and far-east Asia (Yeh, 1955; Bauer, 1991; Scholz, 1997; Hoffman, 1999). 

More recently, the parasite has also been reported from the roundtail chub (G. robusta

Baird and Girard) in a hatchery in Arizona (Brouder, 1999) and in wild populations of the 

arroyo chub (G. orcutti Eigenmann and Eigenmann) (Kuperman and Mattey, pers. 

comm.). In the U.S., the tapeworm also infects the more distantly related 

cyprinodontiforms such as the mosquito fish (Granath and Esch, 1983a), and the plains 

killifish demonstrated in this study and by Brouder and Hoffnagle (1997). 

The parasite fauna in the LCR is also unusual in lacking adult trematodes. This 

absence, and the presence of larval strigeids only, can be related to the presence of only 

one species of mollusc, a species of Physa, in the LCR and its tributaries (unpublished 

observations). Physa spp. are known to be first intermediate hosts of strigeids such as 

Ornithodiplostomum spp. and Posthodiplostomum spp. In contrast, Physa spp. are not 

known to be intermediate hosts of the typical digenean fauna of North American 

freshwater fish parasites (e.g. Allocreadiidae, Gorgoderidae, Lissorchiidae in 

catostomids, Macroderoididae etc.). Furthermore, the benthic macroinvertebrate fauna of 

the LCR is severely affected by the unstable nature of their habitat. Periodic flooding 
 

 

10

causes periodic reduction of some or most of this fauna from the river. Recolonization is 

made difficult by extensive travertine deposition which smothers the benthos and 

encrusts vegetation and rocks. 

The physical nature of the LCR has likely had a long-standing influence on the 

ability of invertebrates to periodically colonise the river, and on the development of 

trophic webs in the system. The relatively short links in this trophic web are reflected in 

the parasite fauna. Four species (Contracaecum sp., B. acheilognathi, C. fimbriatum, and 

M. giganteum) are transmitted to their fish hosts by copepods. Ten species (H. exilis , L. 

cyprinacea, Ergasilus arthrosis., M. lugubris, Ornithodiplostomum sp., 

Posthodisplostomum sp., the oribatid mite, and the 3 species of monogeneans) infect or 

infest their hosts by direct attachment of larvae or by penetration. Seven of these do not 

utilise any prior intermediate host. Two species, Rhabdochona sp. and Eustrongylides sp. 

are transmitted by macroinvertebrates in the diet. Eustrongylides spp. utilise tubificid 

oligochaetes as intermediate hosts as do myxozoans, while Rhabdochona spp. commonly 

have some insect larvae (e.g., ephemetropterans) as intermediate hosts (Anderson, 2000). 

The physical nature of the aquatic environment may explain why the ectoparasites were 

so sporadic in occurrence and relatively rare in the system, and why there are so few 

parasites with a riverine benthic life cycle. 

The physical, and hence biotic, characteristics of the LCR also explain why the 

two native catostomids (bluehead sucker and flannelmouth sucker) have unusually 

depauperate parasite faunas. Catostomids generally possess a rich and taxonomically 

diverse parasite fauna comprising of monogeneans , digeneans , acanthocephalans and 

nematodes (Margolis & Arthur, 1979; McDonald & Margolis, 1995; Hoffman, 1999). 

The characteristic digenean fauna of catostomids utilise sphaeriid bivalves or ancylid 

snails as first intermediate hosts (Hoffman, 1999), neither of which are known from the 

LCR. The humpback chub also has no parasite that could be considered native to the 

LCR. Higher infracommunity richness in humpback chub was a result of the high 

prevalences of B. acheilognathi and Ornithodiplostomum sp. The lack of information on 

the parasite fauna of these fishes in the Colorado River main stem makes it impossible to 

determine whether these native LCR fishes possess more diverse parasite faunas. If they 

do, then the parasites possess the potential to serve as natural markers in understanding 

the movement of these fishes between the LCR and the Colorado River. 

 The parasite fauna of the non-native fishes is also species poor and reduced in 

taxonomic diversity compared to the fauna in their native range. At first glance, this is in 

keeping with the generalisations by Dogiel (1964) and Dogiel et al. (1961) that host 

species that are introduced into areas outside their native ranges undergo a reduction in or 

loss of their parasite fauna. Rainbow trout have only one parasite specific to them (and 

other salmonids) viz. Truttaedacnitis truttae (Hoffman, 1999) in the LCR. Since this trout 

is an occasional migrant and temporary resident in the LCR, and is mainly confined to the 

lower reaches of the river (Tables III, IV), it is likely that its parasite fauna in the 

Colorado River is equally species poor. It is most probable that rainbow trout were 

stocked from one or several hatcheries, in which case it is not a true case of translocation 

and Dogiel’s generalisations, or those of Kennedy and Bush (1994), cannot be easily 
 

 

11

applied. T. truttae has been found in trout in hatcheries, and could have survived the 

translocation process. The finding of T. truttae of various sizes in rainbow trout in the 

Grand Canyon has bearing on the biology and taxonomy of this parasite. Brook lampreys 

are considered to be obligate intermediate hosts of this parasite in Europe, and brown 

trout in Europe become infected by ingesting lampreys (Moravec, 1994). As there are no 

lampreys in the Colorado River in Grand Canyon, some other intermediate host is 

involved. Choudhury and Dick (1996) showed that there was a morphological difference 

between North American and continental European T. truttae. This study highlights the 

fact that there are biological differences as well. 

