Ontogenesis of Endangered Humpback Chub (Gila cypha)

in the Little Colorado River, Arizona

DENNIS M. STONE1 AND OWEN T. GORMAN2

U.S. Fish and Wildlife Service, P.O. Box 338, Flagstaff, Arizona 86002

ABSTRACT.—The largest population of endangered humpback chub Gila cypha inhabits the

Colorado River below Glen Canyon Dam and the lower 14 km of the Little Colorado River

(LCR), Arizona. Currently, adults from both rivers spawn and their progenies grow and

recruit to adulthood primarily within the LCR, where we studied G. cypha’s life history using

hoop net capture data. Humpback chub undergo an ontogenesis from diurnally active,

vulnerable, nearshore-reliant young-of-the-year (YOY; 30–90 mm total length) into

nocturnally active, large-bodied adults (180 mm TL). During the day, adults primarily

resided in deep midchannel pools; however, at night they dispersed inshore amongst the

higher densities of YOY conspecifics. Many YOY G. cypha shifted to nocturnal habitats that

provided greater cover, possibly, to avoid inshore invading adults. These findings mirror

predator-prey scenarios described in other freshwater assemblages, but do not refute other

plausible hypotheses. Gila cypha piscivorous activity may escalate in hoop nets, which can

confine fish of disparate sizes together; adults were significantly associated with YOY

conspecifics and small dead fish in hoop nets at night and eight G. cypha (156–372 mm TL)

regurgitated and/or defecated other fish body parts during handling following capture.

Gila cypha can definitely be piscivorous given the opportunity, but the magnitude of

their piscivorous activity in the wild is debatable.

INTRODUCTION

The largest of six remnant populations of federally endangered humpback chub Gila

cypha resides in the Colorado River below Glen Canyon Dam within Grand Canyon National

Park and the lower 14 km of the Little Colorado River (LCR) on Navajo tribal lands, Arizona

(USFWS, 1990; Douglas and Marsh, 1996). Historically, G. cypha spawned, matured and

recruited throughout both rivers, but these activities have been largely curtailed in the

mainstem Colorado River since its transformation into a regulated tailwater. Cold

hypolimnetic water releases from Lake Powell have reduced the water temperature of the

Colorado River to 8–10 C, inhibiting spawning and embryonic development of G. cypha

(Hamman, 1982; Clarkson and Childs, 2000). Currently, the ichthyofauna of the Colorado

River is dominated by introduced fishes that thrive in these modified river conditions and

have become substantial competitors and predators of G. cypha, especially small young-ofthe-year (YOY) that commonly migrate into the mainstem from the LCR (Minckley, 1991;

Gorman et al., 2005). As a result, the perpetuation of the entire humpback chub population

currently depends on the lower LCR for spawning and juvenile rearing habitat and,

ultimately, for recruitment to adulthood (Gorman and Stone, 1999).

The LCR flows intermittently throughout most of its 573 km corridor and is subject to

episodic floods after spring thaws and summer rains throughout the 69,870 km2 river basin

(Johnson, 1975). Perennial springs located within the lower 21 km of the LCR maintain

a mean base flow of 6.3 m3

/s (Cooley, 1976); however, Gila cypha only naturally inhabit the

1 Corresponding author: Telephone: (928) 226-1289; e-mail: Dennis_Stone@fws.gov

2 Present address: U.S. Geological Survey, Great Lakes Science Center, 2800 E. Lake Shore Drive,

Ashland, Wisconsin 54806-2427; e-mail: Owen_Gorman@usgs.gov

123

Am. Midl. Nat. 155:123–135
terminal 14 km below the Chute Falls travertine dam (Kaeding and Zimmerman, 1983).

The lower LCR fish community is numerically dominated by native species, generally, G.

cypha are most common, followed by speckled dace Rhinichthys osculus, bluehead sucker

Catostomus discobolus and flannelmouth sucker C. latipinnis (Kaeding and Zimmerman, 1983;

Gorman and Stone, 1999). The adult G. cypha population in the LCR peaks in the springsummer months when the resident population is augmented with spawning migrants

from the Colorado River (Douglas and Marsh, 1996; Gorman and Stone, 1999). The LCR

contains a relatively depauperate invertebrate and plant food base, which likely limits its

fish carrying capacity (Kaeding and Zimmerman, 1983; Oberlin et al., 1999; Benenati et al.,

2002). To gain a better understanding of the life history of humpback chub, which is

crucial to correctly identify which actions will best promote their recovery (USFWS, 1990),

we examined the diel locomotor activity, habitat use and association patterns among

different G. cypha life stages in the LCR.

METHODS

We studied humpback chub at two separate 1 km reaches within the lower LCR from

1991–1995. Powell reach was located from 2.4 to 3.4 km upstream of the confluence with the

Colorado River and Salt reach from 10.4 to 11.4 km upstream of the confluence (Fig. 1a).

These combined reaches constituted .14% of the LCR corridor occupied by Gila cypha.

Compared to the Powell reach, the Salt reach contained an overall broader array of habitat

types, such as perennial springs, larger travertine dams, deeper pools and more boulders.

To determine life history strategies under ecologically similar abiotic and biotic

conditions, we focused our analyses on 12 data sets collected during six 1992–1994 summer

sampling trips at both study reaches (Table 1). All 12 data sets were collected when the LCR

discharge was at baseflow and adult G. cypha were not spawning (Gorman and Stone, 1999).

Examination of water chemistry data, which was collected daily at both study reaches (Model

2100P Turbidimeter and Surveyor 3 Hydrolab, Hach Co., Loveland, CO), indicated that

turbidity (mean 6 SE 1⁄4 6.1 6 0.5 nephelometric turbidity units), water temperature (21.4 6

0.2 C), dissolved oxygen (6.5 6 0.1 mg/liter O2), pH (7.7 6 0.4 pH) and specific

conductance (4820 6 17.2 lS/cm) were relatively constant across data sets.

Sampling design.—Fifty cross-channel transects were permanently established at 20-m

intervals throughout both 1 km study reaches. At each transect, unbaited hoop nets (50 cm

diameter 3 100 cm length, 10 cm throat, 6 mm nylon mesh) were deployed at 3–4 m

intervals across the river by attaching them to ropes anchored to opposing stream banks.

Half the transects were set with nets in the morning and half in the evening, whereby all nets

were examined twice at fixed locations (within 2 h after sunrise and 2 h before nightfall)

over a 24-h period and then relocated to the next upstream transect. This resulted in

identical habitats being sampled for both diurnal and nocturnal periods. We only fished

half of each study reach during a sampling trip and alternated the halves being sampled between sampling trips.

We usually measured (mm) all Gila cypha captured for total length (TL); however, to

reduce handling stress at the Salt reach we only measured 731 (mean 6 SD 1⁄4 57 6 5.3 mm

TL) of 1425 YOY captured in July 1993 and 1419 (63 6 7.5 mm TL) of 3444 YOY captured in

August 1993. We measured all YOY G. cypha captured during both sampling periods across

several full transects of nets to provide an unbiased representative sample for activity pattern

comparisons, but mostly measured subsets from each net. Only G. cypha 30 mm TL were

used for analyses because smaller ones could pass through the nets’ 6 mm mesh.

We conducted habitat measurements concurrently with fish sampling. We measured

distance (cm) from the center of each net to the nearest shoreline. Depth and current

124 THE AMERICAN MIDLAND NATURALIST 155(1)
velocity were quantified at 20 points, each spaced 50 cm from adjacent ones within a 1.5 3

2.0 m grid around each net, with a 25 mm diameter pole (Gorman and Stone, 1999). Point

measurements for depths (cm) were analyzed as both mean depth and standard deviation of

depth (hereafter, bottom profile ‘‘a 3-dimensional measure of structure heterogeneity’’,

sensu Gore, 1978) for each net. Surface current at each point was identified to one of six

categories that were defined by patterns of flow around the measuring pole and calibrated

with a flow meter (Marsh-McBirney, Inc. Model 201, Frederick, Maryland) to calculate mean

current velocity (m/s) for each net set (Gorman and Karr, 1978; Gorman and Stone, 1999).

Points showing upstream flow were recorded as eddy currents, which were tabulated and

analyzed as the frequency of eddies per net. The largest substrate existing within each net

grid was identified to one of nine categories (ranging from silt 0.1 mm to large boulders

.3 m) for each net. These six habitat variables were individually calculated for all 1310 day/

night net deployment sites. Habitat associations of 8871 Gila cypha were made by linking

each individual fish to the corresponding net from which it was captured.