Channel catfish, which possess a characteristic parasite fauna within their native 

range (Hoffman, 1999; Pérez-Ponce de León & Choudhury, 2002), are infected in the 

LCR by 4 species that are specific to them and other Ictalurus spp.:(i.e.,H. exilis, C. 

fimbriatum, M. giganteum, and L. floridanus). In addition, the leech M. lugubris and the 

parasitic copepod, E. arthrosis, also appear to be typical of channel catfish (Roberts, 

1970; Hoffman, 1999). Channel catfish were introduced from an unknown source into the 

lower Colorado River basin around 1890 (Miller and Alcorn, 1943, U.S. Fish and 

Wildlife Service, 1980). As result it is impossible to conclude with certainty whether 

their parasite fauna in the LCR indicates a significant reduction or retention of parasites 

that were introduced with them. However, in native waters, channel catfish are 

parasitised by several digeneans that are specific to ictalurids: the unrinary bladder fluke 

(Phyllodistomum lacustri), the intestinal flukes (Crepidostomum ictaluri and 

Polylekithum ictaluri) and two macroderoidids (Alloglossidium corti and A. geminum). 

None of these species are present in the LCR. At least part of the reason for this may lie 

in the abiotic conditions, and the resulting biotic composition, of the LCR. Most of these 

trematodes utilise intermediate mollusc hosts that are not present in the LCR. Although 

the yellow bullhead is also an ictalurid, it did not share any parasites with channel catfish. 

This is likely due to the fact that the typical cestode fauna of Ameiurus spp. comprises 

corallobothrines such as Corallotaenia minutia, and C. parafimbriatum, not C. 

fimbriatum or M. giganteum. Likewise, Ameiurus spp. have their own specific species of 

Ligictaluridus (Hoffman, 1999), while the myxozoan, H. exilis appears to be specific to 

the channel catfish. 

The abundance of B. acheilognathi in non-native cyprinids, such as fathead 

minnows, red shiners, and small carp, as well as in the plains killifish, implicates any of 

these fish species as hosts that introduced the tapeworm into the LCR. It is possible that 

bait bucket transfers into the upper reaches of the LCR or into the Colorado River may 

have been responsible for the introductions. The data on B. acheilognathi infections in 

this study (Tables III, IV, Figures 6, 7, 8) demonstrate the high colonising potential of 

this parasite. This is in keeping with its establishment in non-native areas worldwide 

(Boomker et al., 1980; Bauer, 1991; Kennedy, 1991; Esch & Fernández, 1993; Heckman 

& Furtek, 1993; Font & Tate, 1994; Pérez-Ponce de León et al., 1996; Dove et al., 1997; 

Hoffman, 1999). Comparisons of B. acheilognathi infections with past studies (Brouder 

& Hoffnagle, 1997; Clarkson et al., 1997) show that the parasite is well established in 

native cyprinids (i.e., humpback chub and speckled dace). Humpback chub appears to be 

the most important host in the LCR (Figure 7). Although chub comprised only 8% of the 
 

 

12

total number of fish examined in this study, it harboured 54.1% of the tapeworms 

recovered. These findings are in contrast to those of Dove (1998), who found that nonnative carp were the main hosts of B. acheilognathi in Australia, both in terms of 

numbers and biomass of the tapeworm. Dove predicted that B. acheilognathi required 

carp as a reservoir host for the infections to be maintained in native fishes in Australia. 

This is possibly due to the fact that Australia has a unique and isolated freshwater fish 

fauna, devoid of native cyprinids (Nelson, 1994). Our study suggests that B. 

acheilognathi would persist and maintain its presence in the LCR even in the absence of 

carp or other non-native hosts. 

A combination of behavioural and physiological traits may make humpback chub 

suitable hosts. First, chub are highly omnivorous (Valdez & Hoffnagle, 1999), and 

zooplankton comprises a large percentage of their diet (AZGF, 1996). They commonly 

feed on copepods even as larger juveniles. Second, as a native species, the humpback 

chub is well adapted to exploit habitat and food in the LCR. Speckled dace are also native 

but they are primarily benthivores (AZGF, 1996), as reflected by the presence of 

Rhabdochona sp. Although dace are suitable hosts of B. acheilognathi, their foraging 

behaviour may prevent heavier infections. Finally, the humpback chub is a much larger 

species than the speckled dace. While this in itself should not necessarily mean higher 

infections in humpback chub, ingestion of large concentrated amounts of zooplankton 

indirectly through predation on small planktivorous fish, and its omnivorous feeding in 

the water column may expose it to infected zooplankton at all stages in its life history. 

However, the restriction of our sampling to chub less than 150 mm prevents firm 

conclusions about the nature of chub-tapeworm interactions or about the transmission 

dynamics of B. acheilognathi in larger fish. 

Seasonal patterns of infection with B. acheilognathi were observed in humpback 

chub in both reaches (LC1 and LC2) of the river (Figure 7). The general trend was lowest 

abundance in the summer months with significantly higher abundance values in the 

following fall (September). Temperature related dynamics of B. acheilognathi have been 

demonstrated in the past (Granath & Esch, 1983a, b; Marcogliese & Esch, 1989a, b). The 

LCR provides the tapeworm with the temperatures necessary for its development and 

maturation, mainly during the summer months (Figure 12), but the low abundance of 

worms in the summer (Figure 7) may be related to seasonal changes in copepod 

abundance (see Marcogliese and Esch, 1989a). In addition to seasonal patterns, the data 

also revealed spatial differences in abundance of B. acheilognathi infections in humpback 

chub (Figure 7). The higher abundance values of tapeworm infections in the upper reach 

(LC2) as compared to the LC1 may be due to the presence of both creeks (BCC and 

SAC) and Big Canyon Springs at LC2. The creeks and Big Canyon Springs provide 

landscape diversity and ideal habitat for copepods. Of these habitats, Big Canyon Creek 

may be particularly important. Although humpback chub were rarely caught in Big 

Canyon Creek (2 of 116 fish, with 243 and 45 tapeworms), access to such creeks may 

expose fish to functional reservoirs of infection, maintained by the dace in the creeks. 

Furthermore, the creeks may serve as refugia for copepods, intermediate hosts of B. 

acheilognathi, during flooding episodes in the LCR and as such serve as sources for the 

rapid colonisation by copepods of the near shore backwater environments in the LCR 
 

 

13

after base flows return to normal levels. The absence of such creeks in the lower reaches 

of the LCR precludes such opportunities. 

Significantly higher abundance of B. acheilognathi in speckled dace in the larger 

of the two creeks, BCC (Figure 9), is possibly related to the greater population size of 

dace (mean CPUE: 180.1 dace / 24 hrs in BCC vs. 52.2 dace / 24 hrs in SAC) and 

potentially larger populations of copepods. Salt Creek apparently provides year-round 

temperatures suitable for transmission of the tapeworm, while water temperatures in Big 

Canyon Creek show greater seasonal fluctuation (Figure 12). In Big Canyon Creek, the 

pattern clearly indicates low points in the summer and fall, which contrasts with the 

pattern shown by the parasite in dace in the LCR (Figure 8), where high fall (September 

2000) values are flanked by low summer and spring values. A temperature-dependent 

increase in spring infection values (abundance) from those of the previous respective fall 

lows (Figure 8) is supported by the temperature profile of Big Canyon Creek (Figure 12). 

Metacercariae of the bird fluke, Orinthodiplostomum sp., comprised the other 

abundant parasite in this system. An increase in abundance in the fall from preceding 

summer levels and a decrease in the subsequent spring is evident in both seasonal cycles 

of this study (Figure 10). Significantly higher abundances of Ornithodiplostomum sp in 

dace were also found in the larger of the two tributary creeks (BCC) (Figure 11). Whether 

these seasonal and habitat patterns correlate with habitat use by nesting or feeding 

piscivorous birds and (or) the abundance of the mollusc intermediate host (Physa sp.), is 

open to further investigation. The metacercariae have been shown to alter visually 

mediated behaviour in fish, increasing risk to predation and impacting foraging success 

(Sho & Goater, 2001). Its presence in chub and dace indicates that this parasite needs to 

be monitored as well. 

This study demonstrates the intricate interplay between hosts, parasites and 

habitat in a species poor, yet clearly complex system. The high colonising potential of B. 

acheilognathi is reflected in its ability to infect a variety of fishes and habitats in the LCR 

and in its abundance in two native cyprinids. The study also demonstrates the importance 

of perennial tributary creeks as reservoir areas for copepods and fish, and consequently 

for B. acheilognathi. These facts make monitoring of this parasite an important issue in 

maintaining the biotic integrity of the Grand Canyon ecosystem. Sustained and continued 

studies on B. acheilognathi and other potentially pathogenic parasites 

(Ornithodiplostomum sp., L. cyprinacea) would allow the impact of these parasites on 

native fish species to be better understood as management and remedial activities are 

planned. Finally, the scope of such studies must be broadened to include the Colorado 

River main stem, its tributaries, and warmer feeder creeks that may be critical to success 

of these parasites. Monitoring fishes of the main stem would provide information on the 

entire distribution of these parasites within the Grand Canyon and document if the 

parasites spread, as alternate flow regimes from Glen Canyon Dam and other 

management strategies are executed. 

 
 

 

14

ACKNOWLEDGEMENTS 

Numerous people contributed to the success of this project. We gratefully acknowledge 

the following: Dave Baker, Karl Hayden, L.B. Myers, Gary Burton, Lara Myers, Bruce 

Michael, Wes Shoop, Scott Hale, Scott Hansen, Anson Koehler, Jonathan C. Cambron, 

Ben Galuardi, and Bobbi Hervin, for volunteering their hard work and assistance in the 

field, the field personnel and biologists of the U.S. Fish and Wildlife Service (USFWS), 

Flagstaff, Randy Van Haverbeke, Dennis Stone, Lew Coggins, and Ben Galuardi for their 

help and advice, Scott Reger and Jodi Niccum, Arizona Game and Fish Department 

(AGFD), Flagstaff, and Bill Persons, AGFD, Phoenix, for logistic support, and Carol 

Fitzinger, Grand Canyon Monitoring Research Center (USGS-GCMRC) for loaning the 

satellite phone. AC is deeply indebted to Dave Baker for his help during the June 1999 

sampling trip, and to Scott Hansen for his outstanding technical assistance on this project. 

We also thank Bill Vernieu, USGS-GCMRC, Flagstaff, Arizona, for the unpublished 

LCR temperature data, and the USFWS (#TE008513-0), NPS –Grand Canyon (#9902-

04-002 ), AGFD (#SP920526) and the Navajo Nation ( #030301-025) for sampling 

permits. Finally, we also acknowledge the staff of the USGS-National Wildlife Health 

Center for logistic support. The project was funded by the U.S. Geological Survey 

(USGS) Southwestern Initiative. 
 

 

15

References

Anderson, R.C. (2000). Nematode parasites of vertebrates. Their development and 

transmission. CABI Publishing, Wallingford, U.K., 650pp. 

Arizona Game and Fish Department. (1996). The ecology of Grand Canyon backwaters. 