Diel locomotor activity.—The fact that fishes must be locomotory active to be captured by

passive gears has been used to discern diel locomotor activity of fishes by comparing day vs.

night catch rates (Mendelson, 1975; Magnan and FitzGerald, 1984; Tonn and Paszkowski,

FIG. 1.—Map and photographs depicting humpback chub research in the Little Colorado River

(LCR), Arizona (1991–1995). (a) Gila cypha naturally inhabit the lower 14 km of the LCR below the

Chute Falls; this paper focuses on data collected concurrently at the Powell reach (2.4–3.4 km above

mouth) and Salt reach (10.4–11.4 km) during six 1992–1994 summer sampling trips (12 data sets). (b)

Young-of-the-year G. cypha schooling along a shoreline at the Salt reach in June 1993. (c) Underwater

photo of adult G. cypha residing in a deep (.2 m) midchannel pool at Powell reach in June 1993.

(d) A postspawned adult male G. cypha at the Salt reach in May 1995

2006 STONE & GORMAN: HUMPBACK CHUB 125
1987; Reebs et al., 1995). We assorted humpback chub into 10 size classes beginning with

30–50 mm TL Gila cypha and following in 20 mm TL increments until the final class,

which contained all G. cypha .210 mm TL. As previously described, we only included

a representative sample of YOY G. cypha (30–90 mm TL) captured at the Salt reach in July

1993 (295 of 1425 captured) and August 1993 (126 of 3444); this avoided biases related to

comparing catch rates from nets set in disparate habitats and prevented overshadowing YOY

diel patterns with two atypical data sets. All other G. cypha captured during the study were

included in the analyses (Table 1). We then enumerated and calculated percentages of the

day and night G. cypha captures for each size class.

Diel habitat use and intraspecific association patterns.—Gila cypha were separated into YOY

(30–90 mm TL), juveniles (91–179 mm TL) and adults (180–410 mm TL) size classes for

analyses (Figs. 1b–d). These separations were based on mean YOY growth in the first year

and the lower lengths that some individuals, primarily males, expressed gametes upon

manual stripping during the spring spawning season. We used nonparametric procedures to

examine habitat use patterns because violations to the assumptions for parametric tests were

both common and disparate among habitat variables within each data set. We compared

mean ranks derived from monotonic data transformations within each data set,

independent of the other data sets (Conover and Iman, 1981). Basically, mean ranks

reflected habitat use information for each fish group relative to the other fish groups

despite disparate sample sizes (Siegel and Castellan, 1988). We omitted the June 1993

Powell reach data set from all habitat use analyses involving YOY because none were

captured at night.

Kendall’s Coefficient of Concordance was used to separately compare the day and night

mean ranks of differential habitat use among YOY, juvenile and adult Gila cypha for each

habitat parameter across 11 data sets. Kendall’s ‘‘W’’ coefficients can range from zero (none)

to one (complete) and directly relates to the patterns of the mean ranks (Kendall, 1962).

For example, G. cypha from size classes repeatedly captured closest to shore, at the shallowest

depths and in the slowest currents across data sets would be lower ranked for those variables

TABLE 1.—Summary of humpback chub captured in hoop nets during six sampling trips at Powell

and Salt study reaches (12 data sets) in the Little Colorado River, Arizona. Given for each data set are

the sampling trip dates, study reach, number of hoop nets deployed and resulting captures of YOY

(30–90 mm TL), juvenile (91–179 mm TL) and adult (180–410 mm TL) Gila cypha during the day

and night sampling periods

Sampling trip Reach Nets

YOY Juveniles Adults

Day night day night day night

15–23 Jun. 1992 Powell 90 28 13 57 50 6 18

Salt 82 27 19 100 141 11 40

8–14 Jun. 1993 Powell 104 2 0 15 38 5 11

Salt 118 33 25 5 40 4 34

12–19 Jul. 1993 Powell 133 375 248 8 17 2 9

Salt 97 871 554 4 20 6 57

9–16 Aug. 1993 Powell 146 192 182 11 15 7 3

Salt 110 1512 1932 4 21 4 48

6–13 Jun. 1994 Powell 99 122 86 72 74 4 5

Salt 104 55 121 54 211 3 61

9–16 Aug. 1994 Powell 114 333 245 31 29 2 2

Salt 113 195 172 80 119 10 21

Total 1310 3745 3597 441 775 64 309

126 THE AMERICAN MIDLAND NATURALIST 155(1)
than those from other groups, and vice versa. Thus, resulting habitat use patterns statistically

represent the relative position of each group of fishes with respect to each other across all

data sets.