Final Report. Submitted to Glen Canyon Environmental Studies, U. S. Bureau of 

Reclamation, Flagstaff, AZ. Arizona Game and Fish Department, Phoenix. 

Bauer, O.N. (1991) Spread of parasites and diseases of aquatic organisms by 

acclimatization: a short review. Journal of Fish Biology 39, 679-686. 

Boomker, J., Huchzermeyer, F.W. & Naude, T.W. (1980). Bothriocephalosis in the 

common carp in the eastern Transvaal. Journal of the South African Veterinary 

Association, 51, 263-264. 

Brouder, M.J. & Hoffnagle, T.L. (1997). Distribution and prevalence of the Asian fish 

tapeworm, Bothriocephalus acheilognathi, in the Colorado River and tributaries, Grand 

Canyon, Arizona, including two new host records. Journal of the Helminthological 

Society of Washington 64, 219-226. 

Brouder, M.J. (1999). Relationship between length of roundtail chub and infection 

intensity of Asian fish tapeworm Bothriocephalus acheilognathi. Journal of Aquatic 

Animal Health 11, 302-304. 

Carothers, S. W., Jordan, J.W., Minckley, C.O. & Usher, H.D. (1981). Infestations of the 

copepod parasite, Lernaea cyprinacaea, in native fishes of the Grand Canyon. National 

Park Service Transactions and Proceedings Series 8, 452-460. 

Clarkson, R.W., Robinson, A.T. & Hoffnagle, T.L. (1997). Asian tapeworm 

(Bothriocephalus acheilognathi in native fishes from the Little Colorado River, Grand 

Canyon, Arizona. Great Basin Naturalist 57, 66-69. 

Choudhury, A. & Dick, T.A. (1996). Observations on the systematics and biogeography 

of the genus Truttaedacnitis (Nematoda: Cucullanidae). Journal of Parasitology, 82, 965-

976 

Cole, G. A. (1975). Calcite saturation in Arizona waters. Verhandlungen Internationale 

Vereinigung fur Theoretische und Angewandte Limnologie 19, 1675-1685. 

Dogiel, V.A. (1964). General Parasitology. English Translation. Oliver and Boyd, 

Edinburgh. 516 p. 

Dogiel, V.A. , Petrushevski, G.K.& Polyanski, Y.I. (1961). Parasitology of Fishes. 

English translation. Oliver and Boyd. Edinburgh. 384 p. 
 

 

16

Dove, A.D.M., Cribb, T.H., Mockler, S.P. & Lintermans, M. (1997). The Asian fish 

tapeworm, Bothriocephalus acheilognathi, in Australian freshwater fishes. Marine and 

Freshwater Research, 48, 181-183. 

Dove, A.D.M (1998). A silent tragedy: Parasites and the exotic fishes of Australia. 

Proceedings of the Royal Society of Queensland 107, 109-113. 

Esch, G.W & Fernandez, J. (1993). A functional biology of parasitism. Academic Press, 

New York. 

Font, W.F. & Tate, D.C. (1994). Helminth parasites of native Hawaiian freshwater fishes: 

An example of extreme ecological isolation. Journal of Parasitology, 80, 682-688. 

Fuller, P.L., Nico, L.G. & Williams, J.D. (1999). Nonindigenous fishes introduced into 

inland waters of the United States. American Fisheries Society, Special Publication 27, 

Bethesda, Maryland. 613 p. 

Granath, W.O. Jr. & Esch, G.W. (1983a). Seasonal dynamics of Bothriocephalus 

acheilognathi in ambient and thermally altered areas of a North Carolina cooling 

reservoir. Proceedings of the Helminthological Society of Washington, 50, 205-218. 

Granath, W.O. Jr. & Esch, G.W. (1983b). Temperature and other factors that regulate the 

composition and infrapopulation densities of Bothriocephalus acheilognathi (Cestoda) in 

Gambusia affinis (Pisces). Journal of Parasitology, 69, 1116-1124. 

Heckmann, R.A., Greger, P.D., & Furtek, R.C. (1993). The Asian fish tapeworm, 

Bothriocephalus acheilognathi, in fishes from Nevada. Journal of the Helminthological 

Society of Washington, 60, 127-128. 

Hoffman, G. (1999). Parasites of North American Freshwater Fishes. Ithaca: Cornell 

University Press. 

Hoffnagle, T. L. & Cole, R.A. (1999). Distribution and prevalence of Lernaea 

cyprinacea in fishes of the Colorado River and tributaries in Grand Canyon, Arizona. 

Proceedings of the Desert Fishes Council, 29, 45-46. 

Johnson, P. W. and R. B. Sanderson. 1968. Spring flow into the Colorado River, Lees 

Ferry to Lake Mead, Arizona. Arizona State Land Department, Water Resources Report

No. 34. 

Kennedy, C. & Bush, A.O. (1994). The relationship between pattern and scale in parasite 

communities: a stranger in a strange land. Parasitology 109, 187-196. 
 

 

17

Kennedy, C.R. (1991). Introductions, spread and colonization of new localities by fish 

helminth and crustacean parasites in the British Isles: a perspective and appraisal. Journal 

of Fish Biology 43, 287-301. 

Magurran, A.E. (1988). Ecological diversity and its measurement. Princeton University 

Press, New Yersey. 110 pp. 

Marcogliese, D. & Esch, G.W. (1989a). Experimental and natural infection of planktonic 

and benthic copepods by the Asian tapeworm, Bothriocephalus acheilognathi. 

Proceedings of the Helminthological Society of Washington, 56, 151-155. 

Marcogliese, D. & Esch, G.W. (1989b). Alteration in seasonal dynamics of 

Bothriocephalus acheilognathi in a North Carolina cooling reservoir over a seven year 

period. Journal of Parasitology, 75, 378-382. 

Margolis, L. & Arthur, J.R. (1979). Synopsis of the parasites of fishes of Canada. Bulletin 

of the Fisheries Research Board of Canada, 199. 269 p. 

Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M., & Schad, G.A. (1982). The use of 

ecological terms in parasitology. Journal of Parasitology 68, 131-133. 

Marsh, P.C. & Douglas, M.E. 1997. Predation by introduced fishes on endangered 

humpback chub and other native species in the Little Colorado River, Arizona. 

Transactions of the American Fisheries Society, 126, 343-346. 

McDonald, T. & Margolis, L. (1995). Synopsis of the parasites of fishes of Canada. 

Canadian Special Publication of Fisheries and Aquatic Sciences, 122. 265 pp. 

Milinski, M. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus 

aculeatus L.) under competition for food. Behaviour, 93, 203-216. 

Miller, R.R. and J.R. Alcorn. (1943). The introduced fishes of Nevada with a history of 

their introduction. Transactions of the American Fisheries Society 73, 173-193. 

Minckley, W. L. (1991). Native fishes of the Grand Canyon region: an obituary? In 

Colorado River Ecology and Dam Management (National Academy of Sciences, ed.) 

National Academy of Sciences Press, Washington, DC. Pages 124-177. 

Moravec, F. (1994). Parasitic nematodes of freshwater fishes of Europe. Kluwer 

Academic Publishers, Boston. 473 pp. 

National Academy of Sciences. (1991). Colorado River Ecology and Dam Management. 

National Academy of Sciences Press, Washington, DC. 

Nelson, J.S. (1994). Fishes of the World. 3rd Edition. John Wiley and Sons Inc., New 

York. 600 p. 
 

 

18

Oberlin, G.E., Shannon, J.P. & Blinn, D.W. (1999). Watershed influence on the 

macroinvertebrate fauna of ten major tributaries of the Colorado River through Grand 

Canyon, Arizona. The Southwestern Naturalist, 44, 17-30. 

Peet, R. (1974). The measurement of species diversity. Annual Review of Ecology and 

Systematics, 15, 285-307. 

Pérez-Ponce de León, G. & Choudhury, A. (2002). Adult endohelminth parasites of 

ictalurid fishes (Osteichthyes: Ictaluridae) in Mexico: Empirical evidence for 

biogeographical patterns. Journal of the Helminthological Society of Washington, 69, 10-

19. 

Pérez-Ponce de León, G., García –Prieto,L., Osorio-Sarabia,D. & León-Règagnon, V. 

(1996). Listados Faunísticos de México VI. Helmintos Parásitos de Peces de Aguas 

Continentales de México. Instituto de Biología, UNAM, México. 100 pp. 

Pritchard, M. H. and G. O.W. Kruse. 1982. The collection and preservation of animal 

parasites. University Nebraska Press, Lincoln. 141 pp. 

Roberts, L.S. (1970). Ergasilus (Copepoda: Cyclopoida): Revision and key to species in 

North America. Transaction of the American Microscopical Society, 89, 134-161. 

Robinson, A. T., Kubly, D.M., Clarkson, R.W. & Creef, E.D. (1996). Factors limiting 

the distributions of native fishes in the Little Colorado River, Grand Canyon, Arizona. 

The Southwestern Naturalist 41, 378-387. 

Scholz, T. (1997) A revision of the species of Bothriocephalus Rudolphi, 1808 (Cestoda: 

Pseudophyllidea) parasitic in American freshwater fishes. Systematic Parasitology 36, 

85-107. 

Scholz, T. (1999). Parasites in cultured and feral fish. Veterinary Parasitology 84, 317-

335. 

Sho, S. & Goater, C.P. (2001). Brain-encysting parasites affect visually-mediated 

behaviours of fathead minnows. Ecoscience. 8, 289-293. 

Sousa, W.P. (1994). Patterns and processes in communities of helminth parasites. Trends 

in Ecology and Evolution 9, 52-57. 

Stone, D. (1999). Ecology of humpback chub, Gila cypha, in the Little Colorado River, 

near Grand Canyon, Arizona. M.Sc. thesis. Northern Arizona University, Flagstaff, 

Arizona, U.S.A. 
 

 

19

U.S. Fish and Wildlife Service. (1980). Special report on distribution and abundance of 

fishes of the lower Colorado River. U.S. Fish and Wildlife Service, Albuquerque, NM. 

157 pp. 

 

U. S. Fish and Wildlife Service. (1994). Habitat use by humpback chub, Gila cypha, in 

the Little Colorado River and other tributaries of the Colorado River. Final report 

submitted to Glen Canyon Environmental Studies, U. S. Bureau of Reclamation, 

Flagstaff, Arizona. Arizona Fishery Resources Offices, U. S. Fish and Wildlife Service, 

Pinetop, Arizona. 

Valdez, R. A. & Hoffnagle, T.L. (1999). Movement, habitat use, and diet of adult 

humpback chub. In The controlled flood in Grand Canyon. American Geophysical 

Union Monograph 110 (R. H. Webb, Schmidt, J.C., Marzolf, G.R. & Valdez, R.A. eds.) 

American Geophysical Union, Washington, DC., U.S.A., pp 297-308. 

Valdez, R. A. & Ryel, R.J. (1997). Life history and ecology of the humpback chub in the 

Colorado River in Grand Canyon, Arizona. Proceedings of the Biennial Conference of 

Research on the Colorado Plateau 3, 3-31. 