Wilcoxon Signed Rank tests were used to unravel disparate day versus night Kendall’s

mean rank patterns that resulted from diel shifts in habitat use by one or more groups of

Gila cypha. Comparisons were conducted between day and night monotonic mean ranks of

each habitat variable for each group of G. cypha across data sets. Resulting diel shifts by YOY,

juvenile or adult G. cypha with respect to each habitat variable would only reflect two-tailed

significance if it was directionally repeated across a preponderance of data sets. Inspection

between day and night mean ranks provided the direction of significant shifts in habitat use.

We conducted Spearman correlation tests on sampled habitat data to examine for

significant relationships between habitat variables. All statistical tests were conducted using

SPSS for Windows, Release 9, 1998 (SPSS Inc., Chicago, IL) and those resulting in P-values

,0.10 were considered significant.

Adult humpback chub were separately paired with YOY and juvenile conspecifics to

examine for intraspecific associations during the day and night periods. We pooled data

across all data sets to increase fish sample sizes and resulting power of the association tests

(Zar, 1996). This was justifiable given that all data were collected under ecologically similar

summer conditions (Mantel et al., 1997). We calculated separate chi-square statistics with

Yates correction for continuity for each fish pair during each sampling period from

presence/absence data enumerated into 2 3 2 contingency tables (Cole, 1949; Ludwig and

Reynolds, 1988). For example, the table cells for the nighttime adult-YOY paired association

contained the number of nets that captured (a) adults and YOY, (b) only adults, (c) only

YOY and (d) no fish. All 1310 net sets were included in each paired association and

differences between the observed and expected number of co-occupied nets distinguished

positive from negative associations. Probability values (a 1⁄4 0.1) were obtained from Rohlf

and Sokal (1981) with 1 df. We also calculated the Dice index for each paired association

following the recommendations by Janson and Vegelius (1981) and Huba ́lek (1982). This

index ranges from zero (no association) to one (maximum association).

Indications of humpback chub piscivorous activity.—We provided accounts of Gila cypha that

regurgitated other fishes and/or defecated fish body parts while we were handling them. We

also occasionally found small dead fish in the nets and speculated that larger G. cypha may

have killed many of these fish. Therefore, we conducted chi-square tests (described above)

to examine whether small dead fishes (30–90 mm TL) were significantly associated to either

adult or juvenile G. cypha. All 1310 nets sets were included for each paired association of

each sampling period.

We examined catch rates between sequential sampling trips for patterns potentially

indicative of piscivorous activity. Summer data were not used because only one sampling trip

occurred in 1992, monthly catch rates of YOY Gila cypha increased from June through

August in 1993 as new cohort fish emerged and grew to catchable sizes, and the two

sampling trips in 1994 were separated by over a month (Table 1). Therefore, we compared

catch rates between sequential April and May sampling trips from 1994 and 1995. All spring

sampling trips occurred when LCR discharge was slightly above base flow but stable, large

numbers of adult G. cypha were in the system to spawn, and before new cohort fishes were

being captured. For each sampling trip, mean catch rates were calculated separately for

YOY (11–12 mo old), juvenile and adult G. cypha and speckled dace (30–90 mm) from

hourly catch rates of individual net sets; dace were included for insight of another small fish.

Mean catch rates within two standard errors (62 SE) that did not overlap were considered significantly different.

2006 STONE & GORMAN: HUMPBACK CHUB 127
RESULTS

A total of 13,718 fishes 30 mm TL were captured in 2620 net sets during the summers

1992–1994. Native fishes (99.2% of total catch) included 8871 humpback chub (64.7%),

3761 speckled dace (27.4%), 763 bluehead sucker (5.6%) and 225 flannelmouth sucker

(1.6%). Nonindigenous fishes (0.7%) included 87 fathead minnow Pimephales promelas

(0.6%), 6 channel catfish Ictalurus punctatus (0.04%), 4 common carp Cyprinus carpio

(0.03%) and 1 black bullhead Ameiurus melas (0.01%). The mean 6 SD of humpback chub

TL was 59 6 11.6 mm for 4240 measured YOY (30–90 mm; 7342 were captured), 117 6 23.8

mm for 1216 juveniles (91–179 mm) and 239 6 56.1 mm for 373 adults (180–410 mm).

Humpback chub captures and efforts for each data set are given in Table 1.

Diel locomotor activity.—Humpback chub catch rates progressively decreased during the day

and increased at night with incrementally larger size class fish (Fig. 2). Overall, the catch

rate pattern indicates that Gila cypha undergo an ontogenetic transition from diurnal to

nocturnal locomotor activity. Hereafter, humpback chub classified as YOY should be

considered generally diurnal (53–60% were captured during the day), juveniles mostly

nocturnal (59–82% captured at night) and adults essentially nocturnal (81–84% captured at

night). These diel activity designations agree with day versus night catch rates in 10 of 12

data sets for each size class (Table 1).