Valdez, R. A., Persons, W.R. & Hoffnagle, T.L. (in press). A non-native fish control 

strategy for Grand Canyon, Arizona. In Proceedings of a Symposium and Workshop on 

Restoring Native Fish to the Lower Colorado River: Interactions of Native and Nonnative Fishes. 13-14 July 1999, Las Vegas, Nevada. Region II, U.S. Fish and Wildlife 

Service, Albuquerque, New Mexico. 

Van Cleave, H.J. & Mueller, J.F. (1932). Parasites of Oneida Lake fishes, Part I. 

Descriptions of new genera and new species. Roosevelt Wildlife Annals, 3(1): 1-72. 

Yeh, L.S. (1955). On a new tapeworm Bothriocephalus gowkongensis n. sp. (Cestoda: 

Bothriocephalidae) from freshwater fish in China. Acta Zoologica Sinica, 7: 69-72. 

Zar, J. H. (1996). Biostatistical Analysis. Prentice Hall, Inc., Uuper Saddle River, NJ.
Table I. Lengths, weights, and total number of fish examined in a study of the Lower Little Colorado River  Length1(mm) Weight 1 (g) N 

Fish Species 

Native Catostomus discobolus 84.48 ± 48.83 10.67 ± 23.32 148 

 (35 – 288) (30 – 147) 

C. latipinnis 103.64 ± 86.46 50.89 ± 173.17 73 

(36 – 492) (0.5 – 962)

Gila cypha 93.55 ± 36.43 7.76 ±10.27 116  (34 – 232) (0.2 – 78.3) 

Rhinichthys osculus 69.1 ± 12.12 2.97 ± 4.47 630 

(29 – 115) (0.2 – 85)

Non-native Ictalurus punctatus 381.57 ± 212.71 1147.68 ± 469.3 54 

(48 - 770) (0.8 – 8030)

Cyprinus carpio 119.16 ± 133.83 139.64 ± 463.57 63 

(32 – 600) (0.5 – 2617.5) 

Pimephales promelas 61.97 ± 12.12 2.42 ± 1.61 193 

 (31 – 99) (0.3 - 10.3)Fundulus zebrinus 55.48 ± 9.4 1.67 ± 0.9 113 

(28 – 81) (0.4 – 5.5)

Oncorhynchus mykiss 326.14 ± 44.34 298.69 ± 133.14 22 

(252 – 441) (122 – 441)

Cyprinella lutrensis 60.18 ± 10.31 1.97 ± 0.89 11 

(50 – 88) (1 – 3.9)

Ameiurus natalis 165.42 ± 63.15 76.77 ± 63.84 12 

(80 – 252) (5.7 – 185)

1 Mean ± Standard deviation (minimum - maximum). N = sample size 
Table II. Number of fish of each species necropsied on each trip and in each sampled reach during this study. 

 Native Fishes* Non-native Fishes* 

Trip/Reach BHS FMS HBC SPD CCF CRP FHM PKF RBT RS Summer 1999 (28 May – 9 June)  LCR Reach 3 0 0 0 20 1 0 4 0 0  Big Canyon Springs 0000 00000 Salt Creek 0 0 0 0 0 0 0 0 0  LCR Reach 2 10 13 10 33 4 1 3 0 1  LCR Reach 1 20 12 9 33 5 1 10 1 0  Summer 1999 Total 30 25 19 86 10 2 17 1 1  Fall 1999 (Sept 4 - 13)

 Big Canyon Creek 5 0 1 35 0 0 11 0 0  Big Canyon Springs 0000 00000 Salt Creek 0 0 1 64 0 0 2 0 0  LCR Reach 2 2 0 7 0 8 2 1 0 0  LCR Reach 1 1 0 10 0 3 1 0 0 0  Fall 1999 Total 8 0 19 99 11 3 14 0 0 
Table II continued  Native Fishes* Non-native Fishes* Trip/Reach BHS FMS HBC SPD CCF CRP FHM PKF RBT RSSpring 2000 (9-21 April) Big Canyon Creek 0 0 1 31 0 0 0 0 0  Big Canyon Springs 0000 00000 Salt Creek 0 0 3 19 0 0 0 0 0  LCR Reach 2 26 2 6 31 6 0 5 4 3  LCR Reach 1 6 3 10 16 6 1 14 1 7  Spring 2000 Total 32 5 20 97 12 1 19 5 10 Summer 2000 (4 - 15 June)

 Big Canyon Creek 0 0 0 22 0 0 0 0 0  Big Canyon Springs 0 0 0 31 0 0 0 6 0  Salt Creek 0 0 0 22 0 0 0 0 0  LCR Reach 2 26 0 10 17 3 27 9 4 0  LCR Reach 1 24 23 10 21 4 22 0 1 7  Summer 2000 Total 50 23 20 113 7 49 9 11 7 
Table II continued.  Native Fishes* Non-native Fishes* Trip/Reach BHS FMS HBC SPD CCF CRP FHM PKF RBT RSFall 2000 (25 September - 4 October) Big Canyon Creek 0 0 0 25 0 0 0 0 0  Big Canyon Springs 0 0 0 20 0 0 0 21 0  Salt Creek 0 0 0 30 0 0 0 0 0  LCR Reach 2 6 4 10 26 3 0 47 19 3  LCR Reach 1 1 7 10 10 10 3 34 16 0  Fall 2000 Total 7 11 20 111 13 3 81 56 3 April 2001 (1 – 12 April)

 Big Canyon Creek 0 0 0 30 0 0 2 0 1 

 Big Canyon Springs 10 2 0 30 0 0 2 30 0  Salt Creek 0 0 0 25 0 0 2 7 0  LCR Reach 2 9 1 9 18 1 1 22 2 0  LCR Reach 1 2 6 9 21 0 4 25 1 0  April 2001 Total 21 9 18 124 1 5 53 40 1 Total 148 73 116 630 54 63 193 113 22 

*BHS = bluehead sucker, FMS = flannelmouth sucker, HBC = humpback chub, SPD = speckled dace, CCF = chcommon carp, FHM = fathead minnow, PKF = plains killifish, RBT = rainbow trout, RSH = red shiner, YBH = y
Table III. Parasites of native fishes in the Little Colorado River1. 

_____________________________________________________________________________________________________________ BHS+ FMS HBC SPD 

 (n = 148) (n = 73) (n = 116) (n = 630) _____________________________________________________________________________________________________________Parasite species Monogenea

Gyrodactylus sp. - - - 0.04 ± 0.44 

 (0 – 7) (0.01) Cestoda

B. acheilognathi 0.05 ± 0.58 0.07 ± 0.48 18.36 ± 34.55 1.97± 6.06 

 (0 – 7) (0.01) (0 – 4) (0.03) (0 – 243) (0.84) (0 – 64) (0.43) 

 Corallobothriinae* (pl.) 0.009 ± 0.09 - 

 (0 –1) (0.01) Trematoda

Ornithidiplostomum sp.* (viscera) 0.07 ± 0.59 0.01± 0.12 7.69 ± 20.67 1.53 ± 3.36 

 (0 – 7) (0.03) (0 – 1) (0.01) (0 – 202) (0.67) (0 – 32) (0.4) 

Ornithodiplostomum sp.* (brain) 0.15 ± 0.46 0.03 ± 0.19 

 (0 – 3) (0.11) (0 – 2) (0.03) 

Ornithodiplostomum sp.* (eye) 0.02 ± 0.13 0.001 ± 0.04 

 (0 – 1) (0.01) (0 – 1) (0.001) 

Posthodiplostomum sp. * - - 0.01 ± 0.09 - 

 (0 – 1) (0.01) 

Unidentified metacercaria 0.006 ± 0.82 - 0.009 ± 0.09 0.003 ± 0.06 

 (0 – 1) (0.006) (0 – 1) (0.01) (0 – 1) (0.003) Nematoda

Rhabdochona sp. - - 0.11± 0.39 0.37 ± 1.66 

 (0 –2) (0.09) (0 – 23) (0.12) 

Eustrongylides sp.* - - - 0.001 ± 0.04 

 (0 – 1) ((0.001) 

Contracaecum sp.* - - - 0.003 ± 0.06 

 (0 – 1) (0.003) 
Acari

 Oribatida gen. sp. - - - 0.02 ± 0.18 

 (0 –3) (0.02) Crustacea

Lernaea cyprinacea (adult female) - - 0.07± 0.25 0.01 ± 0.11 

 (0 – 1) (0.01) (0 – 2) (0.01) 

L. cyprinacea (copepodites) - - 0.03 ± 0.37 0.008 ± 0.10 

 (0 – 2) (0.01) (0 – 2) (0.01) _____________________________________________________________________________________________________________

1Mean abundance ± standard deviation (minimum – maximum) (prevalence) 

 Larval stages: pl = plerocercoid. 

 +BHS = bluehead sucker, FMS = flannelmouth sucker, HBC = humpback chub, SPD = speckled dace. 
Table IV. Parasites of non-native fishes of the Little Colorado River1. 

_____________________________________________________________________________________________________________ CCF CRP FHM PKF RBT RSH  (N = 54) (N = 63) (N = 193) (N = 113) (N = 22) (N = 11) _____________________________________________________________________________________________________________Parasites Myxozoa

Henneguya exilis P (0.02) - - - - - Monogenea

Ligictaluridus floridanus 1.13 ± 7.62 - - - - -  (0 – 56) (0.07) Dactylogyrus extensus - 0.27± 0.83 - - - - 

 (0 – 4) (0.13) Gyrodactylus hoffmani - - 0.24 ± 1.32 - - - 

 (0 – 15) (0.09) Cestoda

Bothriocephalus acheilognathi 0.04 ± 0.19 3.5 ± 5.4 0.84 ± 5.28 1.26 ± 4.54 0.04 ± 0.21 1.2 ± 1.3

 (0 – 1) (0.05) (0 – 28)(0.52) (0 – 72) (0.23) (0 – 26) (0.15) (0 – 3) (0.14) (0 – 3) (0Corallobothrium fimbriatum 1.97 ± 7.67 -  (0- 56) (0.35) Megathylacoides giganteum 1.59 ± 2.51 - - - - - 

 (0 – 10) (0.4) Corallobothriinae* (pl.) 0.18 ± 1.12 - - - - -  (0 – 8) (0.02) Trematoda

Ornithodiplostomum sp.* (v) 0.02 ± 0.14 - 0.24 ± 1.56 - - - 

 (0 – 1) (0.02) (0 – 17) (0.06) Ornithodiplostomum sp.* (b) - - 0.01± 0.11 - - -  (0 – 1) (0.01) Posthodiplostomum sp.* - - 0.02 ± 0.36 - - - 

 (0 – 5) (0.005) 
Nematoda

Rhabdochona sp. - - - 0.01± 0.09 - - 

 (0 – 1) (0.01) Truttaedacnitis truttae - - - - 24.8 ± 25.57 - 

 (0 – 108) (1)