Diel habitat use and intraspecific association patterns.—Kendall’s comparisons revealed that

during the day, YOY, juvenile and adult humpback chub were sequentially captured further

from shorelines, at greater depths, in faster current velocities and in fewer eddies (Table 2,

Figs. 1b, c). At night, however, most adults resided between YOY and juveniles with respect to

distance from shore, current velocity and bottom profile.

Wilcoxon signed rank tests reflected a reoccurring inshore shift by adults for the night

that would explain much of the disparity between day and night habitat use patterns. For the

night, adults repeatedly shifted closer to shorelines across all 12 data sets (Z 1⁄4 3.059,

FIG. 2.—Proportions of day (clear bars) versus night (shaded bars) catch rates of humpback chub

from ten different size classes during summers 1992–1994 in the Little Colorado River, Arizona

128 THE AMERICAN MIDLAND NATURALIST 155(1)
P1⁄40.002), into slower current velocities in 10 of 12 data sets (Z1⁄42.275, P1⁄40.023) and more

eddies in 8 of 10 data sets (2 other data sets had tied mean ranks, Z1⁄42.497, P1⁄40.013). Shifts

by the adult population to shallower depths for the night were not significant (8 of 12 data

sets, Z 1⁄4 0.549, P 1⁄4 0.583); however, adult individuals were significantly captured more in

shallower depths at night in 11 of 12 data sets (Z1⁄42.903, P1⁄40.004). Distance to shore at the

1310 net deployment sites was positively correlated to mean current velocity (rs 1⁄4 0.376,

P 0.001) and mean depth (rs 1⁄4 0.206, P 0.001), but negatively correlated to frequencies of eddies (rs 1⁄4 0.106, P 0.001). Thus, all significant habitat shifts by adults

for the night were directed inshore.

Although YOY humpback chub remained in nearshore areas for the night (Table 2),

many individuals shifted to habitats containing larger substrates (10 of 11 data sets; Z 1⁄4

2.045, P 1⁄4 0.041) and, as with adults, to more eddies (9 of 11 data sets; Z 1⁄4 1.778, P 1⁄40.075).

For example, the proportions of YOY captured in nets deployed alongside large boulders

(.3 m; only 3.8% of all net sets) increased from 8.7% during the day to 14% at night, and

those caught in nets set entirely within eddies (only 0.7% of all net sets) increased from

3.6% during the day to 10.1% at night. Many juvenile Gila cypha shifted to more

homogenous bottom habitats at night (9 of 12 data sets; Z1⁄42.134, P 1⁄40.033), leaving adults

and YOY to occupy the more heterogeneous bottoms (Table 2).

Adult humpback chub were not significantly associated with YOY conspecifics during the

day (v21⁄40.179, P . 0.5), but were at night (v21⁄4 11.569, P , 0.001), and the Dice index was

three fold lower during the day (0.08) than at night (0.25). The proportion of YOY Gila

cypha captured in nets with adult conspecifics increased from 3% during the daytime to

28% at night. Although juvenile G. cypha were significantly associated with adults during

both sampling periods, the chi-square statistic and Dice index were much lower during the

day (v2 1⁄4 33.456, P , 0.001; Dice index 1⁄4 0.18) than at night (v2 1⁄4 111.186, P , 0.001; Dice

index 1⁄4 0.40), indicating a greater nocturnal association. The proportion of juveniles

captured in nets with adults increased from 17% during the daytime to 39% at night. The

proportions of adults captured in daytime net sets with YOY (45%) and juveniles (48%) were

only slightly lower than in nighttime net sets (51% with YOY; 62% with juveniles).

TABLE 2.—Kendall’s Coefficient of Concordance results of relative habitat use patterns among YOY

(30–90 mm), juvenile (91–179 mm) and adult (180–410 mm) humpback chub across 11 data sets

collected in the Little Colorado River, AZ (Table 1). The chi-square (v2

) statistic, P-value (2 df; P , 0.100

significant), Kendall’s ‘‘W’’ coefficient and mean ranks (fl denotes the smallest, › the largest) are given

for the day and night diel period of each habitat parameter

Habitat parameter Diel period v2 P-value W

Mean Ranks

YOY Juvenile Adult

Distance to shore day 17.3 0.001 0.788 1.2 fl 1.9 2.9 ›

night 7.1 0.029 0.322 1.4 fl 2.4 › 2.2

Mean depth day 13.3 0.001 0.603 1.3 fl 1.9 2.8 ›

night 5.2 0.076 0.235 1.5 fl 2.0 2.5 ›

Bottom profile day 0.9 0.643NS 0.040 1.8 2.1 › 2.1 fl

night 5.1 0.078 0.231 2.4 › 1.4 fl 2.2

Mean current velocity day 12.7 0.002 0.577 1.3 fl 1.9 2.8 ›

night 11.5 0.003 0.521 1.2 fl 2.5 › 2.3

Frequency of eddies day 6.2 0.045 0.282 2.3 › 2.3 › 1.4 fl

night 6.1 0.046 0.279 2.6 › 1.8 1.6 fl

Largest substrate day 1.6 0.441NS 0.074 2.0 1.7 fl 2.3 ›

night 1.6 0.441NS 0.074 2.3 › 2.0 1.7 fl

2006 STONE & GORMAN: HUMPBACK CHUB 129
Indications of humpback chub piscivorous activity.—While handling humpback chub captured

in nets set at night in 1993: (1) a 279 mm TL Gila cypha regurgitated a 47 mm TL conspecific

and defecated large quantities of incompletely digested fish parts; (2) a 237 mm TL G. cypha

regurgitated a speckled dace, parts of two unidentifiable fish and was bloated with other

fish; (3) a 176 mm TL G. cypha regurgitated a 48 mm TL conspecific; and (4) a 280 mm TL

and (5) a 187 mm TL G. cypha each defecated many fish bones and scales. During later LCR

fishery investigations, a 166 mm TL G. cypha regurgitated a 64 mm TL speckled dace (1 May

1999), a 372 mm TL G. cypha regurgitated a 60 mm TL fathead minnow (3 May 2003) and

a 156 mm TL G. cypha regurgitated a 57 mm TL conspecific (9 September 2004). The five

1993 observations occurred when small fishes were highly abundant, the three later

observations occurred when small fishes were less available. The observations of 156, 166

and 176 mm TL juvenile G. cypha regurgitating whole fish provided evidence that piscivory is

not restricted to adults.

During this study, we found 61 small fishes (30–90 mm TL) dead in the nets: 33

humpback chub, 23 speckled dace, 3 bluehead sucker, 1 flannelmouth sucker and 1

unidentifiable individual. Most mortalities (74%) occurred during the night when adult Gila

cypha were most active, 23% of all carcasses were found in nets also containing live adults

(13% for day vs. 27% for night), and many carcasses appeared masticated. Adult G. cypha

were not significantly associated with mortalities during the day (v2 1⁄4 1.282, P . 0.1) but

were at night (v2 1⁄4 4.468, P , 0.05). Juvenile G. cypha showed no association to small dead

fish (day v2 1⁄4 0.173, P . 0.5; night v2 1⁄4 0.600, P . 0.1).

The April and May sampling trips examined for catch rate patterns were separated by only

19 d in 1994 and 18 d in 1995 (Fig. 3). Whereas the mean catch rates of both YOY humpback

chub and speckled dace significantly declined from April to May in both years, the mean

FIG. 3.—Mean hourly catch rates (62 SE) of YOY (30–90 mm TL), juvenile (91–179 mm TL) and

adult (180–428 mm TL) humpback chub and speckled dace (30–90 mm TL) during April and May

sampling trips of 1994 and 1995 in the Little Colorado River, Arizona

130 THE AMERICAN MIDLAND NATURALIST 155(1)
catch rates of both juvenile and adult Gila cypha remained relatively stable between

adjacent trips in both years.

DISCUSSION

Our findings on the diel activity, habitat use, and association patterns of humpback chub

in the LCR mirror predator-prey scenarios described in other freshwater assemblages;

however, alternative hypotheses exists that cannot be refuted. The argument that adult Gila

cypha can be highly piscivorous deviates from the common perception of this species; for

example, fish are not even mentioned as a potential food item in the Humpback Chub

Recovery Plan (USFWS, 1990). Yet, if true, then this has important implications to future

recovery activities (e.g., translocations, exotic fish removals, food base issues) and, therefore,

is integrated throughout the ensuing discussion. Several dietary studies were conducted on

adult humpback chub in Grand Canyon that offer some pertinent background information.