Eustrongylides sp.* (l) 0.24 ± 0.58 - - - - - 

 (0 – 3) (0.18) Contracaecum sp.* (l) 0.18± 0.55 - - - - 0.09 ± 0.3

 (0 – 3) (0.13) (0 – 1) (0Acari

Oribatida gen. sp. - - - 0.18 ± 0.13 - - 

 (0 – 1) (0.02) Crustacea

Ergasilus arthrosis. 0.02 ± 0.14 - - - - -  (0 – 1) (0.02) Lernaea cyprinacea (female) - - - 0.01 ± 0.09 - - 

 (0 –1)(0.01) Lernaea cyprinacea (copepodite) - - 0.005 ± 0.07 0.12 ± 0.5 0.04 ± 0.21 

 (0 – 1) (0.005) (0 – 3) (0.07) (0 – 1) (0.04) Hirudinea 

Myzobdella lugubris 0.02 ± 0.14 - - - - - 

 (0 –1) (0.02) 

1 Mean abundance ± standard deviation (minimum – maximum) (prevalence), 

P = Present (prevalence) * = Larval stages: (l) = larva, pl = plerocercoid, v = visceral, b = brain.
Table V. Parasite component community diversity1 in humpback chub, speckled dace, and channel catfish. 

_____________________________________________________________________________________________________________

G. cypha R. osculus I. punctatus

June 1999 0.22 (0.47) (N=19) 0.27 (0.57) (N=86) 0.36 (0.59) (N=10) September 1999 0.28 (0.47) (N=18) 0.42 (0.89) (N=99) 0. 50 (0.65) (N=11) April 2000 0.25 (0.53) (N=20) 0.37 (0.48) (N=97) 0.58 (0.69) (N=12) June 2000 0.26 (0.55) (N=20) 0.51 (0.72) (N=113) 0.50 (0.6) (N=7) September 2000 0.31 (0.44) (N=20) 0.49 (0. 63) (N=111) 0.35 (0.48) (N=13) April 2001 0.29 (0.47) (N=20) 0.38 (0.55) (N=124) 

1Shannon-Wiener index (Shannon’s H’) followed by evenness (in parentheses), and the sample size (N) of hosts in parentheses. 
Table VI. Parasite component community diversity1 in humpback chub and speckled dace at different sampling sites. 

_____________________________________________________________________________________________________________

G. cypha R. osculus

_____________________________________________________________________________________________________________

Sampling Site2

LC1 0.27 (0.44) (N=58) 0.46 (0.59) (N=101) LC2 0.29 (0.38) (N=52) 0.55 (0.81) (N=125) BCC - 0.35 (0.51) (N=143) BCS - 0.50 (0.65) (N=81) SAC - 0.43 (0.56) (N=160) _____________________________________________________________________________________________________________

1Shannon-Wiener index (Shannon’s H’) followed by evenness (in parentheses), and the sample size (N) of hosts in parentheses 2See text for sampling sites 

31

Figure Legends 

Figure 1. The Colorado River drainage and location of fish sampling sites in the Little 

Colorado River, Grand Canyon, Arizona. LC1 = RK 0 – 2.5; LC2 = RK 10.6-11.5; LC3 

= RK 14.5-15.1; BCC = Big Canyon Creek; BCS = Big Canyon Springs; SAC= Salt 

Creek. 

Figure 2. Contribution of the different sampling sites (%) to the total fish sample during 

the Lower Little Colorado River (LCR) Study. See Figure 1 and text for acronyms of 

sampling sites. 

Figure 3. Number of species of fish recovered from the different sampling sites during 

the LCR study. See Figure 1 and text for acronyms of sampling sites. 

Figure 4. Mean parasite species richness of the different species of fishes examined in 

LCR study. BHS: Bluehead sucker, FMS: Flannelmouth sucker, HBC: Humpback chub, 

SPD: Speckled dace, CCF: Channel catfish, CRP: Carp, FHM: Fathead minnow, PKF: 

Plains killifish, RBT: Rainbow trout, YBH: Yellow bullhead. 

Figure 5. Mean parasite species richness in 5 of the more abundant fish species in the 

LCR at different sampling periods. Acronyms of fish species as in Figure 4. 

Figure 6. Abundance of B. acheilognathi in 11 species of fishes in the LCR at different 

sampling periods. Acronyms of fish species as in Figure 4. 

Figure 7. Abundance of B. acheliognathi in humpback chub in LC1 and LC2 at different 

sampling periods. Acronyms of sampling sites and fish species as in Figures 1 and 4. 

Figure 8. Abundance of B. acheilognathi in speckled dace in different sampling sites at 

different periods. Big Canyon Creek and Salt Creek at different sampling times. 

Figure 9. Abundance of B. acheilognathi in speckled dace in Big Canyon Creek (BCC) 

and Salt Creek (SAC) at different sampling times. 

Figure 10. Abundance of Ornithodiplostomum sp. in humpback chub and speckled dace 

from different sampling sites. See text for acronyms. 

Figure 11. Abundance values of visceral Ornithodiplostomum sp., in speckled dace from 

Big Canyon Creek (BCC) and Salt Creek (SAC) at different sampling periods. 

Corresponding abundance values of B. acheilognathi are provided for comparison. 

Figure 12. Temperature profiles of Big Canyon Creek (BCC) and Salt Creek (SAC), 27 

September 2000 - 6 June 2001. 

Figure 13. Mean daily temperature of the Little Colorado River at RK 1.2. Blank section 

is due to instrument failure after a flood. Shaded bars are sampling trips.