Dissections of adult G. cypha digestive tracts (excluding empty specimens) uncovered fish

remains from 2 of 14 LCR specimens, but none from 13 Colorado River specimens in 1980–

1981 (Kaeding and Zimmerman, 1983), and 1 of 12 LCR specimens in 1985–1986 (Kubly,

1990). Stable isotope analyses of G. cypha trophic links in 1998–1999 indicated a dietary shift

that included piscivory by adults (via nitrogen enrichment) captured in both the LCR

(Benenati et al., 2002) and Colorado River (Shannon et al., 2001). Conversely, nonlethal

lavage of 168 Colorado River adults in 1991–1993 (Valdez and Ryel, 1997) and 45 in 1996

(Valdez and Hoffnagle, 1999) revealed no evidence of piscivory. All studies indicated that

adult G. cypha are opportunistic generalist feeders; however, evidence of piscivory was more

affiliated with G. cypha in the LCR than in the Colorado River.

The day vs. night catch rates of humpback chub revealed an ontogenetic diurnal-tonocturnal transition in locomotor activity. However, it may be more accurate to consider this

as an ontogenetic positive-to-negative transition in phototaxis because humpback chub show

less diel periodicity under high turbidities when light penetration into the water column is

reduced (Stone, 1999). Either way, YOY Gila cypha are more active during the day than at

night. Perhaps this is solely related to undeveloped sensory abilities; however, many YOY

G. cypha survive repeated flood events and successive months of extremely high turbidity,

which suggests that they possess sensory abilities other than eyesight (e.g., tactile, chemical

and electrical) that should allow for nocturnal activity. Thus, the diurnal activity of many

YOY G. cypha may be a behavioral response to avoid nocturnal encounters with adult conspecifics or other large-bodied fishes. Moreover, small-bodied speckled dace are also primarily

diurnal in the LCR (Stone, 1999), but are considered nocturnal in other systems (Sigler and

Sigler, 1987). Opposing activity patterns between predators and prey has been described in

other freshwater assemblages (Schwassman, 1971; Helfman, 1981; Bourke et al., 1996).

Subadult Gila cypha were most segregated from and least associated to adult conspecifics

during the daytime. Humpback chub from consecutively larger size classes occupied diurnal

habitats that were progressively further from shorelines, at greater depths and in faster

current velocities (Figs. 1b, c). The diurnal residency of adults in deep midchannel pools is

probably related to negative phototaxis (Stone, 1999), whereas the absence of smaller

conspecifics from these habitats may have been a behavioral response to reduce encounters

with adult G. cypha and other large fishes (Harvey and Stewart, 1991). Conversely, adult

G. cypha became much more active at night and dispersed from their diurnal habitats, whereby many individuals shifted inshore amongst the higher densities of smaller conspecifics.

Many YOY G. cypha shifted to larger substrates that provided greater cover for the night,

possibly, to seek refuge from inshore invading adults and other fishes, while many larger

juveniles shifted to more homogeneous bottom habitats, thereby leaving YOY and adults

2006 STONE & GORMAN: HUMPBACK CHUB 131
together in the more heterogeneous habitats. In an analogous assemblage, juvenile eastern

creek chub Semotilus atromaculatus and blacknose dace Rhinichthys atratulus used cover or

moved to avoid nighttime encounters with piscivorous adult creek chub (Fraser and Cerri,

1982; Cerri, 1983; Fraser and Emmons, 1984). The diel occupancy of YOY G. cypha to

nearshore habitats would allow them easy access of shallow depths and cover to seek refuge

from larger fishes (Sogard, 1994). Alternatively, numerous other hypotheses could be

generated to explain these patterns outside of any predator-prey framework.

Our findings from hoop nets indicate that Gila cypha can be piscivorous given opportunity,

but provide little insight into the degree of occurrence in the wild. Gila cypha piscivorous

activity may unnaturally escalate within hoop nets where fishes of different sizes are often

confined together. Most fish carcasses regurgitated by G. cypha appeared more masticated

than digested suggesting that they were consumed that night, probably while inside the nets.

Adult G. cypha likely killed many of the 61 small fishes found dead in nets, especially at night,

when they were most active and most mortalities occurred. Adults commonly escape these

nets overnight (Stone, 2005), which may explain nets containing dead carcasses but no

adults. During a different LCR investigation, we accrued no mortalities out of 9031 small fish

captured in 1588 Gee’s standard minnow traps, which excluded larger fishes. Conceivably,

the presence of small fishes within hoop nets may lure foraging adult G. cypha into the nets;

for example, hoop nets baited with processed hatchery feed (basically fish and meat

byproducts) captured over two fold more G. cypha than unbaited nets (Stone, 2005).

Some evidence of Gila cypha piscivorous activity in the wild does exists and suggests that this

may be a relatively common occurrence, especially in the LCR. The fish parts defecated by

G. cypha after being pulled from hoop nets probably belonged to fish consumed before the

nets were even deployed; for example, bonytail chub G. elegans retained fish material 45 h

after ingestion (Stone, 2004). The dissection studies conducted on adult G. cypha were of

individuals captured in gill and trammel nets, which exclude smaller fishes, yet fish remains

were detected in 11% of nonempty specimens from the LCR (Kaeding and Zimmerman,

1983; Kubly, 1990). The stable isotope signatures of adult G. cypha indicated a trophic shift

inclusive of piscivory from foods assimilated well before those adults were captured (Shannon

et al., 2001; Benenati et al., 2002). Adult G. cypha were observed preying upon YOY conspecifics

underneath an undercut bank in the LCR during 1994 (R. Van Haverbeke, pers. obs.). Largescale piscivory by adult G. cypha could explain the significant catch rate declines of YOY

conspecifics and speckled dace during the springs of 1994 and 1995 (Fig. 3). Those small

fishes survived through winter flood events to steadier spring flow regimes, but declined when

the greatest numbers of adult G. cypha were in the system to spawn. The LCR contains

a relatively depauperate invertebrate food base (Kaeding and Zimmerman, 1983; Oberlin

et al., 1999; Benenati et al., 2002) and insufficient food supply has been found to increase both

piscivory (Starrett, 1950) and cannibalism (Smith and Reay, 1991) in other systems.

Conclusions and conservation implications.—The cumulative evidence indicates that

humpback chub undergo an ontogenesis from diurnally active, vulnerable, nearshore-reliant

YOY into nocturnally active, large-bodied adults. Though adults can definitely be piscivorous

given the opportunity, the magnitude of their piscivorous activities is open for debate. Hoop

net sampling may escalate Gila cypha piscivory on smaller fishes; however, it may still be the

best gear to monitor and study fishes in the LCR. This gear is deployable in a wide range of

habitats and different river conditions, collects data on the entire fish community and

alleviates the potential of harming reproductively capable adult G. cypha with entanglement

(Hopkins and Cech, 1992) or electroshocking devices (Ruppert and Muth, 1997).

We doubt that any remedial actions focused solely within the lower 14 km of the LCR

could significantly improve humpback chub recruitment, especially while they continue to

132 THE AMERICAN MIDLAND NATURALIST 155(1)
numerically dominate the fish community. To reverse their population decline in Grand

Canyon, recovery efforts should focus on improving Colorado River conditions for the

survival and growth of YOY G. cypha that migrate there from the LCR. Their reliance on

nearshore habitats elucidates the need to eliminate diel discharge fluctuations from Glen

Canyon Dam. Otherwise, YOY G. cypha must continually vacate refuges, which increases their

exposure to piscine predators, or become stranded. However, these efforts would likely be

futile without modifying Glen Canyon Dam to release warmer water so that YOY G. cypha

could grow, become less susceptible to piscivory and, ultimately, recruit to adulthood. This

warmer water, stable flow regime should only be implemented in the late summer-early fall

when YOY G. cypha are most abundant in the Colorado River.

Acknowledgments.—We wish to thank J. Seals, Z. Zdinak and 19 other biologists for field assistance;

B. Burch and V. Meretsky for statistical support; S. Chubbuck for helicopter transport; J. Hanson, S. Leon

and B. Ralston for providing administrative support; and D. Blinn, L. Montgomery, J. Fowler-Propst,

B. Pine, J. Shannon, N. Taylor and two anonymous reviewers for remarks that greatly improved this

manuscript. Permits to conduct the research and handle endangered fish were provided by Arizona

Game and Fish Dept., Navajo Fish and Wildlife Dept. and U.S. Fish and Wildlife Service (Federal

Endangered Species Subpermit PRT-676811). Research was funded by the U. S. Bureau of Reclamation

under Contracts 1-AA-40-10480, 1425-96-AA-81-80013 and administered by D. Wegner. The views

expressed in this article are ours and do not necessarily represent those of the U.S. Fish and Wildlife

Service or other federal agencies.

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SUBMITTED 15 MARCH 2005 ACCEPTED 7 JUNE 2005

2006 STONE & GORMAN: HUMPBACK CHUB 135